Some Problems of Reproduction: a Comparative Study of ...

Some Problems of Reproduction: a Comparative 

Study of Gametogeny and Protoplasmic Senescence 

and Rejuvenescence. 

By 

Marcus JM. Hartog, M.A., I>.Sc, F.li.S., 

Professor of Natural History in the Queen's College, Cork. 

TABLE or 

t. Introductory 

Scope of Inquiry 

Bibliography 

Terminology and Notation . 

[I. Typical Agamic Reproduction 

Monadinete 

Myxomycetes . 

Acrasieae . . . . 

III. The Modes of Karyogamy, 

illustiatedchieflyfrom the 

Protophytes . 

1. Isogamy, multiple and 

binary 

(Euisoganiy, Exoisogamy) 

. 

2. Anisogainy . 

3. Hypoogamy . 

4. Oogamy 

5. Siphonogamy 

IV. Comparative Gametogeny in 

the Vegetable Kingdom . 

A. Protophytes and Cellular 

A l g a s . . . . 

PA&E 

3 

3 

5 

6 

7 

7 

7 

8 

8 

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9 

10 

10 

11 

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12 

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VOL. XXXIIIj PAET I. NEW SEE. 

CONTENTS. 

PAGE 

Cheetophoracese and Ulva- 

c e a j . . . . 

Ulothrix 

Cylindrocapsa 

Chlamydomonas 

Desmids, Conjugates, and 

Diatoms 

Volvox, Eudorina . 

Oedogoniacese 

(Beak formation compared 

with that of 

zoosporange in Chytridiese 

and Saprolesniece) 

Coleochtetece . 

Melauophycea; 

Fucacese 

B. Apocytial Forms 

1. Green or Algal Types . 

Cladophora 

SipllOUCEB . 

Sphteroplea 

Vauclieria . 

12 

12 

13 

13 

13 

14 

14 

15 

16 

16 

16 

17 

17 

17 

18 

19 

20

PAOE 

2. Colourless or Fungal 

Types . . .20 

a. Phycomycetes zoosporete 

. . . 20 

Ancylistese . . 20 

Chytridieee (Olpidiopsis,Polyphagus,Zygochytrium,Tetrachytrium) 

. . .21 

Monoblepharis . 22 

Peronosporese. . 22 

Saprolegniese . . 23 

b. Phycomycetes aplanosporem 

. . 26 

Entomophthorete . 26 

Basidiobolus . . 26 

Mucorini . . 27 

c. Higher Fungi . . 28 

Lower Ascomycetes 28 

Lichens . . .28 

Higher Ascomycetes, 

Basidiomycetes . 28 

Ustilaginese . . 28 

Protomyces . . 29 

Uredinea; . .29 

C. Higher Thallophytes . 29 

1. Floridere . . . 29 

Bangiacese . . .30 

Eufloridete . . .30 

(Secondary fertilisation) 

. . .31 

Corallina . . 31 

2. Characeee . .32 

D. Archegoniata . . .32 

1. Muscineas . . .32 

2. Vascular Cryptogams . 34 

E. SiphonoganiEe (Phanerogams) 

. . .35 

1. Gymnosperms . . 35 

Male structures (pollen 

and pollen tube) . 35 

Archegonia . .35 

MAJROtJS M. HAETOG. 

PAOE 

2. Angiosperms . . 36 

Male structures (pollen 

and pollen tube) . 36 

Cell formations in embryo-sac 

. . .37 

Cellular morphology of 

mature embryo-sac . 40 

V. Comparative Gametogeny in 

the Animal Kingdom . 41 

A. Protozoa. . . .41 

1. Flagellata . . . 41 

Euflagellata . . 41 

Cystoflagellata (segmentation 

of zygote 

in Noctiluca) . . 41 

2. JELhizopoda and Heliozoa 42 

3. Gregarinida (Ophryocystis, 

Monocystis) . . 42 

4. Hadiolaria . . . 43 

5. Ciliata . . . . 43 

Free Ciliata and Suctoria 

. . .43 

Vorticellinea . . 47 

B. Metazoa . . . .48 

1. Spermatogeny . . 48 

First mode. . .48 

Second mode . . 49 

Third mode . . 49 

2. Oogeny . . . 50 

Peculiarities of mature 

ovarian ovum or 

Gametogonium . 50 

First nuclear changes . 51 

Gametogenic fissions 

(formation of Oosphere 

and Polar 

Bodies) . . . 52 

"Parthenogenetic ova" 

of the Metazoa . 53 

VI. A General View of Gametogeny 

. . . .54 

A. The Reduction of the Chromatom 

eres in Gametonuclei 54

SOME PROBLEMS OP REPRODUCTION. 

B. The Reproductive Incapacityof 

Obligatory Gametes 5 8 

C. The Adaptation of Gametes 

to different Fates . .59 

D. Analytic Summary of Gametogenic 

Processes . 60 

(Alleged Excretion Proceases) 

. . .62 

VII. The Causes of Protoplasmic 

Senescence and Ultimate 

Reproductive Incapacity 64 

VIII. Protoplasmic Rejuvenescence, 

its Nature and 

Modes. . . .67 

I. INTRODUCTORY. 

PAGE 

A. The Modes of Rejuvenescence. 

. . . G7 

B. The Advantages of Karyogamy 

as compared with 

Agamy and Apogamy . 68 

C. Allogamy and Sex . . 70 

D. The Origin of Sex . . 72 

E. Paragenetic Processes, 

usually comprised under 

the term " Parthenogenesis 

" . . .73 

IX. General Conclusions 

THE curiouB phenomena preceding the maturity of the 

ovum in Metazoa have been the object of much study and the 

groundwork of much theory during the last fifteen years. 

Unfortunately processes occurring in this highly specialised 

group have been assumed to be typical of all organisms ; the 

authors who have put forward explanations of what they have 

seen here have too often sought to extend these explanations 

to other groups, where the facts are different; they have 

created homologies where none such exist in Nature, and overlooked 

those which lay under their eyes. In this way protoplasmic 

changes of various origin and functions occurring in 

Protozoa, Protophytes, and Higher Plants, have been interpreted 

as excretory processes, in order to make them fit in 

with the replacement theories of fertilisation, founded almost 

exclusively on the formation of the polar bodies in the 

Metazoan ovum. 

A careful study of the accessible materials in the gigantic 

storehouse of facts bearing on this subject has led me to the 

views which will be found in the following pages, namely : 

(1) That the most general, but not universal, feature underlying 

the preparations for fertilisation is the specialisation

SOME PROBLEMS OP REPRODUCTION. 

B. The Reproductive Incapacityof 

Obligatory Gametes 5 8 

C. The Adaptation of Gametes 

to different Fates . .59 

D. Analytic Summary of Gametogenic 

Processes . 60 

(Alleged Excretion Proceases) 

. . .62 

VII. The Causes of Protoplasmic 

Senescence and Ultimate 

Reproductive Incapacity 64 

VIII. Protoplasmic Rejuvenescence, 

its Nature and 

Modes. . . .67 

I. INTRODUCTORY. 

PAGE 

A. The Modes of Rejuvenescence. 

. . . G7 

B. The Advantages of Karyogamy 

as compared with 

Agamy and Apogamy . 68 

C. Allogamy and Sex . . 70 

D. The Origin of Sex . . 72 

E. Paragenetic Processes, 

usually comprised under 

the term " Parthenogenesis 

" . . .73 

IX. General Conclusions 

THE curiouB phenomena preceding the maturity of the 

ovum in Metazoa have been the object of much study and the 

groundwork of much theory during the last fifteen years. 

Unfortunately processes occurring in this highly specialised 

group have been assumed to be typical of all organisms ; the 

authors who have put forward explanations of what they have 

seen here have too often sought to extend these explanations 

to other groups, where the facts are different; they have 

created homologies where none such exist in Nature, and overlooked 

those which lay under their eyes. In this way protoplasmic 

changes of various origin and functions occurring in 

Protozoa, Protophytes, and Higher Plants, have been interpreted 

as excretory processes, in order to make them fit in 

with the replacement theories of fertilisation, founded almost 

exclusively on the formation of the polar bodies in the 

Metazoan ovum. 

A careful study of the accessible materials in the gigantic 

storehouse of facts bearing on this subject has led me to the 

views which will be found in the following pages, namely : 

(1) That the most general, but not universal, feature underlying 

the preparations for fertilisation is the specialisation

4 MABCUS M. HARTOG. 

of gametes by rapidly repeated divisions of a cell—the 

gametogonium; 

(2) That the alleged nuclear excretions in the Metazoan egg 

and the Ciliate " gamete/' &c, represent true gametes arrested 

in their development; 

(3) That the so-called "excretions" of protoplasm in plants 

are of various kiuds, many of which are homologous neither 

with the former process nor with one another; 

(4) That the use of the rapid preliminary divisions is a 

purely physiological one; that is, to induce by exhaustion 

the same reproductive incapacity that would otherwise 

require a long series of slowly repeated divisions. 

On these lines we can account for all the facts, from the 

simplest cases of the formation of isogametes to the most 

peculiar phenomena of oogeny and spermatogeny; phenomena 

which the sexual replacement theories of Minot, Balfour, and 

van Beneden, on the one hand, and the more complex replacement 

theory of Weismann, on the other, only profess to 

explain in the higher groups. The views here put forward 

are essentially a development and extension of what we may 

term the "morphological theory" of polar bodies, first enunciated 

by Giard, Biitschli, Whitman, and Mark, 1 and advocated 

especially by the Hertwigs. It will not seem strange that 

this view has never had full justice done it when we reflect 

that it is to men who have worked especially at the Metazoa 

that we owe the greatest debt for shaping our biological 

theories; and that our gratitude has, perhaps, led us to be 

too unquestioning in our attitude of discipleship to such respected 

masters as Balfour, van Beneden, and Weismann. 2 

The exposition of the processes of gametogeny naturally leads 

1 

Mark was the first definitely to express the view that the polar bodies 

represent abortive ova ; see " Maturation, Fecundation, and Segmentation of 

Limax campestris," in 'Bull. Mus. Comp. Zool. Harv. Coll./ vol. vi, 1881. 

2 

I may say that 1 never doubted that some replacement theory of 

fertilisation was sufficient to cover the facts, till I read and meditated over 

Maupas's account of the conjugation of the Ciliata ; and this it was that first 

weakened'my belief, not only in replacement theories, but also in the " preliminary 

excretion " theory on which the others were founded.

SOME PROBLEMS OF REPBODUOTION. 5 

on to a consideration of the causes of the individual reproductive 

incapacity of most gametes; of the senescence of the 

individuals produced in the later generations of a long cycle of 

fissiparous reproduction ; and conversely of the rejuvenescence 

induced by karyogamy and other processes, which are classified 

and discussed. A special section is devoted to those modes of 

rejuvenescence which have been confounded under the name 

of " parthenogenesis/' but which we may term " paragenetic;" 

and a general summary of conclusions closes the present 

study. To keep the exposition clear and continuous I have 

abstained as far as possible from controversy. 

I wish to express my thanks to Professors Mark, G-uignard, 

Strasbiirger, and Weismann for their communication of 

reprints of valuable papers not otherwise readily accessible 

to me. 

I have not deemed it necessary to give references for facts to 

be found in every text-book, though I have verified as far as 

possible every statement from the original authorities. In all 

other cases I have cited my authority in a foot-note. 

The following is a list of the text-books and papers of general 

interest to which I may refer the reader. 

BOOKS— 

'Essays upon Heredity and Kindred Problems,' Weismann (Engl. 

Trans.), 1889. 

' Evolution of Sex,' Geddea and Thomson, 1890. 

' Studien iiber Protoplasmamechanik,' Berthold, 1886. 

' Handbuch der Botanik,' Scbenk (in progress). 

' Pflanzenfamilien,' Engler and Prantl (in progress). 

t Fungi, Mycetozoa, and Bacteria,' De Bary (Engl. Trans.), 1887. 

' Physiology of Plants,' Vines, 1886. 

1 Befruchtung und Zelltheilung,' Strasbiirger. 

' Neuere Untersuchungen,' Strasbiirger, 1884. 

' Protozoa' (in Bronn's ' Tkierreich'), Butschli. 

' Comparative Embryology,' Balfour, 1880. 

'Introduction to the Study of Embryology,' Haddon, 1887. 

'Traite" d'Embryologie' (Ed. Pr.), 0. Hertwig, 1891. 

'Forms of Animal Life,' Rolleston and Hatohett Jackson, 1888.

6 MARCUS M. HARTOG. 

MEMOIRS— 

"Sur la Multiplication des Infusoires cilies," Maupas, in 'Arch, de 

Zool. Exp.,' 1888. 

"Le Rajeunissement karyogamique chez les Cili6s,' Maupas, in 'Arch. 

de Zool. Exp.,' 1889. 

" Karyokinesis and Fertilisation," Part II, Waldeyer (Engl. Trans.), 

in ' Quart. Journ. Micr. Sci.,' Dec, 1889. 

" Vergleicli der Ei- und Samenbilduug bei Nematoden," 0. Hertwig, in 

'Arch. f. mikr. Anat.,' vol. xxxvi, 1890. 

In my terminology I have used the word gamete to designate 

a cell which fuses with another, cytoplast with cytoplast and 

nucleus with nucleus, and zy gote for the cell produced by their 

union; pronucleus and gametonucleus, indifferently, to 

denote the nucleus of a gamete, without any connotation of 

imperfection; gametogonium and progamete to express, 

from slightly different points of view, a cell which divides to 

form gametes or (rarely) passes into the state of a gamete; 

spermatogonium 1 and oogonium, spermatogamete and 

oogamete for male or female gametogonia and gametes 

respectively: facultative and obligatory gametes are discriminated 

according as they retain the primitive cell privilege 

of multiplying by fission (independent of karyogamy) or 

have lost it altogether. I use the phrase gametangium for 

the apocytial chamber in which gametes are developed. Cytoplast 

designates the cytoplasm considered as a unit in contrast 

to the nucleus. 

By apocytium I mean a mass of protoplasm which is 

habitually plurinucleate, cell division remaining in abeyance; 

apocytial plants may be continuous; or septate by 

partitions, which always, however, separate multinucleate 

masses of protoplasm. Apocytial structures which unite 

like gametes are termed gametoids, and the product of 

their union a zygotoid. I have freely used Maupas's admirable 

term karyogamy to comprise all forms of union of 

gametes involving fusion of their nuclei, since fertilisation 

and fecundation are altogether inappropriate to cases of 

1 

Corresponding with the " spermatospore " of Blomfield, not necessarily 

the " spermatogonium " of La Valette St. George.

SOME PROBLEMS OP REPRODUCTION. 7 

isogamy. By endogamy I imply the union of gametes from a 

single gametogonium, by exogamy their union with those 

from other oogonia exclusively. Portions of the nucleated 

or non-nucleated protoplasm, left out in schemes of gametal 

formation, are termed epiplasm. I have found it useful to 

introduce the following notation to denote relationship among 

nuclei, viz. to use a given letter for the parent nucleus, and the 

same letter with that figure as an index which denotes the 

number of bipartitious that have taken place, to denote a 

brood-cell issuing from those bipartitions; thus if N be a 

nucleus, N 5 will denote a brood nucleus of the 5th bipartition 

of N; the notation is abbreviated, N" denoting N-r-2 a . 

II. TYPICALLY AGAMIC REPRODUCTION. 

Before examining into gametogeny we must note the-existence 

of a group of organisms which appear to be essentially 

agamous. I refer to that of MYCETOZOA, including the 

Monadineae of Cienkowsky, the Acrasiese, and the Myxomycetes 

proper. 

In the MONADINEJE, a group relegated with exceptional 

liberality by the zoologists to the botanical " sphere of influence," 

we have a very primitive group, most species having 

the three forms of Mastigopod, Myxopod, and Cyst, beside a 

Resting Stage, which is never preceded by karyogamy. The 

adult forms may become plurinuclear or fuse into plasmodia 

like the Myxomycetes, but no nuclear union takes place; 

nay, even in the plasmodia further nuclear divisions may 

occur. 

In the true MYXOMYCETES, plasmodial fusion always precedes 

spore formation. Possibly, as has often been suggested, plasmodial 

formation has led to the various modes of karyogamy. 

The nuclei pass freely from place to place in the plasmodium, 

and may eventually be far removed from what was their original 

cytoplast; and the cytoplastic elements again undergo a 

reorganisation by their fusion, which we may term plastogamy. 

In this way is fulfilled what I regard as the object


also of karyogamy—the association of nucleus and cytoplast 

that are strangers to each other. 

"We may fairly adopt the view that multiple isogamy, where 

the fusion of the nuclei follows that of the cytoplast, was originally 

derived from plasmodial formation, and that binary 

isogamy and the higher forms of karyogamy are further stages 

in the upward path. 

In the AcRASiEiEj the individuals produced by fission simply 

aggregate together without fusioD before passing into a resting 

state, as a fructification in which their cellular individuality 

is retained. The only explanation I can suggest for this is 

that it indicates the loss of a primitive formation of plasmodia 

at this stage; the Acrasieas would be an apoplasmodial or 

apoplastogamous group, a degenerate offshoot of the M y x o m ycetes. 

III. THE MODES OF KARYOGAMY AS ILLUSTRATED IN 

PROTOPHYTES. 

Undoubtedly the lowest forms of life that present us with cases 

of karyogamy are the FLAGELLATES ; and in the PHYTOMAS- 

TIGOPODS or Green Flagellates we may study its modes from 

isogamy to complete sexual differentiation. From the colonial 

Phytomastigopods we can trace an almost unbroken line upwards 

past the Thallophytes, which in their asexual reproduction 

so often revert to the lowly Flagellate type ; up through 

the Archegoniata to the Gymnosperms and true Flowering 

Plants at the top of the scale. We distinguish the following 

modes of karyogamy :—(1) ISOGAMY—(a) EUISSGAMY, (b) 

EXOISOGAMY ; (2) ANISOGAMY ; (3) HYPOOGAMY ; (4) OOGAMY. 

(1). ISOGAMY.—This is the simplest mode of karyogamy. In 

this process cells exactly similar fuse as gametes, cytoplast to 

cytoplast, nucleus to nucleus; a single nucleated cell, the 

zygote, being the produce. In most cases only two gametes 

unite in binary isogamy; more rarely three or more may 

fuse in multiple isogamy. In many of the Phytomastigopods, 

and some of those simple filamentous or thalloid Algse that


seem hardly more than colonies of Phytomastigopods in the 

resting state, such as Aigse Confervoidese, and such apocytial 

forms as Cladophorese and many Siphonese, in 

these I say the gametes differ in no appreciable respect from 

the ordinary swarmers or zoospores, save that they are often 

smaller; they are usually formed by the segmentation or 

rapidly-repeated binary fission of the cell-body of the 

gametogonium. In some cases these isogametes, failing 

conjugation, may develop like ordinary zoospores; they are 

facultative 1 gametes; but in most cases they have lost this 

power of independent growth, and are obligatory gametes. 

In some cases all the vegetative cells assume the character 

and function of gametogonia; in other cases we may distinguish 

clearly between " brood cells " (gametogonia or zoosporangia) 

on the one hand, and " colonial" or vegetative cells 

on the other. 

Apart from other differentiations we may discriminate two 

grades of isogamy, which we shall term (a) EUISOGAMY, (b) 

ExOISOGAMY. 

(a) In EUISOGAMY, each gamete has the power of uniting 

with the other, irrespective of its origin ; nay, in some cases, 

as in Pediastrese, the gametes of a single gametogonium 

habitually conjugate with one another, thus forming endogatnous 

unions. 

(b) In EXOISOGAMY, a gamete will not conjugate with another 

of the same brood, but will only mate with one from a different 

gametogonium at least. This phenomenon would be difficult 

to demonstrate in the free Flagellates; but it occurs in some 

of the lowest Confervoidp, such as Ulothrix. In this genus 

the gametes, facultative though they be, are strictly exogamous. 

In the Vjjlvocine Pandorina the gametes of different broods 

vary in size, and the small and middle-sized ones will pair indifferently 

with one another, quite independently of their size, 

but on the condition that the two gametes belong to distinct 

broods. About the largest gametes there is some doubt. 

1 I believe De Bary first introduced tbe terms ' facullative' and 'obligatory 

' in treating of parasitic fungi, &o.


Among the marine Siphonese, Dasycladus evinces a yet 

more subtle difference; for Berthold has shown 1 that the 

gametes of one brood may refuse to pair, not only with one 

another, but also with gametes of certain other plants, while 

they do so with others; and yet he failed to make out any 

distinguishing character in the plants themselves. 3 

(2) ANISOGAMY.—This is the second stage of karyogamy, 

where the gametes are similar in form, but of two sizes, large 

and small respectively; and in their union a micro- always 

pairs with a mega-gamete. This maybe regarded as the 

lowest form of sexual differentiation, the smaller more active 

microgamete being the male, the larger more passive megagamete 

the female. Exogamy is a necessity here, for each 

brood is all of one kind, large or small, as the case may be. 

If the gametogonia do not show a corresponding difference 

of size (which they do sometimes), the differentiation of the 

gametes is effected by the smaller number of bipartitions in 

the segmentation which produces the megagametes. Thus in 

Chlamydomonas pulvisculus the megagametes are produced 

in twos or fours, the microgametes in eights. 

We shall note below the transitional conditions between 

isogamy and anisogamy presented by the genera Ulothrix 

and Pandorina. 

(3) EhrpooGAMYor HYPERANISOGAMY.—This is our third stage, 

recognised but not named by previous writers. The gametes 

are similar, but differ not merely in size but in behaviour; 

for the megagamete absolutely goes to rest before the microgamete 

comes to unite with it. This process occurs in slightly 

different modes in two of the lower groups of Olive Seaweeds, 

Cutleriacese and Ectocarpese. The Ectocarpese are 

remarkable for the fact that their microgametes, as well as the 

megagametes, are facultative, or capable of independent 

1 'Botanische Zeitung,' 1880, 648. Possibly the explanation is that the 

ultimate offspring belonging to the same cycle derived from a single zygote 

will not conjugate together any more than they will in certain Ciliate 

Infusorians; and that the individuals that showed this mutual sexual 

incapacity had this blood relationship.

SOME PROBLEMS OF REPRODUCTION. 11 

growth failing conjugation, though the microgametes, indeed, 

are said to form but weakly plants. We know of no other 

case where a well-differentiated male cell retains this power 

of independent growth or parthenogenesis in the strictest 

sense. 

(4) OOGAMY.—This term has been freely applied to cases 

of anisQgamy and hypoogamy. It is, however, better restricted 

to those cases in which the megagamete is neither ciliate nor 

flagellate, but motionless, or at the outside slightly amoeboid; 

while the microgamete or spermatozoon is most frequently a 

free-swimming cell, and consequently retains its primitive 

mastigopod form in the majority of cases, including the highest 

Metazoa. The megagamete is usually termed an ovum or egg 

in animals; but there are profound differences, morphological 

and physiological, between the immature metazoon egg as a 

progameteandtheegg after the expulsion of the polar bodies 

as a true gamete; and I shall henceforth designate the egg 

in this latter stage an "oogamete" or "oosphere," reserving the 

words "egg" and "ovum" loosely for all stages. 

In most cases of oogamy the microgamete is very minute, 

reduced to a " resting" nucleus, with just enough cytoplasm 

to cover it and carry it up to the oosphere. This reduction in 

size finds a curious parallel in the reduction of the male 

Rotifer, a bag with sexual organs, and just enough other 

organs to enable him to find and fertilise the female, the organs 

of nutrition being completely absent. 

The lowest oogamous groups are certain Volvocinere 

belonging to Phytomastigopods, and the Confervoid genera 

(Edogonium and Cylindrocapsa. 

(5) SIPHONOGAMY,—Yet another mode of reproduction has 

to be noted, combined with any of the preceding, that where 

the gametes reach and unite, not by ordinary locomotion and 

as naked cells, but by a protoplasmic outgrowth of the gamete 

or gametogonium, protected by a cellulose tube. This is teimed 

SIPHONOGAMY by Engler; it is a mere distinction ia the 

mechanism of karyogamy, for it is associated with isogamy 

in some Conjugatae, anisogamy in others of this group and


Chlamydomonas pulvisculus, with oogamy in the Peronosporese, 

and in Gymnosperms and Flowering Plants. 

IV. COMPARATIVE GAMETOGENY IN THE VEGETABLE 

KINGDOM. 1 

I propose now to examine, as completely as materials will 

allow, the types of the modes in which gametes are differentiated 

in the vegetable kingdom, from the Protophytes 

upwards. I have not followed any published classification; 

nor have I aimed at absolute completeness in examples, but 

only in types. 

A. PROTOPHYTES AND CELLULAR ALGJE. 

Many of the lower types have been treated incidentally in 

the foregoing section, and I need not revert to them. In 

CH^TOPHORACEJE and ULVACE^; the zoospores are frequently 

4-flagellate, the isogametes 2-flagellate. This would seem to 

indicate that the segmentation which would otherwise have 

formed zoospores has been pushed a stage further in the formation 

of gametes, i. e. that the gametes are formed by the 

bipartition of the nascent zoospores. Multiple union is not 

rare in this group. In several members the conjugation of 

what are supposed to be gametes has not been observed, but 

their nature is a matter of inference from comparison with 

allied forms ; possibly these doubtful gametes are exogamous, 

and could find no suitable mates in the specimens under 

observation. 

To ULOTHRIX I have referred above (p. 9). The formation 

of zoospores and gametes is peculiar : the nuclear divisions are 

completed before the cytoplasm divides; the vacuole becomes 

excentric and peripheral, surrounded by a layer of cytoplasm 

which takes no share in the divisions of the rest of the proto- 

1 

I have not confined myself strictly to gametogeny, but have described 

the formation and fate of the zygote wherever it was necessary for the elucidation 

of the true character of the gametes.

SOME PflOBLEMS OF REPRODUCTION. 13 

plasm which form the zoospores or gametes ; and the vesicle 

so formed persists and is usually expelled with them. But this 

formation does not always take place, and no share is taken 

by the nucleus in it. A similar vacuolar bladder is formed in 

certain Siphonese. The zoospores vary in number, owing to 

the number of nuclear bipartitions that produce them; the 

smallest (of several sizes, however) and most numerous conjugating 

exogamously as (facultative) isogametes. Dodel-Port 

relates 1 that he has seen copulation between small active 

swarmers and larger more sluggish ones, though they usually 

conjugate with those of the same size. So that we have here a 

combination of isogamy and anisogamy. 

CYLINDROCAPSA is oogamous. The oosphere is formed 

simply by the enlargement of a single cell, and is facultative. 

The sperm atogonia are formed by the rapid transverse fissions 

of the vegetative cells; and the cell-body of each divides to 

form two spermatozoa. 

CHLAMYDOMONAS PULVISCULUS, referred to above as anisogamous, 

shows a transition to the siphonogamy of the 

group we shall next examine, for the gametes come to rest, 

surrounded each with a cell-wall, and the microgamete 

" creeps " into the cell-chamber of the megagamete to fuse 

with it therein. 

The DESMIDS, CONJUGATES, and DIATOMS are forms permanently 

enclosed in their cell-walls, and destitute of cilia or 

flagella, never even forming zoospores. In these conjugation 

is altogether isogamous, or in certain Conjugates (Spirogyra) 

the male is only distinguishable by its slightly smaller 

size, and by passing, like that of Chlamydomonas pulvisculus, 

into the megagamete cell-chamber to form the zygote 

therein. In other cases siphonogamy also occurs, but the 

zygote is formed at the junction of the tubes emitted by the 

isogametes. In Diatoms the gametes leave their shells to 

conjugate as naked cells. 

In the Desmid Closterium lunula and certain Diatoms 

1 "Ulothrix zonata," in 'Pringsheim's Jahrbiiclier,' vol. x, 1876, 

p. 539.

14 MAKO[JS M. HAETOG. 

(Epithemia, Amphora) two cells (so-called "frustules") 

approach as " progametes," and division takes place in each ; 

and their offspring conjugate two and two, in the young state 

consequent on recent fission. 

In the Conjugate Sirogonium the gametes are somewhat 

unequal, and are separated by septa from sterile cells; the 

male is formed from the vegetative cell by the marking off of 

two sterile cellsj one on either side, the female by marking off 

of a single sterile cell. 

Facultative gametes occur in all divisions of this group, or 

rather a vegetative cell, instead of assuming the character of a 

gamete, assumes that of the zygote, constituting the azygospore 

of De Bary. 

In the genus VOLVOX a colony is formed by the segmentation 

of a single reproductive cell; at an early stage of this 

process certain cells undergo no further division, though they 

continue to increase in size. These large cells may behave as— 

(1) Parthenogonidia, which after the maturity of the 

colony begin segmenting on their own account to reproduce a 

fresh colony; (2) " Oogonia," which on their maturity, without 

further division,assume the character of oospheres; "Spermatogonia" 

which at maturity undergo rapid segmentation 

and are resolved into the numerous spermatozoa, which 

are biflagellate like the colonial cells. EUDOBINA, another Volvocine, 

is auisogamous, the megagametes being flagellate. 

All the cells of the sexual colonies are fertile, either all becoming 

spermatogonia and segmenting into spermatozoa, or all 

assuming directly the function of oospheres. 1 

The Confervoid OEDOGONIACE^E are also oogamous. Here, 

on the bipartition of a vegetative cell, the one daughter-cell 

enlarges to form the oosphere, the other is sterile. We may 

perhaps regard the latter as a gamete arrested in its development. 

The apical protoplasm of the oosphere grows upwards at 

one side pushing the cell-wall into a short beak, soon perforated, 

or merely forms a hole at this point. The cytoplasm con- 

1 

The case of Pandoriua will be treated below, p. 72.


cerned in this process degenerates into mucus, while the rest 

rounds off, awaiting fertilisation. This process is obviously a 

purely adaptive one, destined merely to favour the approach 

and entrance of the spermatozoon. 

Similar " excretions " occur elsewhere for similar purposes; 

thus in Peronosporese, Saprolegniese, and Chytridiese 

the asexual zoosporange forms a beak for the discharge of the 

zoospore; in Chytridiese the protoplasm which fills this beak 

undergoes degeneration; while in. Saprolegniese it is retracted 

and absorbed into the body of protoplasm not yet fully 

differentiated into zoospores. In the Chytridian Woronina 

polycystis, which I have studied myself, the formative protoplasm 

of the beak contains a nucleus, and appears to be a 

zoospore degraded for the purpose of opening a gate to its 

sisters. 1 Hence neither physiologically nor morphologically 

can excessive stress be laid on such a degradation, whether of 

cytoplasm or nucleated protoplasm. 

The spermatogonia of Oedogonieae are formed by repeated 

bipartitions of the vegetative cells, and are short and 

discoid. In each spermatogonium the protoplasm rounds off 

and divides to form two naked spermatozoa; or this division 

is suppressed, and the protoplasmic body of the spermatogonium 

escapes as a single spermatozoon. The spermatozoa 

have, like the asexual zoospores, a subapical ring of cilia, but 

are smaller. In certain species the discoid cells produce not 

spermatozoa, but so-called " androspores," of similar character 

but of different fate. For the androspores settle on the base 

of the oogonial cell-wall and develop into " dwarf male" 

plants; all the cells of these (save sometimes a sterile basal 

cell) are spermatogonia, and behave like the same organs in 

the other species. This is the first case in which we find sex 

anticipated by or reflected back upon individuals or 

organs antecedent to the gametogonia. 2 

1 

As stated by me in a communication to Section D of the British Association 

at Leeds, 1890, Report, p. 872. 

2 

The colonies of Eudorina and some forms of Volvox only produce 

gametes of one sex, but have no other peculiarity to distinguish them.

16 MAECUS M. HARTOG. 

COLEOCHJETE^: are also oogamous; the oosophere essentially 

resembles that of Oedogoniese, but it is the direct transformation 

of a superficial tissue-cell: its fertilising beak is 

prolonged into a slender tube open at the apex, the "Trichogyne;" 

the formative cytoplasm contained therein degenerates 

as in Oedogoniese, while the rest of the protoplasm 

in the body of the oogonium rounds off into the oosphere. 

The spermatogonium undergoes two binary divisions, and 

the cell-body of each of the cells so formed escapes as a biflagellate 

spermatozoon. In certain species the four daughtercells 

of the spermatogonium are budded off at its apex, and 

though no information has been given we may well believe 

the process to be that following as found in the spore formation 

of Basidiomycetes. The nucleus of the basidium divides 

by two mitoses, and each of the four nuclei so formed migrates, 

accompanied by cytoplasm, into a bud formed at the apex, 

which becomes shut off by a septum from the now sterile and 

enucleate basidium. 1 That we are fairly justified in interpreting 

budding here as a modification of segmentation is obvious when 

we reflect on the behaviour of meroblastic ova or the zygote 

of Noctiluca (infra, p. 41) in their segmentation. 

In the MELANOPHYCEJE, or Olive Seaweeds, we have seen the 

transition from isogamy through anisogamy to hypoogamy. 

True oogamy occurs in the highest order of this group, the 

FUCACEJE. 2 In these the oogonial nucleus divides by successive 

mitoses into eight gametonuclei. In Fucus each of 

these attracts round it one eighth of the cytoplasm, so that 

there are eight oospheres. In Ascophyllum four of the 

nuclei pass to the centre, and four lie at equal distances nearer 

the surface of the cytoplasm.' The cytoplasm aggregates 

around the four peripheral nuclei to form four oospheres, 

leaving the four central nuclei as rejection-bodies in the 

1 

Possibly, however, the formation may take place as in the Meridian genus 

Chondria (infra, p. 30). 

* The following account is taken from Oltmanns' " Beitrage zur Vergleich. 

Entwieklungsgesch. der Fucacese," in ' Sitzungsber. d. Berlin Akad.,' 1889, 

p. 587.

SOME PROBLEMS OF BEPBODUCTTON. 17 

centre. In Pelvetia six of the nuclei pass towards the 

equator of the oogonium, and two lie towards the ends of 

its axis. The cytoplasm separates into two oospheres, each 

containing one of the axial nuclei, while the six equatorial 

nuclei are left out as rejection-nuclei. Finally, in Halidrys 

and Himanthalia, and also Cystoseira, seven of the 

nuclei pass to the periphery as rejection-nuclei, while the 

eighth remains in the centre of the cytoplasm of the oogonium 

which is thus directly resolved into the single oosphere. 

Oltmanns, who gave the first correct account of these processes, 

rightly remarked on their close identity with the formation 

of polar bodies in the Metazoa. It is obvious that the 

formation in Fucus is primitive, and that the advantages due 

to the increased size of the oospheres in the other genera 

are obtained by the abortion of half, three quarters, or seven 

eighths of them, and that this physiological advantage is a 

relative gain and not an absolute necessity. 

B. APOCYTIAL FORMS. 

1. Green or Algal Types. 

CLADOPHORA has septate filaments with many nuclei in each 

joint, and forms zoospores, ordinary or isogametal, by the resolution 

of these apocytia into uninucleated swarmers. In both 

cases a portion of the cytoplasm is eliminated at the boundaries 

of these cells, and takes no further part in the living processes. 

From Berthold's description 1 it appears certain that 

he is correct in regarding this excretion of " epiplasm" as 

derived from a primitive formation of cell-wall, a process 

which has been lost in the evolution of the group. We may 

note that this confirms the propriety of our using Vuillemin's 

term "apocytial" instead of Sachs' "non-cellular." 

The gametes of Cladophora are biflagellate, the ordinary 

zoospores quadriflagellate, a distinction which we interpret as 

1 

Op, cit., p. 302. He expressly notes (p. 305), in opposition to Dodel- 

Port, that such formations, occurring also in asexual spore-formation, can have 

no relation to fertilisation-processes as such. 

VOL. XXXIII, PAET I.—NEW SER. B


indicating the formation of the gametes by a binary fission of 

potential zoospores. 

The SIPHONED form continuous apocytia, parts of which may 

become partitioned off as gametangia. 

ACETABULARIA and BOTBYDITTM are exo-isogamous; their 

gametes are formed in gametogonia, which are formed by the 

resolution of an apocytium into cells, and have the character 

of resting spores. The gametogonium is at first uninucleate, 

at least in Botrydium, judging from the original figure, 1 

and must become plurinucleate before being resolved into the 

gametes. In that of Acetabularia the protoplasm surrounds 

a central vacuole, and the cytoplasm immediately round this 

persists without taking any part in the gametoparous segmentation, 

but serves by its turgescence to liberate the gametes. 

These are exogamous, and in Acetabularia may form multiple 

unions—two to six. 2 

BRYOPSIS is anisogamous. Here gametangia are cut off, 

males and females being on distinct plants. According to 

Berthold, repeated bipartitions of the nuclei precede the resolution 

into gametes. There is a formation of epiplasm between 

the gametes, as in Cladophora, besides a central bladder, as in 

Acetabularia. The reproductive organs of Codium appear 

to be similar in most respects. 

DASYCLADUS forms its gametes also by the resolution of an 

apocytial gametangium into cells ; but here a fusion of several 

vegetative nuclei constitutes each single gametonucleus, a process 

of which we shall find other instances in this group. We 

now learn that the view that a gametonucleus or pronucleus 

differs from an ordinary one in being reduced either by preliminary 

mitosis or " excretion" expresses no universal law. 

We have adverted above to the peculiarly strong exogamy 

of this genus. 

In DERBESIA it is stated 8 that no sexual process is known; 

1 

Of Rostafinsky, in ' Bot. Zeit.,' 1877. 

s 

If the gametogonia be kept long in a resting state, the bodies they produce 

behave like ordinary zoospores, and will not conjugate. 

a 

Welle, in ' Engler and Prantl,' op. cit., i, § 2, p. 129.

SOME PROBLUMS OF REPRODUCTION. 19 

but the zoospores, formed by the resolution of the protoplasm 

into uninucleated cells, have nuclei constituted by the fusion 

of several vegetative nuclei. We may, however, regard this 

multiple fusion of nuclei as a karyogamic process, and the 

zoospores as zygotes issuing from multiple endogamy. This 

process is a further development of the gametogeny of Dasycladus; 

and we shall find that the Saprolegniese and Peronosporese 

have similar relations with one another. 

SPHJE&OPLEA, 1 like Cladophora, has chambered filaments, and 

each chamber is subdivided by protoplasmic septa, in which 

alone the nuclei lie, from one to four in each. The plant is 

oogamous. The spermatozoa are formed in distinct chambers 

to the oospheres; to form the former rapid nuclear fission takes 

place in each protoplasmic septum, which is finally resolved 

into the numerous uninucleate spermatozoa, the parietal 

protoplasm being also used up in the process. 

The oospheres are also formed by the rounding off of the 

protoplasm into numerous uninucleated spheres without epiplasm; 

perforations are formed in the wall of the tube to admit 

the spermatozoa, but how or at what stage is not stated. The 

oosphere-nucleus is formed by the fusion of several nuclei. 

Rauwenhoff writes, 3 " The number of nuclei seems to diminish; 

each aggregation of protoplasm possessing three or four 

chromatophores, .... while I only found one or two nuclei. 

When there were two, they were closely appressed; when a 

single one, it was large and elongated. In either case the 

nucleoli had disappeared; the chromatic elements were visible 

as dots or rods, aggregated in an irregular figure. To all 

appearances, then, several nuclei fuse into one." This account 

might almost fit word for word the phenomena seen in the 

formation of the oospheres of Saprolegnia. 

1 

"Zur Kenntniss der Algengattung Sphseroplea," in ' Berichte d. Deutsch. 

Bot. Gesellsch./ vol. i. 

2 

"Recli. sur le Sphseroplea annulina," in 'Arch. Norland.,' vol. xxii, 

1888. This later paper I only saw during the correction of the proofs. I 

had, in the MSS., anticipated the probability of nuclear fusion in the 

oospheres, despite Heinricher's statement to the contrary.

20 MARCUS M. HABTOG. 

VAUCHERIA is continuous and oogamous. The spermatangium 

is the distal end cut off from a short lateral tube. From 

the number of spermatozoa formed here, as compared with 

the vegetative nuclei of the ordinary protoplasm, it is certain 

that nuclear fission must precede spermatogeny; according to 

Berthold 1 there is here a formation of epiplasm comparable 

with that of the sporangia and gametangia of Cladophora. 

The " oogonium" is formed primitively as a lateral outgrowth 

; it contains at first numerous nuclei, the number of 

which is finally by fusion reduced to one. 2 A beak for the 

passage of the spermatozoa is formed as in Oedogonium, 

and the formative plasma undergoes mucous degeneration. 

Schmitz calls this mucified plasma of the beak a Eichtungskorper 

(polar body), and says it contains "numerous small 

nuclear fragments abstricted from the numerous nuclei of the 

young oogonium." 3 If this meagre statement be accurate 

(and it is all we have), it would seem that nuclear divisions to 

form gametonuclei take place, and half the offspring pass into 

the epiplasm, and the other half fuse to form the pronucleus 

of the single oosphere—a process comparable with that of 

Peronospora (infra, p. 22). 

2. Colourless or Fungal Types. 

(a) Phycomycetes Zoosporeae. 

It is convenient to consider separately the Phycomycetes 

with flagellate spores, comprising Chy tridiese, Ancylistese, 

Monoblepharis, Peronosporese, and Saprolegniese, 

as Zoosporese, in opposition to the higher group 

Aplanosporese, which never form organs of locomotion, and 

which comprises only Entomophthoreae and Mucorini. 

ANCYLISTE/E 4 are in appearance oogamous, the entire con- 

1 

Op. cit, p. 305. 

2 

According to Scbmitz, "Die Zellkerneder Thallopliyten," in 'Sitzungsb. 

d. Niederrh. Ges. zu Bonn/ 1879. 

3 

This k contained as a mere by-statement in a foot-note (on p. 225) to 

bis paper, " Untersuchuugen iiber die Befruchtung der Plorideen," in 

' Bitzungsb. d. Berl. Akad.,' 1883. A full account is much to be desired. 

4 

My account of Ancylistese and Olpidiopsis is taken from Zopf,

SOME PROBLEMS OF BEPBODUOTION. 21 

tents of the female plant condensing into one or more 

" oogonia" (?), that of the male into " antheridia," which 

open one into each "oogonium;" the whole of the male protoplasm 

passes over into the oogonium by siphonogamy, and 

the two plasmas fuse to form the zygote. Though we have 

no information as to the cytology of this group, it would seem 

probable that either gamete has a nucleus formed by the fusion 

of several vegetative nuclei, and that the zygote is also uninucleate. 

No epiplasm is formed. 

CHYTRIDIEJE present conjugation in various modes; in many 

cases the " gamete" contains all the protoplasm of the plant, 

which we know to be apocytial in the vegetative state; but we 

have no evidence as to the nuclei of the so-called gametes and 

zygote. Conjugation has been observed in four genera: 

Polyphagus by Nowakowski, 1 Olpidiopsis by Zopf, 

Zygochytrium and Tetrachytrium by Sorokin. 2 

In the two former genera all the protoplasm goes into the 

gametoid. In Polyphagus the gametoids are formed by two 

distinct plants somewhat different, and the union is siphonogamous. 

In Olpidiopsis the gametoids are differentiated by 

the separation of a single apocytium into a larger part, the 

"oogonium," and a smaller part, the "antheridium;" the latter 

is at first completely shut off by a cell-wall which becomes 

perforated, admitting the whole of the protoplasm of the antheridium 

to enter and fuse with that of the oogoniura, as in 

Ancylistese. In both genera the zygote is a " resting spore." 

ZYGOCHYTKIUM forms gametoids on outgrowths of its mycelium 

which conjugate in (monoecious) pairs, like those of 

Mucor. 

TETEACHYTKIUM forms, in terminal enlargements of the 

mycelium, numerous one-ciliated zoospores which are euisogamous, 

conjugating in pairs as soon as they leave the sporangia, 

" Zur Kenntniss. der Phjoomjceten," in ' Nov. Act. Ac. Leop. Carol.,' 

vol. xlvii, 1885. 

. • In Colm's ' Beitrage,' vol. iii. 

3 ' Bot. Zeit.,' 1874, p. 308. . .


The last two genera have a mycelium unusually well developed 

for this group, and are regarded by De Bary as doubtful 

members thereof. 

MQNOBLEPHARIS 1 forms its spermatozoa by the resolution 

of the protoplasm of spermatangia into one-flagellate cells, 

differing only in their smaller size from the vegetative zoospores, 

and therefore possibly formed by bipartition of potential 

zoospores. The protoplasm of the oangium, after forming a 

terminal aperture, contracts and rounds off into the oosphere; 

which, if uninucleate, has probably, from its size, formed its 

gametonucleus by the fusion of many vegetative nuclei. No 

epiplasm is apparently formed. 

The PERONOSPOREJE are oogamous and siphonogamous. 

The only species in which the formation and union of the 

gametes has been fully studied is Peronospora parasiticaj 

and I shall utilise Wager's careful description 2 of the sexual 

processes in this species, having had the opportunity of verifying 

its accuracy on the original specimens. The spherical 

" oogonium " (or rather oangium) is cut off from the tubular 

hypha by a basal septum if terminal, by two if intercalar; 

it is apocytial, containing numerous nuclei. Each nucleus 

undergoes repeated bipartition; and the majority of the nuclei 

so formed pass into a peripheral layer of protoplasm, thus 

constituting the so-called " periplasm ;" three of them pass to 

the middle of the central mass of protoplasm, the so-called 

" gonoplasm/' and fuse therein into the single pronucleus. 

The " antheridium " (or spermatangium) is an ovoid enlargement 

of a hypha, closely applied by its apex to the oogonial 

wall and cut off by a basal septum ; it contains several nuclei, 

which like those of the " oangium " multiply by mitosis; it 

emits a tube which perforates the oogonial wall and passes 

through the periplasm to open just at the surface of the gono- 

1 

Cornu, " Monographie des Saprolegnie'es," in ' Ann. Soi. Nat. Bot.,' 

ser. 5, vol. xv. 

2 

"On the Structure of the Nuclei in Feronospora parasitica," in 

1 

Annals of Botany," vol. iv (1889).


plasm; a small portion of granular protoplasm carries down a 

single male nucleus to fuse with the female one. The gonoplasm 

secretes an inner coat to the zygote, around which an 

outer one or "epispore" is secreted by the periplasm. The 

nuclei present in this layer can hardly be essential to the formation 

of the epispore, since no nuclei are present in the 

layer of epiplasm which does similar service to the endogenous 

spores of the Ascomycetes. We can only regard the nuclear 

divisions in " oogonium" and antheridium as phylogenetic 

reminiscences of the formation of gametes by cell division; 

the periplasm is thus equivalent to a number of degenerated 

gametes which have taken on the function of epispore formation; 

the multitude of gametes are sacrificed to the few. 

Obviously what we here term the " oogonium" is neither 

morphologically nor physiologically the exact equivalent of a 

single oogonium in cellular, as distinguished from apocytial 

plants, but represents an apocytium of oogonial cells; and the 

antheridium has a similar relation to the spermatogonium of 

cellular plants. 

The processes in those SAPROLEGNIEJE 1 that have been fully 

studied mark a distinct step further in the same path. The 

oangia are at first filled with multinucleated protoplasm ; 

vacuoles appearing and enlarging bring the nuclei closer 

together, and they soon fuse in pairs, a process continued 

until their number is materially reduced j while the mitoses 

observed in Peronospora do not take place. The primitive 

nuclei are vesicles with a central chromatin mass supported 

by a "linin" or nucleo-hyaloplasma network. In fnsion of 

the nuclei the chromatin masses long remain distinct, but 

are smaller and take up stain less readily, and the nuclear 

wall at this stage ceases to stain, so that the fusion nuclei 

have the look of vacuoles in the cytoplasm containing a 

variable number of chromatic granules. During this stage 

the true vacuoles unite to form a large central cavity into 

which fresh vacuoles open, so that the protoplasm forms a thick 

1 

The following account is largely taken from an original paper of my own 

" On the Cytology of Saprolegnieee," still incomplete and unpublished.


mantle around the central space. The protoplasm then becomes 

aggregated into distinct masses, the oospore " origins/' projecting 

into the vacuole and united by a continuous peripheral 

mantle, which thins gradually as its substance becomes taken 

up into these masses. Finally, the connecting mantle gives 

way; the masses separate and round off; after a short rest 

they become amoeboid, and some of their blunt, non-nucleated 

processes become abstricted. Very soon, however, they are 

taken up again by the masses which abstricted them, and 

these masses round off into the " oospores." The very same 

abstriction and resumption of non-nucleated processes of cytoplasm 

takes place in the formation of the asexual zoospores ; x 

it is probably a process derived from cell-wall formation, 

analogous to what we have seen in Cladophora, but in a 

yet more reduced condition. The oospores after coming to 

rest soon become surrounded by a cellulose wall, thickened by 

successive internal deposits; each finally possesses a single 

nucleus in the resting state, i. e. spherical, with a single 

central sphere of chromatin. The complete fusion of the 

nuclei takes place in Saprolegnia as early as the first formation 

of the masses or oospore origins, while in Achlya it may 

be deferred till after the formation of the spore membrane, 

for young oospores are frequently binucleate. 

The antheridiutn is also multinucleate, and lies closely 

appressed to the oogonium; on the rupture of the protoplastic 

mantle of the oogonium and separation of the oospores 

it emits tubes which grow into the cavity of the oogonium, 

and abut against the oospores just before they form a cell-wall 

or during this process; but they do not enter the oospore, 

open, or emit any fertilising bodies. 3 Their contents are 

1 See Rothert, "Entwioklung d. Sporangien bei den Saprolegnieen," 

1888 (this paper was an advance publication of ' Cohn's Beitrage,' vol. v, 

1890; it was abstracted and criticised by me under the title " Recent Researches 

on the Saprolegniese," in ' Annals of Bot.,' vol. ii, 1888. 

3 I have now fully satisfied myself that the contrary statements of Pringsheim 

(in ' Sitzungsber. d. Berl. Akad.,' 1882) are erroneous, being based 

partly on the intrusion of parasites as shown by Zopf, partly on the postmortem 

appearances produced by unsuitable reagents.


granular protoplasm, with small nuclei formed by the division 

of those of the antheridium. Antheridia may be present or 

absent in one and the same species without making the 

slightest difference to the formation of the oospores. 

The homology of the antheridium with that of Peronospora 

is obvious and complete. The oangia behave very 

differently; the mitotic nuclear divisions are suppressed; 

there is no differentiation of gonoplasni and periplasm, but 

the number of the nuclei is reduced by successive fusions, and 

the whole protoplasm becomes finally resolved into uninucleated 

spores. The usual statement made is that this 

group is "parthenogeneticj" but the process is different from 

true parthenogenesis, which means the independent evolution 

of a single gamete. Here the formation of gametes remains 

completely in abeyance; instead of nuclear divisions we have 

nuclear fusions, " Karyosymphysis" if not Karyogamy replacing 

Karyokinesis. What I believe to be the true interpretation 

of the facts is this:—We have a case of multiple 

endogamous union of potential gametes; the preliminary 

nuclear divisions occurring elsewhere have been suppressed 

as useless in anticipation of the subsequent fusions; the 

process of fusion of three nuclei to form the female pronucleus 

in Peronospora has advanced here to the fusion of so many, 

that the part to be played by the male nucleus has been cut 

out as unnecessary. 

If we remember how reckless Nature is of wasting spermatozoa, 

and that in the related Per ono spore se all the antheridial 

nuclei save one are wasted, we shall see that the 

utilisation in Saprolegniese of all the oangial nuclei is 

positively an economy, even though the males (antheridia) 

continue to be formed and die, going to absolute waste without 

fulfilling any functions whatever; in some species, however, 

few or no antheridia are formed. The oospores are then 

endogamous zygotes, not parthenogametes; their rejuvenescent 

nucleus is the product of the fusion of many closelyrelated 

nuclei, not of t w o of different origin as in ordinary cases 

of binary isogamy. The relations of Peronosporese and

26 MARCUS M. HAETOG. 

Saprolegniese find a parallel in those of Dasycladus 

and Derbesia (supra, p. 18). 

Marshall Ward sought 1 to identify the extrusion of protoplasm 

by the forming oospores with the formation of polar 

bodies in the Metazoa; and the resumption of these masses he 

regarded as probably connected with the alleged parthenogenesis 

of the group. The latter view, and indeed the former 

also, break down now that we know that both processes occur 

in the formation of the asexual zoospores; they find their 

explanation in the comparison with the zoospore formation of 

Cladophora. 

(b) Phycomycetes Aplanosporese. 

The Entomophthorese present conjugation between their 

hyphse; as a rule the conjugation takes place in the horizontal 

tube uniting two hyphse, like the cross-bar of an H, and the 

zygote forms a spherical enlargement in the middle. 

Unfortunately we know nothing of the cytology of the 

process in the majority of the species ; it has only been studied 

in Basidiobolus, 2 which is by exception truly cellular (while 

the other genera are apocytial), and which is peculiar in its 

conjugation. 

In this genus two adjacent cells of a hypha grow out sideways 

at their adjacent ends, which turn up side by side, and 

the nucleus of each enters its turned-up tip. Either nucleus 

divides by mitosis; the upper daughter-nucleus passes into the 

extreme tip, and is cut off as a sterile cell; the lower nucleus, 

with all the protoplasm of the cell, fuses with its fellow to 

form the zygote. Here we have the best parallel with polarbody 

formation to be found in isogamous conjugation. If we 

compare this with the conjugation of Closterium or Epithemia 

(supra, p. 14) we find the interpretation obvious: 

the first cells are progametes, and on approaching produce the 

1 

" Observations on Saprolegniese," in ' Quart. Journ. Micr. Sci.,' vol. xxiii, 

pp. 282 (note) and 291. 

3 

By Eidam, in ' Conn's Beitrage,' vol. iii.


gametes by binary fission. Owing to the subterminal position 

of the nucleus in the cell at the time of mitosis one daughternucleus 

has too little cytoplasm around it for further evolution, 

and so forms an arrested gamete, while its sister gets 

the lion's share, and enters into karyogamic union with the 

(5) (O 

FIG. 1.— Conjugation of Basidiobolus : a, early stage; b, division of each cell 

to form active and arrested gametes; c, formation of zygote. I use 

here the nuclear notation explained above. 

corresponding gamete of the other pair. So we describe the 

process thus : the adjacent cells are progametes, each of which 

by unequal divisions forms two gametes, the apical one 

arrested, the other functional. 

The MTJCORINI, in the common phrase, form zygotes by the 

isogamous union of gametes, save in one species, Mucor 

heterogamus, Vuillemin, which is anisogamous. But this 

description is not at all accurate from the present standpoint 

of cytology; for "gametes" and "zygotes," so called, are 

not cells, but apocytia of plurinucleate protoplasm in a cellwall, 

which we may term "gametoid" and "zygotoid" respectively. 

Of the nuclear changes involved in the conjugation 

we know as little as in the Chytridiese. Several 

possibilities are open: 

(1) The nuclei of the respective gametoids may unite two 

and two within the zygote in exogamous union; 

(2) The nuclei may unite in pairs or otherwise, irrespective 

of their origin ; or, finally, 

(3) Rejuvenescence may ensue, as in plasraodial formation,


by the nuclei wandering into foreign protoplasm, and by the 

plastogamy of the cytoplasm. 

" Azygospores" or " pseudo-zygospores" may be formed by 

such gametoids as fail to conjugate. But we must be content 

to leave the true nature of this paragenetic process undetermined 

so long as we are in ignorance of the nuclear processes 

involved. 

(c) Higher Fungi. 

The hyphse of the higher Fungi are transversely septate, 

with usually multinuclear chambers; by lateral tubular outgrowths 

above and below the septa, which fuse and become 

pervious to form loops, or so-called " clamp-connections," protoplasm 

with or without nuclei can pass from one chamber to 

another; but to what extent migration does take place we do 

not know. 

The lower ASCOMYCETES show apparently a siphonogamous 

union, the larger "ascogonial" cell (or gametoid?) ultimately 

growing out into the sporiferous asci; but we. really know 

nothing of the cytology of the process. 

In certain closely-allied LICHENS an oogonium similar to 

that of other Ascomycetes is formed, which, however, emits a 

trichogyne like that of Floridese, but repeatedly septate. 

Spermatia (probably uninucleate) are also formed here by 

abstriction from special hyphaa, and conjugate with the 

trichogyne, after which the ascogonium buds off asci. Here, 

again, we know nothing of the nuclear relations. 

The majority of ASCOMYCETES and all the BASIDIOMYCETES 

are completely apogamous, so far as is known. 

In USTILAGINE^: from the spores is formed a rudimentary 

mycelium j this divides into four gametal cells, which conjugate 

by loop or clamp connections; or else usually four 

elongated uninucleate sporidia are formed which conjugate in 

pairs, forming H-shaped unions with their fellows or neighbours. 

Fisch states that there is no nuclear fusion j 1 but there 

is certainly plastogamy. After conjugation one (or both?) of 

1 

According to Vines, ' Veg. Phys.,' p. 618.


the zygotes emits a tube^which may abstrict spores or grow 

into a vegetative mycelium. This germination of the gametes 

may in some cases take place facultatively independently of 

conjugation. 1 

PROTOMYCES resembles Ustilaginese in the behaviour of its 

gametes; but they are formed endogenously in large numbers 

in the spore, leaving a quantity of non-nucleated epiplasm. 

In UREDINEJE Massee has described a process of siphonogamous 

2 Conjugation between a larger "oogonium" and a 

smaller antheridium comparable to that of the lower Ascomycetes* 

The only cytological observations of importance 

given are that the oogonium is uninucleate before fertilisation, 

and contains several small nuclei on the third day. 

C. HIGHER THALLOPHYTES. 

1. Floridese. 

The Red Seaweeds stand apart from the other Thallophytes 

in many respects, and we follow Falkenberg 3 in regarding 

them as distinct from the true Algse. Their male reproductive 

cells or "spermatia" are all but motionless, and scattered 

by local currents. Their female cells, " carpogonia" or 

" procarpia," are usually permanently fixed in the thallus. 

They emit a trichogyne which does not open, and is abstricted 

after receiving the male pronucleus by conjugation 

with the spermatium, and transmitting it to the female pronucleus 

in the base of the " carpogonium." 

1 

It is noteworthy that the formation of gametes here takes place at a stage 

in no way homologous with the sexual organs of the (more primitive) Ascomycetes. 

It would seem, indeed, probable that this gametal process has 

originated de novoasa specialisation of and advance upon the free anastomoses 

formed between contiguous young hyphse in so many of the higher Pungi. 

There is, indeed, no reason why such processes should not originate afresli at 

a different stage in forms that have become apogamous by the complete loss 

of a sexual process at the usual stage. 

s 

" On the Presence of Sexual Organs in iEcidium," iu ' Ann. of Bot.,' 

vol. ii, 1888. 

3 

In his monograph of the Alg» in Schenk's ' Handbuch der Botanik.'


The BANGIACE-E differ, however, little in the essentials 

of gametogeny from those protophytes which they resemble so 

closely in vegetative growth. In Bangia the spermatogonium 

undergoes repeated bipartitions accompanied by cellwall 

formation; finally, the cell bodies undergo two further 

bipartitions, and become free as four naked spermatia. The 

oogonia produce oospheres by bipartition, which are cells 

with a narrow anterior receptive apex and a dilated base 

containing the nucleus. A spermatium sticks to the narrow 

end (trichogyne), and conjugates with it, and the spermatonucleus 

passes down, we may suppose, to fuse with the 

oonucleus. The basal protoplasm then contracts to form the 

zygote, while the upper part takes no further share in its 

life. The trichogyne is here obviously comparable to the beak 

in Vaucheria or (Edogonium. PORPHYRA differs in minor 

points only from BANGIA. 

In the true FLORIDE;E the spermatia 1 are formed, not by 

ordinary fission, but by budding and abstriction, and are 

uninucleate. In every case they are borne on a persistent 

basal cell, whose nucleus divides, one daughter-nucleus passing 

into the budded cell, the other remaining in situ. We may 

distinguish two modes, which can again be subdivided. 1. The 

budded cell undergoes (one or) two mitotic divisions to form 

four spermatia, all of the same generation, and grandnieces of 

the basal cell: (a) the divisions are crucial and the spermatia 

are collateral, resting on the basal cell (Polyides); (b) the 

divisions are horizontal, and the spermatia form a vertical 

file (Hypnea). 2. The basal cell repeats the former process 

of budding, so that the spermatia are of successively lower 

generations, and the youngest is sister to the ultimate 

basal cell: (a) the buds are collateral and all spring 

directly from the basal cell (Chondria); (b) the buds are 

intercalated in turn between the basal cell and the next older, 

so as to form a basipetal file like the conidia of many Fungi 

(Melobesia). 

1 The following account is taken from Guignard, " DeVeloppement et 

Constitution des Anth&rozoides," in 'Rev. G6n. de Botanique,' vol. i, 1889.


The oosphere or "procarp" has a long trichogyne closed at the 

apex, and a basal enlargement containing the single nucleus. 

The spermatium adheres to the trichogyne and opens into it ; l 

its contents with the male pronucleus pass down j and since 

at this time two nuclei are seen in the base of the procarp, and 

only one shortly after, it is certain that the nuclei must fuse 

in the zygote. The trichogyne is then shut off, its lumen 

being encroached upon to obliteration by a centripetal growth 

of its cell-wall close to the base. Before and after fertilisation 

granules which react to stains like nuclear chromatin are 

present in the plasma of the trichogyne; and Schmitz 

identifies these with excreted nuclear fragments on purely 

& priori grounds, relying on the current theory of fertilisation. 

But he adduces no real evidence as to their origin and 

nature. 

A peculiar process occurring in many Florid ese is secondary 

fertilisation, the zygote forming a new karyogamic 

union as a gamete with an " auxiliary cell" or secondary 

oosphere; or the zygote grows and branches with cell division, 

and its offspring play the part of secondary males to the 

secondary oospheres (Dudresnaya). In this way sometimes 

one spermatium indirectly fertilises several secondary oospheres 

—an economical process as yet unparalleled in nature; its 

explanation is probably to be sought in the motionless character 

of the male cells, and the inadequate adaptations for what 

we may almost term " pollination." 

In CoftALUNA the procarps with their auxiliary cells are 

collected into a disc; the central cells alone possess trichogynes, 

and are fertilised by the spermatia; but as zygotes they 

have no power of development save to fertilise in turn the 

peripheral procarps, which have no receptive organs of their 

1 The following cjtological details are taken from the account by Schmitz 

in ' Sitzuugsber. d. Berl. Akad.,' 1883, 215.


2. Characese. 

In CHARACE^; the spermatozoa are biflagellate; they are 

formed by the direct evolution of the cell-bodies of short discoid 

segments of long confervoid filaments; these grow by 

intercalar divisions, which, perhaps, may be taken to correspond 

with the ordinary gametogenic fissions of a spermatogonium. 

The oosphere is formed by the enlargement of the 

terminal member of a short file of cells. The cutting off of one 

or three sterile basal cells (" Wendungszellen") by oblique 

septa suggests the formation of one functional and one or three 

arrested gametes by one or two divisions of a gametogonium. 

D. ARCHEGONIATA. 

This group is distinguished by the formation of the archegonium, 

a cellular flask-shaped structure, with a single oosphere 

occupying its belly, and a series of canal-cells its neck; the 

latter degenerate to attract and bring in the spermatozoon. 

1. Muscinese. 

Iu the MUSCINE^; one single " initial cell" by its divisions 

forms the archegonium. The earliest divisions separate off 

the tissue-cells destined to form the wall and stalk of the 

archegonium from the "inner cell/' which gives rise to the 

oosphere and canal-cells. This inner cell divides according to 

the accompanying schema (Fig. 2) ; at its bipartition are 

" &c, neck canal-cells. 

NH 

N 3 _ 

N a f N= 

LNM 

belly canal-cell. 

oosphere. 

FIG. 2.—Schema of divisions of inner cell of archegonium in Muscinese. 

formed two cells, a basal " central cell" and an apical " neck

SOME PEOBLBMS 01 REPRODUCTION. 33 

canal-cell." The latter elongates with the neck of the growing 

archegonium which it occupies and fills, and by repeated' 

bipartitions forms a file of cells (a multiple of four) which are 

also termed " neck canal-cells." The proximal cell (central 

cell) occupies the belly of the archegonium, enlarging with it, 

but undergoing no further division till its maturity. Then 

this central cell divides into two, the lower rounding off as 

the oosphere, the upper undergoing mucous degeneration 

like the neck canal-cells, and termed the " belly canal-cell." 

Sometimes these two sister-cells are equal, but usually the 

belly-cell is much smaller. Obviously both are gametes, the 

former functional, the latter degenerate. 

The next question that arises is this :—What are we to regard 

as the "oogonium"—the central cell, the inner cell, 

or the initial cell of the archegonium? The divisions of the 

last are too closely allied to those which form tissue-cells 

elsewhere; and of this nature are the majority of its broodcells 

forming the wall of the oogonium, so that it would be 

rather strained to call the initial cell a gatnetogonium. The 

second alternative would seem most natural: to regard the 

inner cell as a gametogonium, and the neck canal-cells as 

degraded gametes (or rather their offspring). For though the 

growth of these is concurrent with that of the cells of the 

neck and accompanied by numerous divisions, yet the horizontal 

septa are not coplanar with those of the neck wall, and do 

not complete with these the schema of orthogonal trajectories, 

which they should do if they belonged to the same system 

of tissue-cells; their number is always a multiple of four; and 

while the cells forming the oogonial wall have a prolonged 

life, that of the canal-cells is limited, as in most gametes. 

Again,the antheridium is formed from a single initial cell similar 

to that of the archegonium, and similar divisions mark off its 

wall-cells from a single central cell. The latter forms a 

complex of cubical spermatocytes only, by repeated bipartition, 

the cell-walls intersecting at right angles; and the cell body 

of each spermatocyte is converted into a biflagellate spermatozoon, 

a small portion of the cytoplast remaining unutilised 

VOL. XXXill, FART I.—NEW SEE. C

34 MARCTTS M. HAETOG. 

in the great transformation it undergoes. There can be no 

doubt that the " inner cell " of the male antheridium is a true 

gametogonium, since all its brood-cells become functional 

gametes; and as the " inner cell" of the archegonium is the 

homologue of that of the antheridium, we have here an additional 

reason for regarding the former as a gametogonium, 

and the neck canal-cells as the outcome of degraded gametes; 

for we must remember that these are of a lower generation than 

the belly canal-cell and oosphere. 

2. Vascular Cryptogams. 

In VASCULAR CKYPTOGAMS generally the antheridium resembles 

that of Muscinese inessentials; but the archegonium 

is somewhat different, for the initial cell only forms the neckwall 

and inner cell, the belly-wall being formed by a sort of 

epithelial wall segmented off the adjacent cells of the prothallus. 1 

Moreover, the divisions of the inner cell are often symme- 

< ': i XN -> 

Ni (central cell). j / N ! (belly-canal cell). 

j\N 2 (oosphere). 

W (neck-canal cell);


passes directly into the oosphere, 1 and the "law" breaks down 

in our very next group also. 

The spermatozoa of this group are multiciliate, not flagellate 

; a certain amount of cytoplasm is left over in their 

differentiation from the spermatocytes. 

E. SlFHONOGAM^! (PHANEROGAMS). 

1. Gymnosperms. 

In GYMNOSPERMS the pollen-grain or androspore produces 

a few sterile cells at its base, which are recognised as 

equivalent to the male prothallus of a Heterosporous Cryptogam. 

One cell, probably equivalent to the initial of an antheridium, 

grows out into the pollen-tube; its nucleus divides into 

two nuclei, one of which is the gametonucleus; or into a 

number of nuclei; so that the pollen-tube represents an 

apocytium of microgametes. 

The formation of the archegonium is similar to that of the 

Vascular Cryptogams; the initial cell only forms the neck-wall 

and inner cell, the belly-wall being formed from the neighbouring 

cells of the prothallus (so-called endosperm). But 

the gametogenic processes are still further reduced, for in 

Conifers and Gnetads the inner cell only divides once, forming 

directly the oosphere and single canal-cell, while in Cycads the 

inner cell does not divide, but assumes directly the character 

of the oosphere, 3 a cytoplastic beak-like process replacing the 

canal-cell. Thus, in the series of archegoniate plants in 

Vascular Cryptogams two mitoses specialise the oosphere from 

the inner cell; in Conifers and Gnetads one mitosis suffices; 

in Cycads none takes place. This variation is a sure proof that 

there can be no need of these mitoses to eliminate part of the 

egg-nucleus and make room for the male, and that the function 

of these mitoses is not that assigned to them in the 

" replacement" hypotheses. 

1 

"On the Development of Pilularia globulifera," &c, in 'Ann. of 

Bot.,' ii, pp. 247-8. 

8 

According to Eichler, in 'Engler and Prantl,' op. cit., vol. ii, § 1, p. 16.

36 MAEOUS M. HARTOGt. 

2. Angiosperms. 

In ANGIOSPERMS the processes in the pollen-tube show 

a still further degeneration. The original nucleus divides 

into two: (1) a vegetative nucleus corresponding to the 

multicellular body of the Gymnosperms; (2) a reproductive 

nucleus corresponding to the gametogonial nucleus of that 

group : but no cellulose wall separates them; or if a rudimentary 

cell-wall be formed, it is at once absorbed. The 

vegetative nucleus seems here to have a function in connection 

with the growth of the pollen-tube, at the apex of 

which it lies, degenerating when this growth is completed. 

The gametogonial or generative nucleus then passes forward 

into the apex of the tube and undergoes mitosis; one of the 

two nuclei so formed is the male pronucleus, and passes into 

the oosphere. 1 

Here we have the two mitoses demanded by popular theory, 

but an interval of hours or days separates their occurrence; 

and the morphological explanation—that the first differentiates 

a prothalliar from a gametogonial nucleus, and that the 

second (of the latter only) is a gametogenic fission—is absolutely 

incontrovertible, when we compare the pollen-grain here 

with that of Gymnosperms, and again with the androspores of 

Heterosporous Cryptogams. 

The FEMALE GAMETE is differentiated in the embryo-sac by 

a process unrivalled in complexity ; while the morphology of 

the process is still doubtful. In recapitulating this, I will try 

by full notation to make the relations and fates of the nuclei 

as clear as possible. The embryo-sac corresponds to that of 

Gymnosperms, and most morphologists are agreed in regarding 

it as a megaspore, homologous with those of the Heterosporous 

Filicinese that develop into a reduced prothallus 

bearing few archegonia only. Three mitotic divisions of its 

1 Strasbiirger and Elfving, who first discovered this process, originally 

reversed the parts of the respective nuclei. In some cases the generative 

nucleus undergoes two mitoses and so forms four gametouuclei.


nucleus occur as follows:—The first differentiates an Apical 

(N a a) and a Basal nucleus (N a b) respectively. Each of these 

again divides to form a pair of nuclei nearly superposed, which 

we term and letter Apical (N s a), Subapical (N 2 sa), Subbasal 

(N 2 sb), and Basal (N 3 b) respectively. Each of these four 

again divides to form a pair of nuclei of the degree N s . The 

Apical pair (N 3 a + N 3 a) and Basal pair (N 3 b + N s b) are collateral; 

the Subapical and Subbasal pairs are superposed to 

form a file of four nuclei, which we name and letter Upper 

and Lower Subapical (N s usa + N 3 lsa), and Upper and Lower 

Subbasal (N 3 usb + N 3 lsb) respectively. Of the cytoplasm 

lining the cell-wall and surrounding the immense central 

vacuole, each nucleus attracts a certain portion so as to form 

a naked "free cell" somewhat ill-defined, and indeed anything 

but free. The following schema (Fig. 4) shows the for- 

rN>a- 

-N 2 b- 

Synergids 

N 3 a N 3 a Egg apparatus. 

( 

Oospbere i 

N 3 usa j 

I 

lN 3 lsa 

ilsb 

N 3 b N»b I 

Endosperm 

nucleus. 

! Antipodal 

! cells. 

FIG. 4.—Schema of divisions in embryo-sac; the vertical lines separate

38 MAROUS M. HARTOG. 

mation of these cells and their position in the mature embryosac 

ready for fertilisation ; the dotted vertical lines indicate 

successive stages. The symmetrical relation of the eight 

cells formed is in no way exaggerated in the figure. 

Of the eight cells so formed not one is capable of ulterior 

independent development; though it appears from Strasburger's 

figures, 1 and those of other authors, that enough 

interval is left between the mitoses for the nuclei each time 

to resume a resting state. Hence it cannot be the extreme 

rapidity of the mitoses that determines the reproductive incapacity 

of these cells. The fate of these eight cells is very 

different. 

(1) The Apical Pair or Synergids, aptly termed Gehiilfinnen 

(handmaids) by Strasbiirger, are utilised as the channel 

for the transmission of the male pronucleus, sometimes 

undergoing a complete degradation into a gelatinous form of 

cellulose. 

(2) The Upper Subapical Cell is the Oosphere, 

destined on receipt of the male pronucleus to evolve into the 

Embryo. 

(3) The Lower Subapical and Upper Subbasal Cells 

conjugate to form what we may term the Endosperm-cell; 

this undergoes repeated divisions, appropriating at each more 

and more of the parietal cytoplasm of the embryo-sac, till at 

length the brood-cells constitute a continuous cellular layer, 

the Endosperm, in which the embryo lies, and destined to 

destruction as food for the embryo, either during the maturation 

of the seed, or later on in the process of germination. 

For some time no cell-walls separate the brood-cells, which 

thus constitute an apocytium, lining the embryo-sac, and enclosing 

a gigantic vacuole which persists in the Coco-nut. When 

cell-walls divide up this apocytium, their inner tangential walls 

form a continuous lamina, within which remains a layer of 

cytoplasm surrounding the central vesicle, 2 just like that of 

the gametangium of Botrydium or Acetabularia. Here 

1 ' Befruchtung nnd Zelltheilung, 1 &o. 

s Bertkold, op. cit., p. 213,

SOME PROBLEMS OF BEPBODUOTION. 39 

there is no question of giving a mystical significance to this 

"excretion process." 

(4) The Lower Subbasal and the two Basal Cells 

lie huddled and inert at the base of the embryo-sac, as 

"Antipodal cells/ 5 and finally disappear in the growing 

endosperm. 

The homologies of these structures are somewhat obscure, 

but the following explanation may be tendered as a fair 

one: 

(1) The four cells of the form N z correspond to prothallial 

cells of a Cryptogam or Gymnosperm; cells which we 

know form the common initials of both archegonium-wall (or 

neck at least) and oogonium. 

(2) The Apical cell (N 2 a) divides to form an archegonium 

of two neck-cells only, without any oogonium (such an archegonial 

neck of two cells is found in Cycads). 

(3) The Subapical cell (N 3 sa) divides into a superposed 

pair of which the Upper is the oosphere, of whose significance 

as a gamete there can be "no possible doubt whatever." 

(4) The Lower Subapical cell (N 3 lsa) is that which conjugates 

with the Upper Subbasal (N 3 usb) ; as a consequence 

the cell produced by their fusion rejuvenesces, and by its 

repeated bipartition forms the endosperm. This structure is 

comparable to a thallogenous plant of low organisation and 

limited life; the endosperm-cell that produces it must be 

regarded as a zygote, and the two cells that unite to form this 

zygote are necessarily gametes, whose close kinship, though 

the most distant possible under the circumstances, may influence 

the low organisation and limited life of their zygote. 1 

Thus the subapical cell producing by bipartition two gametes 

is a gametogonium; or we may go further and identify it with 

an initial cell, producing an archegoninm without a neck, and 

reduced to the oogonium. Of the two gametes formed by the 

1 This important identification of the endosperm-cell as a zygote was first 

made out by Professor Le Monnier, of Nancy, in an unpretentious little note 

in ' Morot's Journal de Botanique,' vol. i, p. 140 (June, 1887).

40 MARCUS M. HAETOO. 

divisions of the oogonium both are functional though in different 

ways. 1 

(5) The Upper Subbasal cell (N 3 usb) is one of the gametes 

of the endosperm; its sister-cell, the Lower Subbasal cell, 

is, therefore, an arrested gamete; and the Subbasal cell 

(N 2 sb) is a gametogoniura like the subapical (N 3 sa). 

(6) From the symmetry of the embryo-sac we may regard 

the basal cell (N s ) as equivalent to the apical, and their 

divisions as homologous; or we may regard the basal pair 

of cells as the remains of the prothalliar tissue of the Gymuosperms. 

The above identifications we may summarise thus: four 

prothalliar cells (N 2 ) are formed; of these the two in the mean 

position (N 3 sa, N 2 sb) are gametogonia, which by a mitotic 

division form four gametes, three functional, one arrested. 

The apical cell (N 2 a) forms an archegonium reduced to a twocellular 

neck; the basal cell (N s b) forms two cells constituting 

a barren archegonium or mere prothalliar cells. I 

assume that the sister-cell of a gamete is necessarily a 

gamete, functional, arrested, or degraded; but the same rule 

does not apply to a gametogonium, which in all but the lowest 

Protophytes must have tissue-cells, not gametogonia, for its 

sisters. 3 

From the above explanation one thing is certain, that the 

endosperm of Gymnosperms is not homologous with that of 

Angiosperms, though its final function of nourishing the seed 

be the same. 

1 

The relations of position would indeed identify the oosphere with the 

Gymnosperm canal-cell, and the lower subapical cell with the Gymnosperm 

oosphore. 

' From a consideration of Guignard's researches I am now compelled to 

regard the embryo-sac as morphologically equivalent to a spore motber-cell, 

and the four nuclei, N s , as megaspores, which differentiate as in the above 

statement; for it shows the same nuclear reduction in the prophases of its 

first mitosis that occurs in the primary pollen mother-cell, which has certainly 

this value.


V. COMPARATIVE GAMETOGENY IN THE ANIMAL KINGDOM. 

A. PROTOZOA. 

1. Flagellata. 

Our chief knowledge of the gametogeny in the true Flagellata 

is due to the researches of Dallinger and Drysdale. 

After repeated acts of fission karyogamic unions occur, always 

binary. 

In CEKCOMONAS DUJARDINII and TETRAMITUS ROSTRATUS the 

gametes resemble the ordinary forms, and are isogamous. 

BODO SALTANS is anisogamous; the larger gamete, produced 

by the longitudinal fission habitual in this species, has the 

specific form; the microgamete is smaller, and produced by 

transverse fission. BODO CAUDATUS and MONAS DALLINGERII 

are also anisogamous, the microgamete having the same form 

as the megagamete, and only differing in size. In DALLINGERIA 

DRYSDALII the gametes are equal in size, but dissimilar, the 

one being like the ordinary individuals, triflagellate, the 

other uniflagellate; so that in this group we already find tendencies 

to anisogamy, and indications of the specialisation of 

gametes by peculiar forms of bipartition. 

In NOCTILUCA, belonging to the Cystoflagellates, conjugation 

is isogamous between individuals of the ordinary type. 

In this case we shall describe the behaviour of the zygote, 

which affords a most instructive parallel to certain forms of 

spermatogeny in the Metazoa. The nucleus of the zygote 

comes to lie peripherally below an elevation of the cytoplasm; 

and as the nucleus divides, so the cytoplasmic elevation is 

parted by crucial furrows into hillocks, into which the daughternuclei 

pass one to each. By some eight or nine bipartitions 

256or 512 buds are formed, grouped into a disc-like elevation. 

By a basal thinning the buds are abstricted as uninucleate 

flagellates, while the body of the zygote is left, containing a 

residue of cytoplasm but no nucleus, and obviously incapable

42 MAROUS M. HARTOG. 

of further vital evolution. In Dallinger and Drysdale's group 

the whole zygote is resolved into uninucleated spores; and 

the process in Noctiluca is a mere modification of the 

same process. 

2. Rhizopoda and Heliozoa. 

Conjugation is known to occur in some members of this 

group; the gametes appear to be ordinary individuals; but we 

have no full knowledge either of the antecedent or consequent 

processes. 

3. Gregarinida. 

The details of conjugation in this group are not fully made 

out, but that of OPHRYOCYSTIS is interesting. In this genus the 

apocytial body is first resolved into uninucleate cells, which conjugate. 

The two nuclei are stated not to fuse, but to give 

rise to six, two of which unite to give rise to a zygote-nucleus, 

around which the cytoplasm aggregates, while the other four 

nuclei pass to the peripheral cytoplasm, which degenerates 

with them. Obviously the conjugating cells are progametes, 

which only develop gametonuclei afterwards; and of these 

last, two only are functional : the peripheral cytoplasm 

and the other four nuclei represent arrested gametes. It 

would be interesting to know if the tripartite division of 

the nucleus of each of the conjugating animals corresponds to 

the schema annexed (Fig. 5), where N, M, represent the 

M 

N 

i 

3 

_ 

M l 

FIG. 5.—Tentative schema to explain the conjugation of Opbryocystis. 

N, M, are the primitive nuclei of the conjugating pair ; successive stages 

are separated by dotted lines, and the rejection-nuclei are surmounted by 

dashes; the square encloses the zygote-nucleus Z, formed by the union 

of N s , W.

SOME PROBLEMS OF BE PRODUCTION. 43 

nuclei of the conjugating cells. In this case the rejectionnuclei 

would be of different generations, like the first and 

second polar bodies. 

In MONOCYSTIS Wolters has shown 1 that the nucleus of 

either conjugating individual divides into two, a rejectionnucleus 

which passes out like a polar body, and a gametonucleus 

which fuses with that of the other individual. 

4. Radiolaria. 

In COLLOZOUM and SPHJEROZOTJM anisozoospores (of two 

sizes) are formed, but are not known to conjugate. The size 

of the anisozoospores is inversely proportioned to the number 

of the brood. Both are formed by preliminary divisions of 

the nucleus, and the resolution of the contents of the central 

capsule into uninucleate swarmers. 

5. Ciliata. 

a. Free Ciliata and Suctoria. 

The conjugation in this group differs from that in any other, 

for in either gamete two pronuclei are formed, one of which is 

exchanged for a pronucleus derived from the other gamete; 

in each gamete the original and derived pronuclei fuse to form 

a new nucleus; and the two separate without cytoplasmic 

fusion, and after a time resume their normal life and fissiparous 

powers. To understand fully this process we must premise 

that the nuclear apparatus of the Ciliata is double, consisting 

of a larger and smaller element, now termed meganucleus 

and micr onucleus respectively. The meganucleus divides by 

mere constriction, the micronucleus by a true mitosis, in fission; 

and there is reason to believe that the meganucleus is the seat 

of what we may term the physiological properties, the micronucleus 

of the morphological or atavistic properties of the 

single nucleus of other organisms. A fact that supports this 

1 In 'Arch. f. mikr. Anat.,' vol. xxxvii, 1891, p. 91.

44 MARCUS M. HAKTOG. 

view is that in conjugation the meganucleus undergoes a disorganisation 

and is sometimes completely destroyed, while the 

pronuclei which conjugate are descendants of the micronucleus 

only. From the conjugation-nucleus is regenerated a 

complete nuclear apparatus in the exconjugates; rarely is even 

a part of the old meganucleus retained and utilised by concrescence 

with the new one formed from the conjugationnucleus. 

The details are singularly interesting. Two Ciliates approach 

as apparent gametes, and join by the ventral surface. Their 

meganuclei undergo fragmentation. The micronucleus in each 

enlarges and then undergoes three mitotic divisions; usually 

three of the four nuclei formed at the second division (which 

we may letter JU 2 ) abort as rejection-nuclei (" noyaux de 

rebut" of Maupas), and they degenerate and are excreted or 

digested; while the fourth nucleus (/x s ) divides to produce the 

two pronuclei (ft 3 ). The only difference between the three 

abortive and the one preserved nucleus of the brood (/u s ) is 

that of position; it is the nucleus nearest the mouth of the 

gamete that produces the pronuclei. Again, the pronuclei 

are absolutely similar in all save position:—that nearer the 

mouth of the gamete passes over as a migratory pronucleus 

into the other gamete, the one more remote as a 

stationary pronucleus awaits the arrival of the migratory 

pronucleus from the other gamete. For convenience and 

by analogy we may term the migratory and the stationary 

gametes "male" and "female" respectively, but we must 

remember that there is no essential difference between them, 

and we shall find in Vorticellines, where the gametes fuse 

completely and only one zygote-nucleus is formed, that it is 

constituted by the union of two migratory nuclei. After 

the fusion of the pronuclei is complete the gametes separate. 

I give a schema of the processes in a single gamete up to this 

point (Fig. 6).


r/ 3 s-~z~]- 

J/«"8- Z 

*-u 3 m 

•{! 

v 

V 

FIG. 6.—Schemaof formationof pronuclei in a conjugating Ciliate. /t=original 

microuuoleu3 of one of the gametes. /i 3 s and /« 3 m = the stationary and 

migratory (female and male) pronuclei respectively. v 3 m = migratory 

pronucleus from the other conjugate, which lies the other side of the 

dotted line. The pronuclei are supposed to unite in the square Z. The 

dash above indicates rejection-nuclei. 

Some Ciliates have habitually two micronuclei; in this case 

both undergo the first two mitoses to form eight nuclei (ft 2 ), 

and seven of these abort, leaving only one to undergo the final 

mitosis; or, again, one of the two micronuclei undergoes the 

first mitosis only before its brood abort. 

The conjugation-nucleus undergoes at least two mitoses, 

and of the four nuclei so formed in the simplest cases two 

become mega- and two micro-nuclei, and at the first fusion of 

the exconjugate one mega- and one micro-nucleus pass to each 

daughter-individual. Though this is the easiest type to 

understand it is not the commonest, but the processes, though 

'of interest, are complex and too remote from our subject. 

Some of the progeny of the zygote-nucleus in certain species 

are eliminated as rejection-nuclei—a very significant fact. 

The main peculiarities of the conjugation in the Ciliata 

(apart from the formation of rejection-nuclei, to which we shall 

return) are—(1) the formation of two fertile pronuclei; (2) 

the separation of the gametes after karyogamic union of the 

nuclei has taken place without any transference of cytoplasm. 

After noting that here, at least, conjugation is an essentially 

nuclear process, we proceed to infer from the coexistence of 

conditions 1 and 2 that they are correlated phenomena. Let 

us consider the process after the second mitosis and elimination 

of the three rejection-nuclei.


The following schema contrasts the conjugation of the 

Desmid Closterium, and of a Ciliate. 

The zygote of the Closterium is totally different from the 

gametes, whose structure can only be obtained afresh by a 

very complex reorganisation and after protracted rest. The 

Ciliate, on the contrary, carries away from conjugation its 

cytoplast with all its complexity retained, and yet has a 

nucleus of the same " form " as that of the zygote of Closterium. 

The process then seems to involve the suppression 

of formation of proper gametes, in order to gain the advantage 

of the retention of the cytoplasmic body unchanged. 

Fie. 7.—Comparisons of three stages of the processes immediately leading 

up to conjugation in Closterium (A) and Paramoecium (B). la each case 

two zygote-nuclei of the value (N' + M' = Z) are formed, but the cytoplasts 

are unchanged in B, and totally altered in A. 

Having found a key to the final processes of conjugation we 

can step back, and consider the first two mitoses with the formation 

of the rejection-nuclei. We may fairly regard these 

also as attempts to form a plurality of gametes comparable 

with the processes observed in certain Fucacese, the position 

in the cytoplast determining which nuclei shall be rejected. 

Possibly, too, the failing energies of the meganucleus at this 

stage are insufficient to determine the division of the cytoplast;


indeed, the fact that cytoplastic division remains in abeyance 

during the absence of a meganucleus in " working order " is an 

additional argument for regarding this as a directive organ. 

We may note that the pairing individuals are in many cases 

much reduced below the normal size by a rapidly repeated 

series of bipartitions. 

We may then briefly state our view of the homologies of the 

process of conjugation thus:—(1) The three mitoses of the 

micronucleus point to a primitive formation of gametes in 

broods of eight. (2) The fact that no cell division accompanies 

these mitoses may be the physiological result of the inertness 

of the now disorganised meganucleus. (3) The formation of two 

fertile pronuclei in each gamete points to an ancestral stage, in 

which a binary division of two mutually attached individuals 

immediately preceded the conjugation of their offspring. (4) The 

interchange of pronuclei and separation of the gametes are 

probably modifications of the process indicated in (3), directed 

to the preservation of the highly organised cytoplast. (5) 

The pairing Ciliata before the completion of the preliminary 

mitoses are not true gametes, but progametes. 

b. Vorticellinea. 

The group of VORTICELLINES, consisting of attached forms, 

is exceptional in two respects. (1) The conjugating individuals, 

instead of being similar, are unlike and unequal; the 

larger individual being of the ordinary attached type, the 

smaller free, and produced by repeated vertical fissions from 

an ordinary individual. (2) Instead of the gametes separating 

ultimately, they fuse, the larger absorbing the smaller into 

itself; and of the four pronuclei which are formed as in other 

Ciliates, only two unite to form a single conjugation-nucleus. 

The preliminary mitoses and formation of rejection-nuclei 

offer no exceptional character, save that in the male two 

micronuclei are formed (indicating a further suppressed fission). 

Two pronuclei are formed in either gamete, and the 

migratory pronuclei, instead of passing one another, fuse 

where they meet; while the stationary pronuclei both abort.

48 MARCUS M. flARTOG. 

This confirms our interpretation of the rejection-nuclei in 

general, as gametonuclei that have failed to find cytoplasm. "We 

must admit that the fusion of the gametes in Vorticellines, 

externally resembling a true sexual process, is only derived 

from the peculiar temporary conjugation of the free Ciliata. 

B. METAZOA. 

The gametogenic processes in the Metazoa are strangely 

uniform as compared with the wide range of organic differentiation 

they present; and it is easy to see that workers 

impressed by the latter fact should have laid undue stress on 

the former. In my introductory remarks I have pointed out 

that, as most of our biological thought has been largely 

moulded, nay, created by the Metazoan zoologists, a reverence 

for great teachers has impressed itself in provinces where they 

had neither the knowledge nor the training to guide theory 

aright. 

1. Spermatogeny. 1 

The spermatozoa may be formed in one of the three following 

ways. 

(a) The most primitive mode, existing in some Sponges, 

Ccelenterates, Vermes, and possibly other groups, is this : a 

germinal cell or spermatogonium undergoes segmentation to 

form a more or less coherent mass of cells, not inaptly termed 

a " sperm-morula " by comparison with the morula of alholoblastic 

oosperm. Each brood-cell (" spermatocyte " of La 

Valette, St. George's) develops usually into a uniflagellate 

spermatozoon. One of the simplest cases occurs in Ascaris 

megalocephala, an organism which, for researches on Metazoan 

gametogeny and karyogamy, has taken the place 

occupied by the classic Frog in the physiological laboratory : 

here the spermatogonium by two divisions forms four spermatozoa 

; but the simplicity is probably derived, not primitive; 

1 Here, as elsewhere in the paper, I have omitted the proper ontogeny of 

the spermatozoa, or the modifications by which it arises from the spermatocyte, 

its youngest stage, as foreign to the scope of the inquiry.


and the spermatozoon is amoeboid. 1 By the passage of segmentation 

to budding we have a transition to mode (b). 

According to Ebner, 2 in the Rat each spermatogonium 

divides into four spermatocytes; and a number of the broods 

so formed contract a syncytial union with an attached and 

uninucleated cell (Sertoli's cell), which thus plays the part of 

a nurse to numerous spermatozoa. 

(b) The second mode of spermatogeny is that fully studied 

by Blomfield in Lumbricus. Here the nucleus of the spermatogonium 

undergoes repeated divisions; the brood nuclei 

come to the surface of the apocytium so formed and pass into 

cytoplastic buds, whose ends finally taper into flagella. These 

uuinucleate buds are ultimately, as spermatozoa, abstricted 

from a central residue of non-nucleated cytoplasm, the " blastophore" 

of Blomfield. It is uncertain whether a cytoplastic 

blastophore is left in all cases of spermatogeny by budding; 

and the differentiation in this case from mode (a) is difficult. 

Comparing the holoblastic and the centrolecithal ova, the 

segmentation of the zygote in Euflagellates and in Noctiluca, 

we can fully realise of how little general import, physiological 

or morphological, is the presence of the non-nucleated 

blastophore. 

(c) The third mode of spermatogeny occurs in the Sponge 

Grantia (Sycandra), 8 the Mollusc Helix, and some Vertebrates. 

Here, at an early stage of gametogenic fission (at the 

first bipartition in sponges), one nucleus undergoes no further 

divisions, and can only have a nutritive (or protective) function 

henceforward. In most cases the spermatogonium is attached 

by the basal cytoplasm in which this nucleus lies; the other 

nuclei pass to the free end of the cell, and henceforward sper- 

1 

We may correlate the absence of a flagellum here, as in most Arthropods 

also, with the absence of cilia in the tissue-cells, and the complete chitinisation 

of the body. 

3 

" Spermatogenese bei Saugethieren," in ' Arch. f. mikr. Anat.,' Xsi, p. 236. 

Unfortunately Ebner's views are contested, and the matter is unsettled. 

3 

And in Spongilla fluviatilis; see R. Fiedler, " Ueb. Ei- und Samenbild. 

bei Spongilla fluviatilis," in 'Zeit. f. Wiss. Zool.,' t. 48. In this 

group the ' nutritive cell' forms an investment to the brood of spermatocytes. 

VOL. XXXIII, PART I. NEW SEE. D


matogenygoes on by budding as in mode (6). The spermatozoa 

become free and leave behind a uninucleated blastophore, 

which is not known to be capable of further growth or division. 

We may fairly connect this peculiarity with the attachment of 

the spermatogonia in most cases, the nucleated blastophore 

serving as an active intermediary for the exchanges between 

the wall of the tube and the developing spermatozoa. And 

this is a character of adaptation, of no morphological, and of 

minor physiological importance. 1 I annex a schema (Fig. 8) of 

a spermatogonium of this kind, in which four divisions are 

supposed to have occurred. Owing to the fate of one of the 

• 2 4 " 1 = 8 spermatozoa. 

N N l nucleated blastophore. 

Pie. 8.—Schema of spermatogeny, with formation of nucleated blastophore; 

Grantia type. 

first two nuclei the number of spermatozoa formed at the 

nth bipartition of the nucleus is only 2""" 1 , instead of 2", 

i. e. only half the normal number. 

2, Oogeny. 

The Metazoan oogonium, the "ovarian egg" or u ovum" of 

authors, is peculiar in attaining an enormous size, owing to its 

power of storing up reserve supplies in the form of unorganised 

yolk-granules to supply the metabolism of the future embryo; 

and, correlated with this, it usually possesses an immense 

1 Our interpretation of the nucleated blastophore, as a nutritive organ 

rather than as an excretion, is confirmed by the fact that the numerous 

broods of Rat spermatozoa, formed by mode («), contract a union with a basal 

cell; and this syncytium is undistinguishable from the apocytium of the 

Bpermatocytes and nucleated blastophore in mode (c).


vesicular nucleus, the germinal vesicle, with its chromatic 

elements concentrated and fused into a spheroidal mass, the 

germinal spot, supported by a delicate network of " intranuclear 

protoplasm," "nucleo-hyaloplasm," or "linin." In 

the structure of its nucleus the ovum recalls the only other 

cells that enjoy a prolonged life uninterrupted by fission, and 

that attain to an equally large size—somatic ganglion-cells. 

The first symptom that marks the maturity of the ovariau 

ovum and its return to active life is the disappearance of its 

nuclear wall, and the merging of part of its " achromatin" 

contents, together with the true nucleoli, in the cytoplasm; 

while the chromatic elements of the germinal spot become 

separate as rods. It is to this process and stage that we must 

refer the elimination of mere trophic elements from the 

nucleus of the ovum—a process in many ways comparable to 

the disorganisation of the meganucleus of the conjugating 

Ciliates. There is every reason to believe that the nucleus of 

a cell destined to lie quietly feeding and fattening for days, 

months, years, or decades, must be of a very different character 

from one that has to undergo rapidly repeated fission; in 

other words, between a purely anabolic and an essentially 

katabolic nucleus. If we accepted Greddes and Thomson's 

view, 1 that there are actually entities that we can term 

anastates and katastates, we should have to reject their conclusions, 

and say that this preliminary disorganisation of the 

germinal vesicle is the elimination of its anastates : for henceforward 

all the phenomena manifested are katabolic, even 

without the advent of the male; and in ova which are not 

parthenogenetic the resumption of anaboly is henceforward 

impossible. This process is to some extent comparable 

with the elimination of the trophic element of the spermatogonium, 

the blastophore, nucleated or non-nucleated j 

but the parallel is a very remote one, and purely physiological. 

1 A view which I no more accept than I do Sachs's view, that roots are 

formed at the base of a wallflower and flowers at the top by the migration 

downwards of "root-forming," and upwards of "flower-forming substances" 

(Wiirzel und Blumen-bildende Stoffe).

52 MAROtJS M. HAKTOG. 

In the present case the trophoplasm eliminated from the 

nucleus passes into the cytoplast, and is utilised, not excreted. 

The chromatic elements of the nucleus now become more or 

less free, and in anticipation of two mitoses undergo two successive 

longitudinal fissions. 1 This is, as 0. Hertwig shows, 

only an anticipation (comparable with precocious segregation 

in embryonic development) of the subsequent mitoses, 

which follow one another in rapid succession with no interval 

of rest in the vesicular state separating the first 

from the second, as is usually the case between two successive 

mitoses. 

The nucleus is at this time peripheral. A mitotic spindle 

is formed with its axis concurrent with that of the ovum. A 

very uneven cell division now takes place, the smaller cell 

being apparently hudded off from the larger, which retains the 

name of the ovum, the smaller being termed the "first polar 

body." The nucleus of the first polar body then passes into a 

resting state in some animals. What we may term the 

secondary nucleus of the ovum at once forms a second spindle, 

and a " second polar body" is budded off like the first. The 

nucleus produced in the egg by this second mitosis is the 

gametonucleus, the egg being now converted into the 

oosphere. In most animals 3 the process is made symmetrical 

by the division of the first polar body into two. In this case 

the brood consists of four gametes, three arrested and one 

functional. When three polar bodies are thus formed the 

nuclei of all four cells are exactly similar and equivalent. 

The only difference between the polar bodies and the oosphere 

lies in their cytoplasts. Adopting the usual nomenclature of 

mother- and daughter-cells, the relationships here may be 

noted thus : the oosphere and second polar bodies are sisters, 

1 

This account is taken from A sea ris megalocephala. It is by no means 

certain that the peculiar characters of the two mitoses here are universal, 

though they have formed the chief morphological base for a very big theory. 

Similar " anticipated " mitoses, however, occur in spermatogeny also. 

2 

Coelenterates, Molluscs, Vermes, and Vertebrates, according to 0. 

Hertwig.


and both are nieces of the first polar body. I append a schema 

to show these relations (Kg. 9). 1 

No 

Fie. 9.—i. Schema to show usual formation of polar bodies in Metazoa. 

ii. Schema of polar bodies iu Ascaris. 

Unmistakably these processes point to a primitive condition, 

when each ovarian ovum divided in two stages to form a brood 

of four oospheres. Unfortunately the phenomena of the 

gametogenic bodies have been made too much a study isolated 

from other similar formations, and false interpretations have 

been put on the peculiarities of their mitoses to suit preconceived 

ideas. Doubtless had the segmentation of the Metazoan egg 

proceeded after the type of Cystoseira (supra, p. 17), ingenious 

hypotheses would have been framed to explain what 

plasmic properties resided in each of the seven nuclei rejected, 

and for what reason each one had to be expelled from the egg 

to leave a pronucleus fit for fertilisation. 

The remarkable uniformity of oogeny (in the restricted 

sense) in the Metazoa as compared with other equivalent 

groups is perhaps attributable to the fact that its processes 

are usually limited to the short time during which the ovum 

is free before fertilisation, and to the fact that it is usually 

free at that time: a uniformity of external conditions has 

preserved uniformity of results. The much greater variability 

of spermatogeny which takes place under much more varied 

conditions supports this view. 2 

1 

Blochmann has found in some Insects that the second polar body divides, 

but not the first (" Zahl d. B.iclituugsk6rper,'.&c," in ' Morph. Jahrb.,' 18S9). 

s 

I have omitted the consideration of " paracopulation " iu the "winter 

eggs" of Cladocera, as described by Weismann and Ischikawa (in ' Zool. 

Jahrb.,' "Abtheil f. Anat. u. Ontog. d. Thiere," iv, pp. 155—196), In

54 . MAEOTJS M. HAE.TOG. 

Though we are now considering gametogeny, we must turn 

aside to note that in most cases of so-called " parthenogenesis " 

of Metazoa only one polar body is formed, and the ovum, 

rather a progamete than an oosphere, segments and develops 

directly. We revert to this process below in its proper 

place (p. 74). 

We must, however, note that in some cases the true oosphere, 

differentiated by two mitoses (i. e. the formation of both polar 

bodies), is a facultative gamete, and may develop without 

fertilisation; this has been demonstrated in Liparis dispar 

and some other Lepidoptera, and in the Hive Bee (Apis 

mellifica); and in the last case the produce of the unfertilised 

oosphere is always a male or drone. This is proof conclusive 

that the formation of polar bodies is not necessarily an 

elimination of male elements or " katastates ;" on the other 

hand, it would work in well with the very old view that in 

bisexual union the " superiority " of one parent determines 

that the offspring shall be of the opposite sex. But such 

considerations are outside the limits of our theme. 

VI. A GENERAL VIEW OF GAMETOGENY. 

Before summarising the results of our systematic survey 

we have to consider several points of general bearing. 

A. The Reduction of the Chromatomeres in 

Gametonuclei. 1 

A frequent, but certainly not universal, process in gametogeny 

is the reduction of the number of chromatomeres or 

these eggs, destined to form the two polar bodies and to be fertilised by a 

spermatozoon, a portion of the nucleus is segmented off before maturity 

and remains in the egg, ultimately to fuse with one of the segmentation 

nuclei at tbe first or third segmentation. I confess myself unable to explain 

this fact, or bring it into line with other phenomena of gametogeny. 

1 

Most of the details of this section are taken from Strasbiirger, 'Kernund 

Zelltheilung' (1888), and from K. Hertwig's paper cited above; and during 

the impression of this paper I have consulted Guignard's " Sur la Consti-


rods, into which the chromatin of the nucleus resolves itself 

in the early stages (prophases) of mitosis. 

It appears to be the rule that, apart from gametes and their 

antecedent cells, all the nuclei of a given species have the same 

number of chromatomeres; each of these during mitosis splits 

into two, lengthwise, and one half goes to each daughter-nucleus. 

In most flowering plants the normal number of chromatomeres 

in the vegetative cell is 16; at a certain stage, anterior 

to the gametogonium proper, the chromatin wreath (which 

had shown 16 rods at its formation) now segments in its prophases 

into a smaller number than were present in the metaphases 

and anaphases of the previous mitosis, which number 

is perpetuated in the gametogonia and gametes. Thus in 

Helleborus and most Liliacese the reduced number is 12, 

two thirds the original; in the Liliaceous genus Allium it is 

8. But in Convallaria (Lily-of-the-valley), also belonging to 

the same order, there is no reduction, and in Muscari (Grape 

Hyacinth) it is raised to 24. In Orchids, also, no reduction 

has been observed. 

The cell in which this reduction first takes place does not 

appear fully determined in all cases; but we know this much, 

that in the male (anther) it furnishes vegetative as well as 

reproductive offspring. For it occurs, according to Guignard, in 

the pollen mother-cell, which forms four pollen grains, each 

to produce a vegetative and a gametogenic nucleus. All 

these perpetuate the reduced number of chromatomeres by 

normal mitosis. 

In the female (ovule) this reduction is first shown by the 

original nucleus of the embryo-sac. In some cases, at least 

(Lilium Martagon), Guignard, whose recent account is 

slightly different from Strasbiirger's and from his own previous 

statements, has shown 1 that the normal number of chromatotution 

des Noyaux cellulaires chez les V6g6taux," ' Comptes Rendus,' May 11, 

1891. See also Boveri's " Zellen Studien : Verlialten der chromatischen Kernsubstanz 

b. d, Bildung der Richtungskorper u. b. d. Befruchtung," in 'Jen. 

Zeit.,' 1890. 

. i " Nouvelles Recherches sur le Noyau cellulaire," in ' Ann. des Sei. 

Nat. Bot.,' ser. 6, xx, p. 334, and ' Const, des Noyaus:'

56 MAROUS M. BARTOG. 

meres in the vegetative cells is 24 ; x that of the progametal and 

gametal nuclei, 12; and the "basal nucleus" produced at the 

first division of the nucleus of the embryo-sac reverts to 16 

for itself and its offspring, so that of the two gametonuclei 

that conjugate to form the endosperm nucleus the lower has 

the normal, the upper the reduced., number of chromatomeres. 

In the liverwort Riella Clausonii, 0. Kruch has found the 

number 8 constant for the inner cell of the antheridium and 

its brood-cells, and the oosphere; the first two cells of the 

embryo have each 16 chromatomeres; but whether the latter 

number is characteristic of the tissue-cells, and the number 

found in the spores, has not been made out. 

In Metazoa the reduction appears usually to take place in 

the gametogonium, and is much more uniform in most animals 

than is demonstrated for plants, 2 the number of chromatomeres 

being here usually one half the normal; consequently in 

karyogamy or fertilisation as spermato- and oo-nucleus each 

brings an equal number of chromatomeres, the zygote nucleus 

and its offspring reverting to the number characterising the 

species. 3 This, however, is not always the case; for in Arion 

empiricorum (the Cellar Slug) there are numerous chromatomeres 

in the oo-nucleus, but two only in the spermatonucleus. 

4 

The schema of mitosis is sometimes modified in the animal 

gametogonium, the longitudinal splitting of the chromatomeres 

taking place earlier than usual, and even being doubled, so as 

to produce four times the (reduced) number of chromatomeres. 

In this case, which occurs notably in both the male and female 

gametogonia of Ascaris megalocephala, the longitudinal 

splitting does not, of course, occur again in the successive 

gametogenic mitoses; but the chromatomeres, thus formed in 

1 Not 16 as given in his previous paper. 

2 In ' Malpighia,' vol. iv (1891). Professor Strasbiirger kindly directed my 

attention to this paper. 

3 It must be remembered that the numbers have only been counted in very 

few cases—at the outside twenty or thirty. 

4 See Platner, "Ueb. d. Befr. bei Arion empiricorum," in 'Arch, f, 

mikr. Anat.,' vol. xxvii.


advance, are only evenly distributed between the daughtercells. 

This obviously, as stated, is only another way of distributing 

the segments formed. If in the schema B, C, represent 

two of the chromatomeres of the gametogonial nucleus, 

B 1 , C 1 —B 2 , C 2 , those produced by their splitting, and the 

dotted lines the cell divisions, we see that the sole difference 

needed to change this into a schema of ordinary cell division 

would be to prolong the middle dotted line back to the level of 

B 1 , C 1 —B\ C 1 . 

/B a , C 3 

58 • MARCUS M. HARTOG. 

asexual spores in Archegoniate Cryptogams. Hence we may 

be allowed to conjecture that the reduction also takes place 

in the latter group ; and, by parity, that it is not confined 

to gametogonia, but will be found in all mothercells 

destined by multiple fission to give birth to a 

brood of reproductive cells. In that case the return to 

the normal number of chromatomeres would necessarily be 

effected by the slow process of nutrition in asexual spores 

or their offspring, instead of by the direct process of 

summation in the case of gametes. This would give a clear 

insight into the action of karyogamy in bringing about rapid 

and complete rejuvenescence. 

The question of the individuality of the chromatomeres and their persist, 

ence, as maintained by Boveri and Rabl, should find its treatment here ; but 

I have not yet completed a research bearing on this point. I therefore confine 

myself now to the statement that, with Hertwig, I believe the evidence 

very inadequate for the support of the theory that the chromatomeres have 

distinct and persistent individualities. Professor Strasbiirger has written me 

a letter to the same effect, though he had advocated Rabl's views in his 

' Kern- und Zelltheilung.' 

B. On the Reproductive Incapacity of Obligatory 

Gametes. 

The reproductive incapacity of gametes is no exceptional 

phenomenon among cells, nor is it brought about only in the 

differentiation of gametes. It occurs in other cases throughout 

the Metaphytes and Metazoa, and we have instances of 

its existence as low down as the Colonial Flagellates. In the 

genus Volvox all the numerous cells of the colony other than 

the few ''germinal cells" (parthenogonidia, oogonia, or spermatogonia), 

perfect flagellates equipped with eye-spot, contractile 

vacuoles, and nucleus : all these, I say, are affected 

by that very reproductive incapacity which is the character, 

istic of the gametes, while they lack the potentiality of 

karyogamic rejuvenescence possessed by the latter. In 

the majority of Metazoa and Metaphytes the tissue-cells as a 

rule suffer from the same impotence in virtue of their differ-

SOME EBOBLEMS.Of BEPRODUCTION. 59 

entiation, so that the indefinite reproductive capabilities of the 

cells of Mosses and BegoniaSj Coelenterates and Flat-worms 

are usually cited as exceptions to the rule; though the indefinite, 

if not unlimited, capacity for fissile reproduction 

must have been primitively inherent in every cell. The limitation 

of this power in most Metazoa occurs at a very early 

stage if the brilliant results of Chabry 1 prove to have a general 

application^ for he has shown that in Tunicates the destruction 

of a single blastomere may determine the absence of the 

organ it should produce. 

C. The Adaptation of Gametes to Different Fates. 

Our next subject for parallel is the arrest or degradation of 

certain gametes of a brood, or, if we please, the favouring of 

single gametes of a brood at the expense of others. This is a 

common phenomenon of the struggle for existence between 

members of a colony, whether cells, organs, zooids, or even 

individuals, especially those destined for reproduction. Thus, 

in the ascus of the Truffle four to six spores are formed endogenously, 

but usually only one matures. In the Heteror 

sporous Filicinese sixty-four megaspores are formed (in 

sixteen tetrads) in each megasporange; but only one matures, 

the other sixty-three undergoing complete disorganisation. In 

Eleocharis and other Sedges the pollen mother-cell undergoes 

two unequal divisions, just like the Metazoan ovum, and 

produces a single fertile pollen grain and three abortive ones. 

The ovarian ovum of Hydra attains its full size by devouring 

all the others in the ovary, and in many Arthropods the fertile 

ova develop at the expense of others. In Ascaris megalocephala 

some of the ova and spermatogonia are sacrificed and 

abort in the germ-tubes (0. Hertwig). In Vertebrates also 

many of the primitive ova are degraded to mere food material. 

As for Organs and individuals, in Gymnosperms several 

archegonia may be formed and fertilised in each embryo-sac; 

1 

" Embryologie Normale et T6ratologique des Asoidiens Simples," in 

'Robin's Jour». del'Anat./1887, p. 167.

60 . MABCTJS M. HABTOG. 

nay, in some cases the oosperm or zygote in each archegonium 

by early fission produces four embryos; and yet only one 

embryo ripens in the seed. In Angiosperms the proportion of 

matured seed to ovules and carpels varies very greatly. In 

Anemone several ovular origins are formed, but only one 

ovule attains full size in each carpel; in Drupacese two 

ovules are present, but only one ripens into a seed, the exception 

constituting the well-known " Philippina " of stone-fruit. 

The one-seeded Acorn is the outcome of an ovary with three 

biovulate carpels. 

The fate of the central procarpia or oogonia of Co rail in a, 

reduced to the position of mere agents for the transmission of 

the male substance, finds a parallel in the peculiar transformation 

undergone by the showy sterile peripheral flowers in the 

inflorescence of Viburnum, Hydrangea, and some Composites, 

into mere signboards, attracting the insects whose 

visits fertilise the less conspicuous central flowers. The petals 

of many flowers (e.g. Ranunculaceae) are merely the 

degraded sterile outer stamens. 

Iu the animal world severe competition exists between 

embryos in those Molluscs which have numerous eggs in a 

single capsule. Here the first larvae to hatch out in the veliger 

stage eat up their more tardy brothers and sisters. 

We may note that some of the nuclei produced by the 

zygote nucleus of the exconjugate Ciliate are rejection-nuclei, 

and fail to take any share in the life of its offspring. 

D. Summary of Gametogenic Processes. 

1. In many Protozoa the gametes are apparently ordinary 

individuals or swarmers, the product of normal fission or 

brood-formation. 

2. In many Phytomastigopods and Protophytes the gametes 

differ from ordinary zoospores in being produced by more 

rapidly repeated acts of fission or segmentation, and in their 

smaller size.


3. When the gametes are unequal the males are usually 

the product of a more complex segmentation than the 

females. 

4. The number of repeated fissions to form the oogametes 

from the oogonium varies, and the divisions may even remain 

in abeyance and the oogonium assume directly the character 

and functions of an oosphere (Volvox, Moridese, Cycas). 

5. Owing to adaptive modification only one gamete of a 

brood may be fertile, and the rest aborted, either arrested, 

or degraded into accessories of the sexual process. Thus in 

Metazoa out of a brood of four gametes three are arrested as 

polar bodies. In the Archegoniate Cryptogams, Conifers, 

and Gnetacese, a similar formation of a single fertile oosphere 

takes place, but the infertile gametes are degraded to form the 

channel for the transmission of the spermatozoon. 

6. The gametogenic divisions may only affect the nuclei, 

cytoplastic fission remaining in abeyance. In such cases 

arrested gametonuclei may remain (a) in the periphery of the 

protoplasm of the fertile one (polar bodies of many Arthropods); 

(b) be digested, ejected, or excreted (certain Ciliata and 

Fucacese), or simply degenerate in situ (periplasmof Peronospora, 

Ophryocystis). 

7. The number of such rejection-nuclei is determined by 

two factors : (a) the primitive number of gametes in the brood; 

(6) the number of fertile gametes formed and requiring nuclei. 

Thus in Pucacese, where eight is the primitive number of 

gametes, four, six, or seven sterile nuclei are eliminated, 

according as the number of fertile oospheres produced in the 

oogonium is four, two, or one. 

8. Hence it follows that the number of arrested gametes (or 

rejection-nuclei), being variable, can have no universal physiological 

significance. 

9. While the specialisation of gametes by fission is the 

rule, gametogenetic fissions do not occur when a vegetative 

cell undergoes direct conversion into an oosphere. 

10. In some Apocytial Plants the gametes are formed by 

the resolution of the apocytium into uninucleate cells,

62 . MARCUS M. HAHTOG. 

either directly or after preliminary division of the nuclei 

(Cladophora). 

11. In some Apocytial Plants the gametonucleus (whether 

of iso- or oo-gametes, but not of spermatogametes) is the product 

of the union of several nuclei, either the ordinary vegetative 

nuclei (Dasycladus), or the offspring of the vegetative 

nuclei by antecedent mitotic divisions (Peronospora). In 

both cases the gametes are obligatory. 

12. Hence preliminary nuclear division is not a necessary 

antecedent to the differentiation of obligatory gametes. 

13. Since the nuclei formed in heterogeneous gametogeny 

(§§ 5—7) are all similar, and contain (in every case when the point 

has been worked out) an equal number of chromatic elements, 

we conclude that the difference between an arrested and a 

functional gamete lies in their cytoplasm, not in their nuclei 

(0. Hertwig). 

14. The alleged "processes of excretion" antecedent to 

fertilisation and incidental to gametogeny are neither universal 

nor uniform. Under this head we may group the following 

processes, which I have made to include all cases where part 

of the gamete takes no share in the formation of the zygote. 

(a) Part of the oogamete is utilised in the formation of a 

receptive or transmitting organ for the male; of this character 

is the trichogyne in Coleochseteaa and Floridese; 

the beak with its mucified cytoplasm in Oedogoniese (and 

Vaucheria?). 

(b) The formation of non-nucleated epiplasm by isogametes, 

originally referable to a formation of cell-walls, which remains 

in abeyance, in some apocytial plants (Cladophoreae and 

Protomyces ; found also in similar formation of the asexual 

zoospores). 

(c) The cutting off of a wall of cytoplasm around the central 

vacuole of an apocytium or cell (Acetabularia, Botrydium, 

and Ulothrix). 

(d) A similar excretion to (b) of non-nucleated protoplasm 

from the oospores of Saprolegniese, afterwards resumed by 

them; the same process occurs with the asexual zoospores.

SOME PROBLEMS OF REPBODTJOTION. 63 

(e) The non-utilisation of all the cytoplasm in the elaboration 

of the flagellate (or ciliate) spermatozoon from a tissuelike 

cell, leaving anon nucleated residuum (higher Cryptogams 

and some Animals). 

(/) The leaving over of a central portion of cytoplasm, as a 

non-nucleate blastophore, in the modified sperm morula, 

where budding replaces true segmentation (Lumbricus, 

Metazoa, &c). 

(g) The differentiation of the basal cell of one of the earlier 

stages of the fission of an attached sperm atogonium as a 

nucleated blastophore (Helix and some Vertebrates ; it is 

the first daughter-cell of the spermatogonium in Sponges). 

(h) The abortion of some of the spermatogonial or oogonial 

cells (Ascaris). 

(i) The abortion of some of the gametes of a brood as 

" polar bodies " in the Metazoa, owing to one appropriating 

the greater part of the cytoplasm. 

(A) The abortion of some of the gametonuclei, with or without 

a minimal quantity of cytoplasm, as rejection-nuclei 

(Ciliate Infusoria and some Fucacese). 

. (I) The degradation of some of the oogametes or progametes 

of a brood to serve as transmitting media for the spermatozoon 

(canal-cells of Archegoniates and Gymnosperms). 

(m) The retention of numerous gametonuclei in the peripheral 

part of the apocytial cytoplasm, which is destined to 

form an outer investment around a single central gamete 

when transformed into the zygote (Peronosporese and 

Ophryocystis?). 

(n) The first formation of sterile cells in the pollen grain of 

Gymnosperms, and of a vegetative nucleus in those of Angiosperms 

representing the formation of a vegetative prothallus, 

and having no real connection with the subsequent gametogenic 

divisions of the other or sexual nucleus. 

(o) The non-utilisation of some of the gametonuclei formed 

in the pollen-tube of the Siphonogamous Metaphytes, and 

the antheridium ofPeronospora. 1 

1 This case finds a close parallel in the formation of the innumerable sper-

64 MAUCtJS M. HATJl'OG. 

We see that these processes fall into several distinct classes, 

which cannot be at all homologised morphologically or physiologically,, 

(a) is a type quite apart; (b) (c) and (d) are 

modifications of one and the same process; (e) (/) and (g) 

again may be grouped together, though a nucleus is lost in 

(g), but not in the two other types; (h) (i) and(k) again form 

a similar group united by homoplasy, to use the term that 

Lankester introduced to denote the similar products of similar 

physiological conditions, irrespective of common origin ; (I) is 

distinct, showing a certain analogical relation to (a); (m) 

stands alone, and so does (n); (o) is only brought into the 

present relation because of the false homologies to which it 

has given rise. 

15. From the above it follows that excretion of protoplasm is 

no essential condition of gametogeny. 1 

VII. THE CAUSES OF PROTOPLASMIC SENESCENCE AND 

ULTIMATE REPRODUCTIVE INCAPACITY. 

Maupas has established an important fact which sheds a 

flood of light into a very dark corner of biology. In the 

Ciliata, the offspring of a long-continued series of fissions 

ultimately degenerate, and lose first the power of entering 

into the conjugation that would rejuvenate them, and finally 

that of further fission. This degeneration he terms SENES- 

CENCE. We have evidence on all sides to show that 

asexual reproduction, colonial or cellular, is rarely continued 

indefinitely in those organisms which have a sexual 

process. After a certain continuance of asexual reproduction 

the strain deteriorates, as Andrew Knight showed a century 

matozoa in many mammals, where only one fertilises the single ovum. Yet 

no one has suggested that the others are excretion products. 

1 From the above summary it is obvious that Waldeyer fails utterly in his 

contention that Biitschli's identification of the formation of polar bodies 

" must fall to the ground if it be established that sperm mother-cells also 

give rise to polar bodies," since the "polar bodies" or "excretions" in 

spermatogeny are neither universal nor fully homologous with one another, 

nor with the formation of polar bodies in the egg.

SOME PROBLEMS OF EEPRODUOTION. 65 

ago. The one case which occurs to me, writing in Ireland, 

is the Champion Potato, which proved the salvation of the 

country after the great famine by its resistance to the 

"blight" (Phytophthora vastatrix), but which after forty 

years has now completely lost this resisting power. Again, we 

have ample direct evidence for regarding the apparently "resting 

" nucleus in a cell as having the same sort of relation to the 

cytoplast as a nerve-centre has to an organism, 1 a view supported 

too by the fact that the nucleus approximates in 

chemical composition to nerve substance, being richer in 

lecithin and phosphorus generally than the cytoplasm. Now, 

in ordinary cell division, on the principle of continuity, there 

is no essential chauge in brood-cytoplast and brood-nucleus, 

and the result of repeated cell fission is merely a multiplication 

of these. But we know that a nerve-centre ceases to 

respond readily to a continued or repeated stimulus of the 

same kind. It would seem then probable that, after a prolonged 

association in life continued through a series of fissions, 

the nucleus would respond less readily to the stimuli 

received from the cytoplast; consequently its directive powers 

would be diminished; and conversely the protoplasm would do 

its work more imperfectly; the nucleus again would be less 

nourished; and a vicious circle of deterioration would set up 

in the cell, ending in senescence and death. Maupas has told 

us that in the senescent Ciliata the cell-body is dwarfed and 

deformed, the nuclear apparatus reduced and degenerated. 8 

1 Cf. Haberland's researches on the behaviour of the nucleus in the activity 

of the vegetable cell; Griiber's on artificial division of Ciliata; Eimer has 

even adduced evidence to show that in nerve-centres themselves the nuclei of 

the ganglion-cells play the part of primary centres (" The Cell-nucleus as 

Central Nervous Organ," in 'Organic Evolution' [Bng. Trans.], p. 349). 

" The recent researches of Fol (' Comptes Rendus, 1 April 20, 1891), 

Guignard (' Comptes Rendus,' March 9 and May 11,1891), and Flemming 

('Arch. f. mikr. Anat.,' t. xxxvii, pt. 2) complete the evidence that the "centrosome 

" of Boveri plays an essential part in mitosis and karyogamy; and the 

phrase "nucleus and centrosome" should in this section be used to replace 

" nucleus" wherever it is used in antithesis to cytoplast in the present discussion. 

VOJ,. XXXIII, PART I NEW SEE. E


Parallel cases of failure by continued association are numerous, 

both in organic life and in human affairs. Seed raised on 

the same soil for several generations yields stronger plants 

when transferred to a different soil or another climate. In a 

great business the disadvantages of too unchanged a management 

or a staff are recognised. 

As cell multiplication is essentially an exhaustive process, 

requiring nutrition to compensate for the losses incurred by 

the active metabolism involved, it is obvious that any acceleration 

of the rapidity of the fissions and reduction of the 

interval of recovery of the cell must necessarily weaken the 

organism in a sort of multiple ratio, and so precipitate 

degeneration. 

In this way we can see how the reproductive incapacity of 

obligatory gametes may be frequently effected merely by the 

rapidly succeeding fissions that differentiate them. The replacement 

theory of Balfour is true in its main proposition, 

that the formation of polar bodies is a process whose object 

is to prevent parthenogenesis; though not by the mechanism 

he implies, the removal of a male element. The rapid cell 

divisions, uninterrupted by any interval for nuclear rest and 

reconstitution, must precipitate and accentuate reproductive 

incapacity—a view which is essentially 0. Hertwig's. 1 It is 

probably due to this physiological gain to the race that the 

page of morphological history, revealing that the oogamete 

was primitively one of a brood of at least four, has not been 

obliterated from the ontogenetic records of the Metazoa. 

From the standpoint that a well-constituted cell should be 

capable of doing anything that any cell can do—feeding, 

moving, growing, dividing, and so on—our specialised gametes 

are indeed stricken with utter degeneration; for they can 

neither feed, move (as far as the oogamete is concerned), 

grow, nor reproduce their kind, but as individuals are doomed 

to death or to the extinction of their individuality in a zygote. 

1 

But it does not seem made out or even probable that in gametogeny the 

nuclear divisions proceed, as a rule, in tbe same breathless hurry as in Asoaris 

megalocephala; they certainly do not in the Angioapermous embryo-sac.


VIII. PROTOPLASMIC REJUVENESCENCE, 

ITS NATURE AND MODES. 

From the degeneration and loss of constitutional vigour 

produced by the over-prolonged association of nucleus and 

cytoplast, unchanged through a long chain of fissions, the 

escape lies through a REJUVENESCENCE of the " firm," as we 

may term them. And this is effected in various ways. 

A. THE MODES OF REJUVENESCENCE. 

1. REST from a given stimulus is sufficient to rouse again 

the irritability of a nerve-centre when not unduly fatigued. 

Even the operative weaver or working engineer, who from 

constant habit is barely conscious of the unceasing din of the 

machinery, would feel it afresh after a few weeks' absence. 

And in the resting cell the nucleus has, moreover, the opportunity 

of complete nutritive restoration. In the agamous 

Monadinese, resting states, more or less prolonged and 

accentuated, separate the stages of active growth and fission. 

Here, too, as so often occurs in plants of higher organisation, 

the more marked resting state usually precedes a recrudescence 

of active cell division. 

2. CHANGE OF THE MODE OF LIFE is another mode of bringing 

about an harmonious readjustment of the relations of 

nucleus and cytoplast. It may be accomplished by mere 

POLYMORPHISM, or by HETERCECISM, the change of host, so 

frequent in the life cycles of parasitic organisms. Marshall 

Ward has drawn attention to this in the case of the higher 

Fungi which are so frequently apogamous. 1 

3. NUCLEAR MIGRATION, i. e. the transference of a nucleus 

to a portion of cytoplasm with which it has not been asso- 

1 " On the Sexuality of the Fungi," in ' Quart. Journ. Micr. Sci.,' 1884; 

see pp. 59, 60 (of reprint) especially, where Ward compares the sojourn in a 

new host " to a trip to the sea-side, where the weary and enfeebled organism 

enjoys fresh diet and associations for a time, which in their turn pall and 

prepare their recipients to renew old modes of life."

68 MAECUS M. HAETOG. 

ciated, may occur in apocytial plants, as through the clamp 

connections 1 and anastomoses of the Fungi with septate 

hyphse. 

4. PLASMODIUM FORMATION, that is the cytoplastic union of 

cells without nuclear fusion. This, of course, brings about 

complete mixture of the cytoplasts, comparable to that of the 

nuclei in karyogamy, and which we have termed plastogamy. 

The nuclei are thus furnished with totally new cytoplasts on 

the resolution of the plasmodium into cells. This is a more 

thorough-going process than the preceding, and occurs in 

agamous plants only. It is generally held that karyogamy 

arose as an advance on this process. 

5. KARYOGAMY, or the fusion of two or more nuclei as well 

as of their cytoplasts into a uninucleate cell, the zygote. In 

binary union the cytoplast of one of the gametes may be practically 

nil. 

6. THE FUSION OF APOCYTIAL GAMETOIDS. We distinguish 

this for convenience' sake, as we know nothing of the cytology 

of this process ; but it must ultimately fall under the head of 

plasmodial formation or karyogamy; possibly the cytological 

details may vary even from species to species. 

B. THE ADVANTAGES OF KARYOGAMY AS COMPARED WITH 

AGAMY AND APOGAMY. 

If the rejuvenescence due to karyogamy be of the nature I describe, 

that is, the formation of a nucleus new to the cytoplast 

with which it is associated, a change in the constitution of the 

"firm " and " staff," to speak metaphorically, the consequence 

should follow that, by introducing a suitable nucleus into an 

empty cytoplast, we ought to obtain the same rejuvenescence 

1 

These are formed by lateral outgrowths above and below a septum, which 

meet and anastomose to form an open loop round the barrier. 

5 

Ward, op. cit., p. 58, regards the sexual process as " consisting essentially 

in the invigoration of the protoplasm ;" but in the preceding pages he clearly 

shows a belief in replacement theories. But his statement" that the sexuality 

of the higher fungi has disappeared, because its purpose has been equally well 

or better attained otherwise than by means of sexual organs," is fully in the 

spirit of the views advocated here,

SOMB PROBLEMS OF REPRODUCTION. 69 

as in karyogamy. And this very feat has been accomplished ; 

for the Hertwigs some years ago showed that Echinoderm 

eggs when shaken up in sea water break into fragments ; and 

observed a spermatozoon entering such a non-nucleated fragment 

and segmenting therein, like the zygote segmentationnucleus. 

Since then, as O. Hertwig recalls in the above-cited 

paper, 1 Boveri has repeated the observations, and proved that 

the normal tnorula was formed and developed into a larva. I 

do not see how this is consistent with any theory of karyogamy 

but Biitschli's—that it is a process of rejuvenescence, to which 

term we are now endeavouring to attach a definite connotation. 

Our definition of rejuvenescence, karyogamic or other, 

is that it is essentially a process of constitutional 

invigoration, 2 as its converse, senescence, is one of constitutional 

enfeeblement. We can now, grasping this idea, understand 

the continued existence of agamous and apogamous forms 

side by side with those where not merely karyogamy, but allogamous 

sexual reproduction is essential. Every arrangement 

that makes for protection and comfort tends to become by habit 

indispensable,and the privation of such an "acquired need" 

may produce effects none the less disastrous because it was acquired, 

and not primitive. A couple of examples from human 

life will illustrate this. The Maoris found scant clothing necessary 

in their cool but not extreme climate until the Europeans 

introduced blankets; but now their occasional reversion to the 

practice of going unclothed is said to lead to disastrous results. 

Civilised nations who cook their food largely escape the attacks 

of entozoa : but, on the other hand, when they do occur, 

these attacks disturb and disorder the system the more 

seriously for their rarity; while the Abyssinian, who feeds 

daily on raw beef, thinks it positively unlucky to be without 

a tapeworm in his intestines. The coexistence of agamous, 

karyogamous, and apogamous types proves that the need for 

karyogamy belongs to the class of acquired needs or necessary 

1 ' Vergleich der Ei,' &c, p. 85. I have not been able to consult Boveri's 

original paper in the libraries of our scientific societies. 

3 Of course I use " constitutional" in the medical sense.


superBuities—all but indispensable to those that can obtain 

them, not missed by those that have never known them, and 

capable of being laid aside in time by a few of the former class. 

Conversely, referring karyogamic rejuvenescence to mere constitutional 

invigoration, we can see that agamy and apogamy 

are harmless conditions where other modes of rejuvenescence 

prevail. 1 

C. ALLOGAMY AND SEX. 

Again, if the invigorating effects of karyogamy be due to 

the mere infusion of new blood into the firm " Cytoplast, 

Nucleus, and Co.," it is, of course, an advantage that the new 

blood should be as new as possible within the limits of possible 

harmonious co-operation—that is, usually, within the bounds of 

the race or species. And this must have been the cause which 

determined exogamy in the lowest organisms. In this case 

the members of a brood of gametes are incapable of entering 

into fertile karyogamic union with one another, being affected, 

as we may say, by the disqualification of consanguinity. This 

disqualification has been attributed to a latent sexual differentiation 

; but to admit this view is, as we shall see at once, to 

deprive the word "sex" of the connotation of a differentiation 

of organisms into two complementary categories. 

For if exogamy implied any sexual differentiation in the 

ordinary sense, and we considered any twenty-six broods of 

gametes, say of Botrydium, they should fall into two categories, 

which we will term A—M, N—Z respectively; any of 

the gametes of the former category would be incapable of 

forming fertile union with any other of its own category, but 

would pair freely with any of the other, and vice versa. But 

1 It is interesting to note that Ferns, which are dimorphic, have a resting 

state (spore) interposed between the terrestrial Fern-plant and the palustrine 

prothallus, asexual karyogamic union between the palustrine and the terrestrial 

states. In some exceptional cases the one or other transitional form of rejuvencsceuceis 

omitted: in apospory the paluslrine form supervenes without the 

resting state of spores ; and in apogamy the terrestrial state supervenes without 

karyogamic rejuvenescence : but a combination of these two phenomena is 

uot known in the samespecies, or I think I may say the same group.

SOME PKOBLEMS OF REPRODUCTION. 71 

no two such categories exist; on the contrary, all the evidence 

goes to prove that a gamete of the A brood will pair with one 

of any other brood from B to Z, and so on right through the 

alphabet. Maupas has told us that for two Ciliates in the 

eugamic state to pair successfully they must belong to two 

different cycles of descent—that is, they must be descended 

from two different exconjugates. If we use the term sex for 

such cases as these we must admit the existence of as many 

sexes as there are broods or cycles of the species in existence, 

and that difference of sex means not a binary antithesis of 

characters, but a mere question of kinship, which is a reductio 

ad absurdum. 

We see, then, that exogamy is merely the expression of consanguineous 

incompatibility, or allogamy, as it has been long 

termed. So far from indicating latent sex, allogamy may 

or may not coexist with very high binary sexual differentiation. 

In Orchids, for instance, side by side with the majority of 

flowers adapted for cross-fertilisation exclusively, we find one 

or two species that are " autogamous" or self-pollinating. 

If we call allogamy by the name of " sex," it is a sex superimposed 

on ordinary binary sex, and distinct from it; and the 

question occurs here, in an allogamous species, How many 

sexes are we to ascribe to the innumerable individuals, each 

incapable of self-pollination, but capable of fertilising the flower 

of any other individual? 

We must remember, too, that in many isogamous forms, even 

those which are exogamous, like Acetabularia, conjugation 

may be multiple, as many as five gametes uniting into the 

single zygote. Admitting the supposition that exogamy involved 

latent binary sex, what would be the several functions 

of each of these five gametes? The only conclusion left us is 

the one we have stated, that exogamy expresses not an early 

form of sexuality, but a growing sensibility of the organism to 

the fact that the advantages of karyogamy are not fully gained 

by the union of closely allied gametes j and this fastidiousness 

we find an increasing factor as we ascend the scale of karyogamic 

unions.


D. THE ORIGIN OF SEX. 

If we seek for the origin of binary sex we may find a clue 

in the history of Ulothrix, or even better the Volvocine 

Pandorina, referred to above (p. 9). 1 The gametes of this 

last species are of three sizes, micro-, meso-, and megagametes, 

which we may letter », b, C respectively. These are 

in the first place strictly exogamous, but subject to this condition 

the following unions are said to be possible—a+a and 

b + b (isogamous), as well as a+b, a+C, b+C (anisogamous): but 

the other conceivable pairing,C+C, does not occur; as if, concurrent 

with its enlargement, the form C had become too inert 

to form isogamous unions. We might say that a and b are 

sexually differentiated with respect to C, but not between themselves 

or with one another. We may conceive that the gametogenic 

divisions in a species being inconstant, broods of 

gametes would be formed whose size was inversely proportional 

to the number of the brood ; 2 the extreme forms would 

be small active gametes and large sluggish ones respectively. 

As the latter are ill fitted to conjugate among one another, in 

the struggle for pairing the small numerous active ones would 

be most likely to find pair with these large ones, and the 

rejuvenescence of such unions would be the more efficacious 

because of the difference of temperament between the parent 

gametes. The middle forms being produced in smaller numbers 

than the little gametes, and less useful either way, would tend 

to disappear. The difference of size between the micro- and 

mega-gametes would tend to increase and a division of labour 

take place, the megagamete tending to accumulate nourishment 

to give the zygote a good start, the microgamete gaining activity 

1 The following account is based on the abstract in Butschli, op. cit., p. 788. 

1 In Pandorina, however, each gametogoniutn forms eight gametes, large, 

medium, or small as the case may be. In Ulotlirix the number is inversely 

as the size : the smallest are capable of isogamous union, which is the rule; 

but they are also capable of anisogamous unions with larger, more sluggish 

zoospores.

SOME PEOBLEMS OF REPRODUCTION. 73 

and delicate sensibility j 1 and by this differentiation of temperament 

the zygote would be the gainer. This I take to be the 

ORIGIN 01? SEX. Once started in some such way, the difference 

of temperament between the gametes would tend to be more and 

more accentuated and, so to say, crystallised; and this would be 

as it were anticipated, first in the organs and then in the individuals 

producing the gametes. I accept then one main thesis' of 

the " Evolution of Sex," that male and female are distinguished 

by their respective temperaments; though it is obvious that I 

reject utterly its theory of sexual karyogamy that the male 

brings " katastates," the female " anastates," which combine 

to make the zygote a perfect organism equipped for any event. 

I have stated that I consider the difference of temperament 

to be the advantage brought by bisexuality; and in allogamic 

bisexuality this advantage is doubled: hence the many indications 

on which has been based the old adage that " nature 

abhors perpetual self-fertilisation." But, on the other hand, 

if we admit that allogamy is, like karyogamy itself, a mere 

" acquired need " or " necessary superfluity," we have no difficulty 

in understanding the continuance and hardiness of many 

self-impregnating flowers, and of that sturdy group of selffertilising 

animals, the parasitic Flat worms. 2 

E. PARAGENETIC PROCESSES, USUALLY COMPRISED UNDER THE 

TERM " PARTHENOGENESIS." 

By PARACSENESIS I designate all modes of reproduction in 

which a body, not the zygote, simulates the behaviour of the 

1 The way many Arthropods find their mates by smell is well known; 

spermatozoa of plants find the oosphere owing to their very delicate sensibility 

to chemical stimuli. 

1 The variation in individual susceptibility to harm from close breeding is 

extreme. The human race is usually believed to suffer greatly from close 

breeding; and yet some of its hardiest and finest specimens are the members 

of fishing communities, isolated by position or by custom, and bound togetlier 

by the closest and most complex ties of blood. Similar facts as regards the 

vigour of cleistogamous and other self-pollinating types of plants have led to 

many attacks On the adage cited above, made notably by A. W. Bennett, G. 

Henslow, Neehan, &c.


zygote in the same or allied forms. Logically, of course, all 

these being processes of rejuvenescence should have been 

treated earlier, but the foregoing discussion was necessary to 

the full understanding of the analysis of paragenetic phenomena 

which I now proceed to give. 

1. TRUE PARTHENOGENESIS we define as the development of 

a single unfertilised (facultative) gamete. It occurs in the following 

cases: 

a. ISOGAMETES.—Not infrequently facultative. 

b. MICROGAMETES.—Only known to be facultative in Ectocarpus; 

the reduction of cytoplasm is too heavy a disadvantage 

for the resumption of active cellular life. 

c. MEGAGAMETES are more frequently facultative in the 

lower Algse and in Chara crinita. In other Metaphytes 

parthenogenesis is unknown. The only cases of true parthenogenesis 

of the Metazoan oosphere, differentiated as such 

by the formation of both polar bodies, are the following 

—Liparis dispar and some other Lepidoptera, and Apis 

(Drone eggs). 

2. SIMULATED CELLULAR, PARTHENOGENESIS occurs when a 

vegetative cell that might otherwise have formed a gamete 

assumes directly the behaviour of a zygote (" azygospores" of 

Conjugatse, " auxospores" of certain Diatoms). 

3. SIMULATED APOCYTIAL PARTHENOGENESIS occurs when an 

apocytial gametoidassumes the behaviour of a zygotoid ("azygospores" 

of Mucorini). 

• 4. PROGAMETAL REJUVENESCENCE occurs when a progamete 

assumes the behaviour of a zygote. This is stated to be the 

case in many Arthropods where the ovum, after the expulsion 

of one polar body only, develops without fertilisation. According 

to the recent discoveries of O. Hertwig and Boveri, 

many cases referred to this (if not all) should be placed under 

the following heading. 

5. METAGAMETAL REJUVENESCENCE is the best term I can find 

to fit the case of certain flowering plants (Coelebogyne, 

Citrus, Funkia, Nothoscordum), where the tissue-cells 

adjoining the apex of the embryo-sac grow into it, and

SOME PROBLEMS OF BJEPBODUCTION. 75 

assume the behaviour of zygotes by developing as normal 

embryos. 1 

6. PARAGAMY comprises those cases where the fusion of 

sister-nuclei replaces the advent of a male nucleus. 

a. OOPARAGAMY occurs in the Metazoa in this wise: after 

the first polar body is formed a second polar spindle is formed 

in the egg, as if to form a second polar body; but the nucleus 

corresponding with the second polar body moves back again 

to fuse with the nascent oosphere nucleus. This has been 

observed in Ascaris and Pterotrachea by Boveri, and 

in Asteracanthion by 0. Hertwig. The fusion nucleus 

thus formed has the same number of chromatic elements as the 

normal zygote nucleus, double that of the gametogonium; and it 

is essentially different from the nuclei produced by mere fission 

during the whole cellular cycle since the last rejuvenescence. 

b. APOCYTIAL PARAGAMY occurs when the fusion of the 

nuclei of an apocytium wholly replaces the formation and 

union of gametes. This occurs in Saprolegniese and 

Derbesia. 

IX. GENERAL CONCLUSIONS. 

The following theses state concisely the results of our 

inquiry: 

1. Absolutely agamous forms exist in the group Monadinese; 

in these REST is the only agent of rejuvenescence. 

2. CHANGE OF THE MODE OF LIFE is a frequent mode of 

rejuvenescence in apogamous and self-fertilising organisms. 

3. In the higher Monadinese and the Myxomycetes a 

plasmodium formation occurs, so that the cytoplasm is renewed 

by PLASTOGAMY, and the nuclei wander from their original 

cytoplasts. 

1 The apogamic development of the plant of Pteris cretica from a group 

of cells in the prothallus, instead of from a fertilised oosphere, comes very 

close to this group of processes. I should note that apogamy is a purely 

negative word, implying solely the excision or loss of a sexual process 

from the life-history of an organism ; but this may be effected and compensated 

in most divers ways, which might be classified if it were not 

rather outside the scope of the present essay to do so.

76 MABCUS M. HAETOG. 

4. Isogamy, plural or binary, is a step in advance of plasmodium 

formation, involving, as well as plastogamy, KARYO- 

GAMY, or the reconstitution of a nucleus by the fusion of. old 

ones. 

5. The rejuvenescence of karyogamy is due to the fact 

that the zygote nucleus and cytoplast form a new cell 

association. 

6. A similar rejuvenescence may take place by the mere 

migration of a nucleus into a vacant foreign cytoplast, as in 

the union of a spermatozoon with the non-nucleated fragment 

of the egg of an Echinoderm. 

7. Many cases of so-called "parthenogenesis" involve 

really the fusion of nuclei, the resulting nucleus being essentially 

different from the fission nuclei of the previous cellcycle. 

8. Other modes of rejuvenescence may replace the karyogamy 

of gametes (e. g. a prolonged rest of the gametogonial 

cell of Botrydium gives its brood-cells a power of independent 

development instead of the tendency to unite as 

gametes). 

9. Those organisms that have attained the capability of 

karyogamic rejuvenescence may, by prolonged fissile reproduction 

without karyogamy, pass into a senile condition; marked 

by reproductive incapacity. In these, therefoi'e, karyogamic 

rejuvenescence has become essential to the preservation of the 

race. 

10. Rapidly repeated nuclear fissions, without sufficient 

interval for nutrition and recovery, may lower the vital energy 

or constitution of the cell, and accelerate this reproductive 

incapacity; and this may be the physiological import of the 

fissions that so frequently differentiate the gamete, and determine 

its obligatory character. 

11. The reproductive incapacity of most microgametes finds, 

however, a sufficient explanation in the extreme reduction of 

their cytoplasm. 

12. The reproductive incapacity due to long or rapidly repeated 

acts of fission uninterrupted by karyogamy is a matter


of constitutional temperament or vigour characteristic 

only of the race, for— ; 

(a) It is absent in primitive, agamous types. 

(b) It is slight in groups where parthenogenesis occurs, 

though often absolute in closely-allied forms. 

(c) It has been lost in apogamous groups. 

13. A further evolution of this constitutional weakness takes 

place in forms which are either (a) exogamous or {b) sexually 

differentiated. Here the nuclei that fuse to remove this reproductive 

incapacity by rejuvenescence must be of distinct 

origin. 

14. Exogamy of isogametes cannot be taken as indicating 

latent sex ; it is merely the expression of karyogamic incompatibility 

of close blood-relations; this, under the name of 

Allogamy, has been long since recognised when associated 

with, and superadded to, bisexuality. 

15. The constitutional weakness reaches its highest degree 

in those organisms where allogamy is most marked; the evil 

effects of close-breeding are commensurate with the habitual 

advantages of cross-breeding which has here become an 

"acquired need." 

16. Here again we find, from the occasional existence of 

types, strains, or even couples, whose offspring does not 

degenerate from close breeding, that the need for allogamy is 

not absolute,, but a question of constitutional weakness or 

vigour. 

17. Since, in all cases of plasmodial and karyogamic rejuvenescence, 

we find the migration of the nucleus to foreign 

cytoplasm, or the reconstitution of the cytoplasm or of the 

nucleus, or a combination of these to be the sole necessary 

factors: we infer that the constitutional weakness of the 

later terms of a cycle of fission is largely due to the 

continuance of the association of nucleus and cytoplast 

unchanged. 

18. From considerations of (a) the known functions of the 

nucleus; (i) its chemical composition; (c) the effects of rest, 

change of form, or change of habit (polymorphism and

78 MABCUS M. HARTOG. 

heteroecism) in effecting rejuvenescence, and often replacing 

karyogamy: it is suggested that the evil effects of the prolonged 

association of cell and nucleus are due (a) to the 

nucleus responding less actively to the stimuli from the cytoplasm 

; (b) its consequently inadequate directive power; (c) to 

the resulting bad performance of its work by the cytoplast; 

(d) to the imperfect nutrition of the nucleus; (e) the failure 

of the cell as an organic whole. 

19. The process of nuclear reduction in progametal cells 

and gametes is, though general, neither uniform nor universal. 

Its occurrence in the pollen-mother-cells of Flowering Plants 

leads us to anticipate its occurrence in the mother-cells of 

broods of reproductive cells generally, sexual or asexual. 

Pending the settlement of this point, explanation is premature. 

20. Replacement theories of fertilisation are inadmissible, 

since all fail to account for one or more of the following facts : 

(a) Multiple isogamy. 

(b) The non-discrimination of the broods of exo-isogametes 

into two categories, of which the members of either would pair 

with those of the other category, but not of their own. 

(c) The absence of " excretion phenomena " of any kind in 

so many cases of gametogeny. 

(d) The existence of true parthenogenesis of male as 

well as female gametes. 

(e) The formation of a male individual from the exclusively 

female oosphere of the Hive-bee. 

We have now finished our task; the theory (theses 1—17) 

and the hypothesis (18) set forth are based only on facts lying 

in the fields of biological observation and experiment; aa 

undertaking which should be more profitable than castlebuilding 

in the shadowy dreamland of & priori speculation. 

CORK, March 3,1891.' 

1 

Section VI, A was written after the completion of the rest of the MS., 

and again modified during its passage through the press. Slight alterations 

and additions have been made at the same time in the rest of the study 

(July 30th, 1891).


Postscript.—In writing the foregoing essay, and even in 

seeing it through the press, I omitted to state one cardinal 

point, really underlying the whole theory of gametogeny now 

proposed; but the necessity of expressing it in set terms 

appeared as soon as I had to consider the best mode of presenting 

a concise account of my views to an audience of the 

British Association in Cardiff (August 22nd), 1891. Two 

distinct modes of fission occur in relation to the growth of the 

organism in Protozoa and Protophytes : in the first, after each 

division the daughter-cells grow to the size of the parent 

(more or less) before dividing in turn; in the second, the 

intervals of growth are suppressed, and a series of successive 

fissions takes place, resulting in a brood of small individuals 

(" swarmers," " zoospores," &c.). We call this second type of 

fission " brood-formation," the resulting individuals " broodcells." 

Necessary, like facultative, gametes are essentially, 

in origin at least, modified brood-cells. Hence, when the 

ancestral development is not lost, gametes will always be 

produced by brood-formation, while tissue-cells (except 

in the earlier embryonic state) are formed by the first 

mode of fission. 

September, 1891.

Some Problems of Reproduction: a Comparative Study of ...

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