CSIRO PUBLISHING
Invertebrate Systematics, 2014, 28, 491–500
http://dx.doi.org/10.1071/IS13064
Monophyly and phylogenetic origin of the gall crab family
Cryptochiridae (Decapoda : Brachyura)
Sancia E. T. van der Meij A,C and Christoph D. Schubart B
A
Department of Marine Zoology, Naturalis Biodiversity Center, Darwinweg 2, 2333 CR Leiden, The Netherlands.
Biologie 1, Institut für Zoologie, Universität Regensburg, D-93040 Regensburg, Germany.
C
Corresponding author. Email: sancia.vandermeij@naturalis.nl
B
Abstract. The enigmatic gall crab family Cryptochiridae has been proposed to be phylogenetically derived from within
the Grapsidae (subsection Thoracotremata), based on the analysis of 16S mtDNA of one cryptochirid, Hapalocarcinus
marsupialis, among a wide array of thoracotremes, including 12 species of the family Grapsidae. Here, we test the monophyly
and phylogenetic position of Cryptochiridae using the same gene, but with an extended representation of cryptochirids
spanning nine species in eight of 21 genera, in addition to further thoracotreme representatives. The results show that gall
crabs form a highly supported monophyletic clade within the Thoracotremata, which evolved independently of grapsid crabs.
Therefore, the Cryptochiridae should not be considered as highly modified Grapsidae, but as an independent lineage of
Thoracotremata, deserving its current family rank. Further molecular and morphological studies are needed to elucidate the
precise placement of the cryptochirids within the Eubrachyura.
Additional keywords: 16S mtDNA, coral-associated organisms, evolutionary origin, superfamily.
Received 20 December 2013, accepted 26 June 2014, published online 13 November 2014
Introduction
Gall crabs (Cryptochiridae) are obligate symbionts of living
scleractinian corals, residing in galls, tunnels or pits in the
coral skeleton. The family consists of 21 genera and 49
species (Ng et al. 2008; Davie 2014) and is recorded from
both shallow and deeper waters down to 512 m (Kropp and
Manning 1987; Kropp 1990). The first known gall crab
species was described by Stimpson (1859), who named the
species Hapalocarcinus marsupialis and referred to it as ‘a
remarkable new form of Brachyurous Crustacean’. Stimpson
did not assign H. marsupialis to a crab family, but remarked
that – in the series – it would probably fit between Pinnotheres
and Hymenosoma, which belong to the Pinnotheridae De Haan,
1833 and the Hymenosomatidae MacLeay, 1838, respectively.
Heller (1861) described a second gall crab species, Cryptochirus
coralliodytes, and commented on its similarities with Ranina
and Notopus (Raninidae De Haan, 1839). A. Milne-Edwards
(1862) described yet another species, Lithoscaptus paradoxus,
mentioning that this new species did not fit in any of the
known crab families. Paul0 son (1875) subsequently erected
the subfamily Cryptochirinae within the Pinnotheridae to
accommodate the gall crabs, which Richters (1880) elevated
to family level. A more complete overview of the history of
the family Cryptochiridae Paul0 son, 1875, can be found in Kropp
and Manning (1985).
Close phylogenetic affinities between the Cryptochiridae and
Grapsidae s.str. (cf. Schubart et al. 2002) were proposed by
Journal compilation CSIRO 2014
Wetzer et al. (2009). The authors recommended dropping the
superfamily Cryptochiroidea (see Ng et al. 2008) and suggested
considering Cryptochiridae as just one of many separate
‘grapsoid’ families. The zoeal features of Cryptochiridae
present numerous traits that are unique within the Brachyura
(Tudge et al. 2014 and references therein). Based on the larval
development, a close relationship between grapsids and
cryptochirids had been proposed by Fize (1956), who regarded
cryptochirids as a transitional group between Grapsidae s.l.
and Calappidae. Fize and Serène (1957) deviated from this
placement and argued that Cryptochiridae has closest affinities
with Pinnotheridae, based on the morphology of the female
abdomen. When considering the larval morphology (based on
Troglocarcinus corallicola Verrill 1908), cryptochirids also
appear closely related to Pinnotheridae, with close affinities
to Hymenosomatidae and Leucosiidae (Scotto and Gore 1981).
Utinomi (1944) had previously considered the zoea of
Hapalocarcinus and Cryptochirus to belong to the so-called
Grapsizoea (including genera of the Cancridae, Grapsidae,
Xanthidae and some Oxyrhyncha) and dismissed suggestions
of a close affinity of Cryptochiridae with Pinnotheridae. Affinities
with several other crab families (Hymenosomatidae, Leucosiidae,
Pinnotheridae, Palicidae and Retroplumidae) were discussed by
Kropp (1988), who suggested monophyly of the Cryptochiridae
based on a series of unique morphological characters (gastric mill,
lateral lobe of the antennule, lack of mandibular palp). Guinot
et al. (2013), based on several morphological structures, also
www.publish.csiro.au/journals/is
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Invertebrate Systematics
concluded that the cryptochirids form a monophyletic group.
The spermatozoa of C. coralliodytes and H. marsupialis were
studied by Jamieson and Tudge (2000) and share a striking
synapomorphy that is unique for the family Cryptochiridae
(Tudge et al. 2014). Tudge et al. (2014) also compared the
sperm ultrastructure and operculum of Cryptochiridae to those
of species belonging to the Majoidea and the Hymenosomatidae.
The sperm ultrastructure proves to be somewhat equivocal with
regard to placement of the cryptochirids in Thoracotremata or
Heterotremata. The morphology of the female reproductive
system was studied by Vehof et al. (in press) who showed that
the Cryptochiridae share characteristics with the thoracotreme
families Varunidae, Ocypodidae and Pinnotheridae. The
cryptochirid reproductive system is nevertheless remarkable in
having ovaries that are expanded into the abdomen ( = pleon),
which is exceptional among Brachyura and has only been known
from pinnotherids so far (Becker et al. 2011).
In the most recent treatments of the Brachyura (Ng et al. 2008;
De Grave et al. 2009; Ahyong et al. 2011; Tsang et al. 2014), the
Cryptochiridae is classified in the superfamily Cryptochiroidea,
and placed in the subsection Thoracotremata. The main argument
to place Cryptochiridae in the Thoracotremata is the sternal
location of male gonopores (Guinot 1977). This is in
agreement with Scotto and Gore (1981), who regarded adults
of the Atlantic species Troglocarcinus corallicola as exhibiting
an advanced thoracotreme state. The Cryptochiridae have
alternatively also been considered Heterotremata (e.g. Guinot
and Richer de Forges 1997; Guinot and Bouchard 1998),
advanced Heterotremata (Martin and Davis 2001) or a ‘basal
heterotreme eubrachyuran superfamily’ (Guinot et al. 2013).
Indeed, in the first paper employing molecular data to clarify
the position of the gall crabs within other brachyurans, its
placement in the subsection Thoracotremata was confirmed
(Wetzer et al. 2009).
The monophyly and phylogeny of the Cryptochiridae
among the Thoracotremata were re-evaluated by using 16S
mtDNA data for 10 gall crab species belonging to nine genera.
We reused almost the entire dataset from Wetzer et al.
(2009), but expanded it by adding 10 gall crab sequences, and
24 additional sequences from thoracotreme crab species
and families not included in the previous study. We used this
enlarged dataset for analysis of the position of the Cryptochiridae
within the Thoracotremata and to test Wetzer et al.’s result that
Hapalocarcinus marsupialis evolved from within the family
Grapsidae.
Materials and methods
Wetzer et al. (2009) used two 16S mtDNA sequences of
Hapalocarcinus marsupialis, combined with 49 GenBank
sequences of thoracotreme species and four heterotreme
species as outgroup to evaluate the relationships between
Cryptochiridae and other Brachyura. To re-evaluate the
position of the Cryptochiridae, we added nine additional
species belonging to eight cryptochirid genera (see Fig. 1).
We based our identifications on Fize and Serène (1957),
Kropp (1989, 1990) and van der Meij (2012). We included
one additional sequence of H. marsupialis for comparison
with the material of Wetzer et al. (2009).
S. E. T. van der Meij and C. D. Schubart
An enlarged dataset encompassing a minimum of two
species of all known thoracotreme families was used as a more
complete dataset for research on the phylogenetic position of the
gall crabs. Type genera and species were included whenever
the corresponding data were available in GenBank. The full list
of GenBank sequences and species authorities can be found in
Table 1.
The following changes and additions were made in
comparison to the dataset of Wetzer et al. (2009):
(1) The Old World freshwater crabs used by Wetzer et al. (2009),
Sartoriana spinigera (Gecarcinucidae) and Geothelphusa
pingtung (Potamidae), were moved to the ingroup together
with additional freshwater crabs from other continents, while
Crossotonotus spinipes (Crossotonotidae) and Palicus
caronii (Palicidae) were kept as outgroups. This was done
in consequence to the newest brachyuran phylogeny
by Tsang et al. (2014), which shows that Old World
freshwater crabs of the superfamily Potamoidea (see Klaus
et al. 2009) are placed at the base of the Heterotremata
which in turn are the sister group to all Thoracotremata.
This implies that the Potamoidea are phylogenetically closer
to Thoracotremata than most other Heterotremata are
to Thoracotremata. Furthermore we wanted to root the tree
in a comparable way to previous phylogenies of the
Thoracotremata (Schubart et al. 2000, 2002, 2006).
(2) Sesarma windsor (Sesarmidae) was deleted from the dataset
as it is a close sister species of S. meridies (see Schubart and
Koller 2005) and does not contribute to the phylogenetic
diversity, whereas Sesarmoides longipes (Sesarmidae) was
removed, as it is a very basal sesarmid that often clusters
weakly (see Schubart et al. 2002) and will be dealt with
separately. Instead, the type species of the family, Sesarma
reticulatum, was added, as well as the Asian sesarmid
representative Chiromantes haematocheir.
(3) Hemigrapsus oregonensis (Varunidae) was removed from
the dataset, as it is not a typical representative of the genus,
and will probably be placed in a separate genus after revision.
In addition to these changes, we noticed that GenBank no.
AB002125 (Wetzer et al. 2009: table 2) does not correspond
to Scopimera globosa (De Haan, 1835), but to S. bitympana
(Dotillidae). We used the latter in our analyses. Taxon selection
for the enlarged dataset was also tested with species belonging
to heterotreme families, but in all preliminary analyses the
cryptochirids consistently nested in the Thoracotremata,
similar to the results of Wetzer et al. (2009). Furthermore,
several potential outgroups were tested.
Collecting
The gall crabs, with the exception of Cryptochirus coralliodytes,
were collected in Indonesia (Raja Ampat, Papua; Ternate,
Halmahera) and Malaysia (Semporna, E Sabah) by the first
author from 2007 to 2010. Corals were searched for galls and
pits, and subsequently split with hammer and chisel. The gall
crabs were preserved in 80% ethanol, after being photographed
with a digital SLR camera equipped with a 50 mm macrolens. The material is deposited in the collections of Naturalis
in Leiden, The Netherlands (formerly Rijksmuseum van
The phylogenetic origin of the Cryptochiridae
Invertebrate Systematics
Fig. 1. The cryptochirid taxa used in this study: (1) Hapalocarcinus marsupialis; (2) Utinomiella dimorpha; (3) Opecarcinus lobifrons;
(4) Fungicola utinomi; (5) Dacryomaia sp.; (6) Fungicola fagei; (7) Fizesereneia sp.; (8) Lithoscaptus tri; (9) Pseudocryptochirus viridis.
No picture is available for Cryptochirus coralliodytes. Not to scale.
493
494
Invertebrate Systematics
S. E. T. van der Meij and C. D. Schubart
Table 1. GenBank sequences used in molecular analyses (taxonomic authorities based on Ng et al. 2008)
* = sequences used in this study, but not included in Wetzer et al. (2009)
Family
Species
GenBank No.
Camptandriidae
Baruna trigranulum (Dai & Song, 1986)
Paracleistostoma depressum De Man, 1895
Crossotonotus spinipes (De Man, 1888)
*Cryptochirus coralliodytes Heller, 1861
*Dacryomaia sp.
*Fizesereneia sp.
*Fungicola fagei (Fize & Serène, 1956)
*Fungicola utinomi (Fize & Serène, 1956)
Hapalocarcinus marsupialis Stimpson, 1859
Hapalocarcinus marsupialis Stimpson, 1859
*Hapalocarcinus marsupialis Stimpson, 1859
*Lithoscaptus tri (Fize & Serène, 1956)
*Opecarcinus lobifrons Kropp, 1989
*Pseudocryptochirus viridis Hiro, 1938
*Utinomiella dimorpha (Henderson, 1906)
Dotilla wichmanni De Man, 1892
Ilyoplax deschampsi (Rathbun, 1913)
*Scopimera bitympana Shen, 1930
Tmethypocoelis ceratophora (Koelbel, 1897)
Cardisoma carnifex (Herbst, 1796)
*Discoplax hirtipes (Dana, 1852)
Gecarcinus lateralis (Fréminville, 1835)
Gecarcoidae lalandii H. Milne Edwards, 1837
*Holthuisana biroi (Nobili, 1905)
*Lepidothelphusa cognetti (Nobili, 1903)
Sartoriana spinigera (Wood-Mason, 1871)
Glyptograpsus impressus Smith, 1870
Platychirograpsus spectabilis De Man, 1896
Geograpsus lividus (H. Milne Edwards, 1837)
Goniopsis cruentata (Latreille, 1803)
Grapsus grapsus (Linnaeus, 1758)
Leptograpsus variegatus (Fabricius, 1793)
Metopograpsus latifrons (White, 1847)
Metopograpsus quadridentatus Stimpson, 1858
Metopograpsus thukuhar (Owen, 1839)
Pachygrapsus crassipes Randall, 1840
*Pachygrapsus fakaravensis Rathbun, 1907
*Pachygrapsus gracilis (Saussure, 1858)
Pachygrapsus marmoratus (Fabricius, 1787)
Pachygrapsus minutus A. Milne-Edwards, 1873
*Pachygrapsus plicatus (H. Milne Edwards, 1837)
Pachygrapsus transversus (Gibbes, 1850)
Planes minutus (Linnaeus, 1758)
*Heloecius cordiformis (H. Milne Edwards, 1837)
*Macrophthalmus crinitus Rathbun, 1913
*Hemiplax hirtipes (Jacquinot, in Hombron & Jacquinot, 1846)
Mictyris brevidactylus Stimpson, 1858
*Mictyris guinotae Davie, Shih & Chan, 2010
*Ocypode quadrata (Fabricius, 1787)
*Uca borealis Crane, 1975
*Uca tetragonon (Herbst, 1790)
*Ucides cordatus (Linneaus, 1763)
Palicus caronii (Roux, 1828)
Percnon gibbesi (H. Milne Edwards, 1853)
*Percnon guinotae Crosnier, 1965
Austinixa aidae (Righi, 1967)
Austinixa patagoniensis (Rathbun, 1918)
Pinnotheres pisum (Linnaeus, 1767)
AB002129
AB002128
AJ130807
KM114587
KM114582
KM114581
KJ923707
KM114583
EU743929
EU743930
KM114586
KM114584
KJ923730
KJ923710
KM114585
AB002126
AB002117
AB002125
AB002127
AM180687
FM863830
AJ130804
AM180684
FM180132
FM180134
AM234649
AJ250646
AJ250645
AJ250651
AJ250652
AJ250650
AJ250654
AJ784028
DQ062732
AJ784027
AB197814
FR871306
FR871303
DQ079728
AB057808
FR871310
AJ250641
AJ250653
AM180695
AB537376
AB440189
AB002133
AB513632
FN539018
AB535403
AB535405
FN539019
AM180692
AJ130803
FN539015
AF503185
AF503186
AM180694
Crossotonotidae
Cryptochiridae
Dotillidae
Gecarcinidae
Gecarcinucidae
Glyptograpsidae
Grapsidae
Heloeciidae
Macrophthalmidae
Mictyridae
Ocypodidae
Palicidae
Percnidae
Pinnotheridae
(continued next page )
The phylogenetic origin of the Cryptochiridae
Invertebrate Systematics
495
Table 1. (continued )
Family
Species
GenBank No.
Plagusiidae
Euchirograpsus americanus A. Milne-Edwards, 1880
*Plagusia depressa (Fabricius, 1775)
Plagusia squamosa (Herbst, 1790)
Geothelphusa pingtung Tan & Liu, 1998
*Potamon potamios (Olivier, 1804)
*Potamonautes perlatus (H. Milne Edwards, 1837)
Epilobocera sinuatifrons (A. Milne-Edwards, 1866)
Armases elegans (Herklots, 1851)
*Chiromantes haematocheir (De Haan, 1833)
Sarmatium striaticarpus Davie, 1992
Sesarma meridies Schubart & Koller, 2005
*Sesarma reticulatum (Say, 1817)
Austrohelice crassa (Dana, 1851)
Brachynotus atlanticus Forest, 1957
Cyrtograpsus affinis Dana, 1851
Eriocheir sinensis H. Milne Edwards, 1853
Helograpsus haswellianus (Whitelegge, 1899)
Hemigrapsus sanguineus (De Haan, 1835)
Paragrapsus laevis (Dana, 1851)
Pseudogaetice americanus (Rathbun, 1923)
Varuna litterata (Fabricius, 1798)
*Xenograpsus ngatama McLay, 2007
*Xenograpsus testudinatus Ng, Huang & Ho, 2000
*Xenophthalmus pinnotheroides White, 1846
AJ250648
AJ250649
AJ311796
AB266168
AB428515
AM234647
FM208778
AJ784011
AJ308414
AM180680
AJ621819
AJ225867
AJ308416
AJ278831
AJ130801
AJ250642
AJ308417
AJ493053
AJ308418
AJ250643
AJ308419
FM863828
FM863827
EU934951
Potamidae
Potamonautidae
Pseudothelpusidae
Sesarmidae
Varunidae
Xenograpsidae
Xenophthalmidae
Natuurlijke Historie, collection coded as RMNH.Crus.D). The
specimen of C. coralliodytes (made available by Dr Danièle
Guinot) was collected in New Caledonia, more material of the
same series is in the collections of the Muséum national d’Histoire
naturelle (Paris).
the likelihood scores was 0.01042. The burnin was set to discard
the first 25% of the sampled trees. The consensus tree, constructed
using the ‘sumt’ option in MrBayes, was visualised using FigTree
1.3.1. (Rambaut 2009).
Results
Analyses
DNA was isolated from muscle tissue of the fifth pereiopod, using
the Qiagen DNeasy® Kit according to the manufacturer’s
protocol for animal tissue. Maceration took place overnight for
~18 h. The final elution step was performed with 100 mL elution
buffer. PCR was carried out with standard conditions (2.5 mL
PCR buffer, 0.5 mL DNTPs, 1.0 mL of primers 16L2 and 16H10
(Schubart 2009), 0.3 mL Taq, 18.7 mL MilliQ and 1.0 mL DNA
template). Thermal cycling was performed as follows: initial
denaturation at 95C for five minutes, followed by 39 cycles
of 95C for five seconds, 47C for one minute, and 72C for
one minute and finalised by 10 min at 72C. Sequences were
assembled and edited in Sequencer 4.10.1.
The alignment was constructed with Clustal X (Larkin et al.
2007) and minimally modified by hand. It includes 82 sequences
consisting of 589 basepairs, of which 374 are variable and 319
are parsimony informative. A model selection analysis was
carried out to select the best-fit model based on the Akaike
Information Criterion (AIC) in jModelTest 2.1.1 (Darriba et al.
2012), which rendered TrN+I+G as the best model. A Bayesian
phylogeny was estimated with MrBayes 3.1.2 (Ronquist and
Huelsenbeck 2003) using the next most complex GTR+I+G
model. Four Markov-Monte-Carlo chains were run for
3 000 000 generations with a sample tree saved every 1000
generations (outgroup Palicus caronii). The split frequency of
The topology of Fig. 2 is derived from the Bayesian inference
50% majority rule consensus of the trees remaining after the
burnin, with high support values in the basal part as well as in
the distal phylogenetic branches. The outgroup is separated by a
long branch, whereas the freshwater crabs from four families
form a sister clade to the highly supported monophyletic
Thoracotremata. Within the Thoracotremata, four major clades
can be distinguished. The cryptochirid taxa included in the
analyses form a monophyletic clade with a long branch length
compared to the other clades. Within this highly supported
clade, Utinomiella dimorpha, Pseudocryptochirus viridis and
Opecarcinus lobifrons hold a basal position with respect to the
remaining gall crabs. Our specimen of H. marsupialis differs from
the specimens used in Wetzer et al. (2009) by 15–17 basepairs
(bp) out of 533 bp. Nevertheless, Hapalocarcinus marsupialis is
for now regarded a single species, but may well be a complex of
species (see also Castro 2011).
A second clade contains Glyptograpsidae, Heloeciidae,
Pinnotheridae, Ocypodidae and Sesarmidae. Ocypodidae and
Pinnotheridae together form a paraphyletic clade. The single
representative of the Heloeciidae appears as a sister group of
the Glyptograpsidae. All Sesarmidae taxa form a monophyletic
clade. A third clade is formed by the Macrophthalmidae and
Varunidae. The Macrophthalmidae are polyphyletic, while the
Varunidae are paraphyletic because of non-reciprocal monophyly
496
Invertebrate Systematics
S. E. T. van der Meij and C. D. Schubart
outgroup
Palicus caronii
Crossotonotus spinipes
Armases elegans
95
100
100
90
91
Sesarma meridies
100
Sesarma reticulatum
Sarmatium striaticarpus
Chiromantes haematocheir_
Glyptograpsus impressus
100
Platychirograpsus spectabilis
Heloecius cordiformis
Sesarmidae
100
69
100
Austinixa hardyi
Austinixa patagoniensis
Glyptograpsidae
Heloeciidae
Pinnotheridae
Pinnotheres pisum
Ocypode quadrata
Ucides cordatus
100
Ocypodidae
Uca borealis
Uca tetragonon
100
Plagusia depressa
Plagusia squamosa
Euchirograpsus americanus
Cardisoma carnifex
Discoplax hirtipes
Gecarcinus lateralis
Gecarcoidea lalandii
Xenograpsus ngatama
100
Xenograpsus testudinatus
100 Hemiplax hirtipes
Austrohelice crassa
Helograpsus haswellianus
99
99
Cyrtograpsus affinis
Hemigrapsus sanguineus
80
Brachynotus atlanticus
73
78
52
Pseudogaetice americanus
57
Eriocheir sinensis
Paragrapsus laevis
Varuna litterata
Macrophthalmus crinitus
Fungicola fagei
73
Dacryomaia sp.
100
100
100
100
82
100 Hapalocarcinus marsupialis
Hapalocarcinus marsupialis
Hapalocarcinus marsupialis
Fizesereneia sp.
93
Cryptochirus coralliodytes
92
Fungicola utinomi
Lithoscaptus tri
Opecarcinus lobifrons
Pseudocryptochirus viridis
Utinomiella dimorpha
Gecarcinidae
Xenograpsidae
Macrophthalmidae
Varunidae
Macrophthalmidae
100
82
100
100
86
Percnon gibbesi
Percnon guinotae
100 Mictyris brevidactylus
90
100
54
Cryptochiridae
Percnidae
Mictyridae
Dotillidae
Xenophthalmidae
Camptandriidae
Grapsidae
Gecarcinucidae
Potamonautidae
Potamidae
Pseudothelphusidae
Heterotremata
98
Mictyris guinotae
Dotilla wichmanni
83
Ilyoplax deschampsi
99
Scopimera bitympana
100
Tmethypocoelis ceratophora
93
Xenophthalmus pinnotheroides
Baruna trigranulum
Paracleistostoma depressum
Geograpsus lividus
92
Pachygrapsus gracilis
Pachygrapsus crassipes
94
100
Pachygrapsus minutus
Pachygrapsus transversus
Goniopsis cruentata
Pachygrapsus fakaravensis
94
65
Grapsus grapsus
Pachygrapsus marmoratus
Leptograpsus variegatus
Planes minutus
Pachygrapsus plicatus
Metopograpsus latifrons
100
Metopograpsus thukuhar
51
Metopograpsus quadridentatus
Holthuisana biroi
100
Sartoriana spinigera
Lepidothelphusa cognetti
Potamonautes perlatus
Potamon potamios
100
Geothelphusa pingtung
Epilobocera sinuatifrons
Thoracotremata
98
Plagusiidae
0.2
Fig. 2. Phylogenetic placement of the Cryptochiridae within the Thoracotremata, based on 16S mtDNA sequences of 82 taxa (including outgroups). This tree
is rooted with Palicus caronii. Topology derived from Bayesian inference 50% majority rule, significance values are posterior probabilities.
(overlapping taxa) between these two families. Lastly, Grapsidae
form the fourth monophyletic clade. The genus Pachygrapsus is
paraphyletic, and the genus Metopograpsus clusters basally
compared to the other grapsids. In addition to these major
clades, several monophyletic families can be discerned based
on our taxon sampling: the Mictyridae, Percnidae, Plagusiidae
and Xenograpsidae. The Xenophthalmidae (represented by only
one species) are included in the Dotillidae, which is a sister
group of the Camptandriidae. The Gecarcinidae do not cluster
together.
Discussion
The present molecular phylogeny, including 16S mtDNA of
ten cryptochirid species belonging to nine genera, showed that
The phylogenetic origin of the Cryptochiridae
Cryptochiridae form a highly supported monophyletic
clade within the Thoracotremata with an unquestionable
posterior probability of 100%. Within the Cryptochiridae,
representatives of Utinomiella, Pseudocryptochirus and
Opecarcinus cluster basally to the other included genera.
These remaining genera form one clade, with three possible
subclades. Hapalocarcinus clusters weakly with Fungicola
fagei and Dacryomaia sp., but with a long branch. Our results
are largely in agreement with Van der Meij and Reijnen
(2014), who, based on 16S and COI mtDNA, retrieved
Utinomiella as the basal genus to all other cryptochirids. They
also found Pseudocryptochirus forming a well supported clade
with Neotroglocarcinus, and Opecarcinus forming a highly
supported clade with Pseudohapalocarcinus. In their study,
the remaining six genera (seven species) formed a fourth
clade, with Hapalocarcinus weakly clustering as a sister clade.
The position of Hapalocarcinus within the Cryptochiridae
therefore remains unclear to some degree.
According to our phylogeny, gall crabs should not be
considered ‘highly modified Grapsidae’ (see Wetzer et al.
2009), but an independent lineage deserving its current family
rank. The conclusion that gall crabs are highly modified grapsids
was based on low bootstrap (53%) and posterior probability
(58%) values supporting the inclusion of H. marsupialis in the
Grapsidae. Here we show that the conclusions of Wetzer et al.
(2009) would have been different if there was better cryptochirid
sampling. This may also be the case in the recent study by Tsang
et al. (2014), where again only one cryptochirid taxon was used
for a multi-gene phylogenetic analysis. In this case, Dacryomaia
sp. is found in an unsupported sister taxon relationship with
the family Xenograpsidae. It shows that conclusions on the
phylogenetic position of (non-monotypic) families or other
higher taxa, may be premature if based on a single species,
especially when representatives are chosen that are not the
type species of a genus, and when no information is available
on the monophyly of the respective taxa.
Our results, and the ones by Tsang et al. (2014), do confirm
the conclusion by Wetzer et al. (2009) that the Cryptochiridae
belong to the Thoracotremata. In our analysis cryptochirids
are consistently nested with thoracotreme crabs, when
different heterotreme species were added to the dataset or
used as outgroups. Yet, no clear affinities with a particular
thoracotreme family could be identified. Thoracotreme crabs
inhabit a wide diversity of habitats. Paulay and Starmer (2011)
postulated that Thoracotremata evolved in ‘safe places’, such as
intertidal, non-marine, deep water and endo-symbiotic habitats.
Several thoracotreme families consist mainly of intertidal or shore
crabs (e.g. Grapsidae, Sesarmidae, some Varunidae) occurring
in different habitats, with some of them being specialised
mangrove and mudflat dwellers (Camptandriidae, most
Sesarmidae and Ocypodidae, with the exception of Ocypode,
which specialises on sandy shores) or freshwater-dependent crabs
(Glyptograpsidae and some Varunidae) (Schubart et al. 2002).
Xenograpsidae with the genus Xenograpsus are specialised
on hydrothermal vents (Ng et al. 2007) and many Sesarmidae
and Gecarcinidae have invaded repeatedly terrestrial and/or
freshwater habitats (Schubart et al. 2000). Only the
Pinnotheridae have a similar lifestyle to the Cryptochiridae, by
living in a permanent symbiosis with bivalves and ascidians
Invertebrate Systematics
497
(Becker et al. 2011). Survival and diversification of
thoracotreme crabs might therefore be related to their
adaptability to new environments (Paulay and Starmer 2011).
The branch support at the family/genus level is high for
most clades. One of the largest clades is formed by the
Glyptograpsidae, Heloeciidae, Ocypodidae, Pinnotheridae and
Sesarmidae. A possible phylogenetic relationship between the
Glyptograpsidae and Sesarmidae (see Schubart et al. 2000;
Wetzer et al. 2009) or Glyptograpsidae and Ocypodidae (see
Schubart and Cuesta 2010) had previously been proposed based
on the same gene (in addition to histone H3 in Schubart and
Cuesta 2010). However, a close affinity between these families
was not confirmed by the study of Palacios-Theil et al. (2009).
There is ongoing debate about the phylogenetic affinities of the
genus Ucides (e.g. Ng et al. 2008; Schubart and Cuesta 2010).
In our analyses, the relationship of U. cordatus with regards to
the ocypodid genera Ocypode and Uca and the Pinnotheridae
is not resolved. A study on the morphology of the female
reproductive system shows that the overall anatomy of
U. cordatus is similar to other ocypodids (Castilho-Westphal
et al. 2013). For now, we therefore continue to recognise Ucides
as a genus within the Ocypodidae (see also Schubart and Cuesta
2010) and not in its own family as suggested by Ng et al. (2008).
The Grapsidae form a monophyletic family. The separate
clustering of the genus Metopograpsus within the Grapsidae
has been shown before (e.g. Kitaura et al. 2002; Wetzer et al.
2009). In Schubart et al. (2006) and Schubart (2011),
Metopograpsus holds a basal position within the Grapsidae
in analyses carried out with the same molecular marker. The
genus Pachygrapsus appears to be polyphyletic in this study,
confirming results from Schubart (2011).
Kitaura et al. (2002) and Schubart et al. (2006) proposed
that the Macrophthalmidae and Varunidae are sister groups,
but with low confidence values. Our phylogeny shows a closer
relationship between selected Macrophthalmidae and Varunidae,
with high support levels. The species Hemiplax hirtipes clusters
with the Varunidae (see also Kitaura et al. 2010; McLay et al.
2010). If H. hirtipes would be included in the Varunidae, then this
family could again be considered monophyletic (see previous
work by Schubart et al. 2002), based on the included taxa. The
Mictyridae appears related to the Percnidae (but with very long
branches), which is a new and unexpected hypothesis considering
the large phylogenetic distance between these two families in the
trees of Schubart et al. (2006) and Wetzer et al. (2009). In their
study on the Plagusiidae and Percnidae, Schubart and Cuesta
(2010) did not include species belonging to the Mictyridae; there
the genus Percnon holds a basal position to other thoracotreme
families. In our tree, the Thoracotremata form a polytomy and
thus no basal lineage can be postulated.
In Wetzer et al. (2009), the Camptandriidae are polyphyletic:
Paracleistostoma depressum clusters as a sister group to the
Mictyridae and the Pinnotheridae, whereas Baruna triganulum
clusters with the Dotillidae. In our results both species form
a clade with the Dotillidae. The species Xenophthalmus
pinnotheroides stands together with the Dotillidae. Based on
molecular data and larval morphology, Palacios-Theil et al.
(2009) also suggest a close relationship of Xenophthalmus
pinnotheroides with the family Dotillidae. Ng et al. (2008)
already discussed the strange position of the Xenophthalmidae
498
Invertebrate Systematics
and found that it resembles the Dotillidae, but some characters
argue against lumping them into the family. Hence they followed
Serène and Umali (1972), and treated it as a good family. As the
Xenophthalmidae and the Heloeciidae are represented by single
species in this study, no overall conclusions about their position in
the Thoracotremata should be drawn.
Overall, several phylogenetic relationships (Heloeciidae–
Glyptograpsidae, Varunidae–Macrophthalmidae, Pinnotheridae–
Ocypodidae) argue against the classical and current (Ng et al.
2008) superfamily concept within the Thoracotremata. Therefore,
Schubart et al. (2006) suggested to refrain from this superfamily
concept and treat the constituent families separately until a clearer
picture of phylogenetic relationships within the Thoracotremata
has been reached. The unsuitability of the current superfamilies has
been re-confirmed by Schubart and Cuesta (2010) and Tsang et al.
(2014). Here again we argue against it and would hence propose
to refrain from using the superfamily Cryptochiroidea (see Ng
et al. 2008), until the evolutionary origin of Cryptochiridae (and
taxonomic classification reflecting it) is better understood.
In summary, the Cryptochiridae is a highly enigmatic family,
for which the closest relatives so far remain unknown. The present
study is based on a single gene fragment, and additional support
needs to be obtained from independent molecular markers.
Further studies on the evolution of Cryptochiridae within the
Thoracotremata should for that reason be based on multiple
markers, to obtain more insight in their unusual biology and
life history.
Acknowledgements
We are indebted to Dr Danièle Guinot (MNHN) for making available a
museum specimen of Cryptochirus coralliodytes, Bastian Reijnen (Naturalis)
for assistance with the laboratory work, Theodor Poettinger (Universität
Regensburg) for help with software, and Dr Roy Kropp for discussions in
an earlier stage of this manuscript. The fieldwork in Indonesia was jointly
organised by Dr Bert W. Hoeksema (Naturalis) and Mrs. Yosephine Tuti
(RCO-LIPI), while the research permits were granted by LIPI (Raja Ampat)
and RISTEK (Ternate). Funding for the fieldwork in Indonesia was provided
by the A.M. Buitendijkfonds, and L.B. Holthuisfonds (both Naturalis), Leiden
University Funds, Schure-Beijerinck-Popping Fund, and the Stichting
Fonds Doctor Catharine van Tussenbroek (Nell Ongerboerfonds). The
2010 Semporna Marine Ecological Expedition (SMEE2010) was jointly
organised by WWF-Malaysia, Universiti Malaysia Sabah’s Borneo Marine
Research Institute, Universiti Malaya’s Institute of Biological Sciences and
Naturalis Biodiversity Center, and funded through WWF-Malaysia. Research
permits were granted by the Prime Minister’s Department, Economic
Planning Unit Sabah, Sabah Parks and Department of Fisheries Sabah. We
thank two anonymous reviewers for their comments and suggestions on an
earlier version of the manuscript.
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