Bauplans vs. morphological misfits in biology

Groups of related organisms (animals, plants, fungi) usually have a set of architectural rules in common which are called the bauplan (body plan, constructional plan). Bauplan in living organisms captures the idea of the architectural constraints existing in such a functional design. Bauplans are generalizations of our thinking and classifying brain. There is no doubt that certain animals and plants evolved structures (organs, appendages) that cannot be sensibly accommodated in traditional descriptions. Some plant groups were outlined as morphological misfits by Adrian Bell (1991), who highlighted the fact that morphological misfits are ‘misfits to a botanical discipline not misfits for a successful existence’. Morphological misfits are also observable in animals (Minelli, 2015b). Various morphological misfits emerged as morphological key innovations (perhaps ‘hopeful monsters’) that gave rise to new evolutionary lines of organisms (Theissen, 2006, 2009; Masel and Siegal, 2009). Morphological misfits provide opportunities for investigating character evolvability. The concept of ‘morphological misfits’ is an eye-catcher that allows labelling of all kinds of morphological deviations in the wild, mainly based on major genetic changes such as homeosis (ectopic gene expression in a seemingly wrong position), and other kinds of developmental repatterning (Arthur, 2011; Minelli, 2015b, 2016).

In most seed plants, there is only one major type of construction, the classical root–shoot (CRS) bauplan, with roots and shoots (i.e. stems with leaves) as bauplan units, as well as ‘flowers’ (i.e. unbranched short shoots) serving for sexual reproduction. Strong deviations from the CRS bauplan are usually taken as morphological misfits. Well-known morphological misfits in flowering plants are the Lentibulariaceae (bladderworts and allies) and the Podostemaceae (river-weeds). Both families have members with released (decanalized) body plans, strongly deviating from the CRS bauplan of typical seed plants. The change from terrestrial life to the aquatic habitat may have caused the loss of the CRS bauplan. This seems to be the case in Podostemaceae; less so in Lentibulariaceae (as will be discussed below). Bell (1991) described the free-aquatic duckweeds (Lemna and allies, Araceae) with thalloid stem–leaves and the one-leaf plants (Monophyllaea, Streptocarpus, Gesneriaceae) as additional examples of morphological misfits in flowering plants (Landolt, 1998; Möller and Cronk, 2001; Ayano et al., 2005; Harrison et al., 2005; Cusimano et al., 2011; Tsukaya, 2014).

Aim of this paper

There is no consensus of opinion on how to label and to describe the various structural units comprising the vegetative bodies in both Lentibulariaceae and Podostemaceae. Examples for these terminological difficulties will be given below under the headings ‘The river-weed puzzle’ (Figs 1–8) and ‘The bladderwort puzzle’ (Figs 9–14). It will be shown that Lentibulariaceae and Podostemaceae (in spite of being labelled as morphological misfits) have unique sets of architectural rules (branching patterns) that may be called ‘bauplans’ again. In the final discussion, the findings on bladderworts and river-weeds are incorporated into a more general concept on developmental robustness. The question remains as to whether or not the developmental switches to rather unusual new bauplans had facilitated rather than prevented the evolution of species diversity across bladderworts and river-weeds. The present essay places emphasis on the heuristic value of Sattler’s continuum approach and fuzzy ‘Arberian’ morphology for developmental genetics and character evolution transgressing plant organs, e.g. root–shoot indistinction (Arber, 1920, 1950; Sattler, 1986, 1996; Rutishauser, 1995, Rutishauser and Isler, 2001; Kirchoff et al., 2008; Rutishauser et al., 2008). All scanning electron micrographs (SEMs) and microtome sections (Figs 1–14) were produced in the author’s lab at Zurich University with material collected in the field (see figure legends for details on specimens). The material and methods used have been described elsewhere in detail (e.g. Rutishauser, 1997; Rutishauser and Isler, 2001; Ameka et al., 2003; Moline et al., 2007).

Open in a separate window

Fig. 1.

Podostemoid river-weeds (Podostemaceae – Podostemoideae), as observable in nature. (A) Apinagia latifolia (K.I.Goebel) P.Royen [Source: Bittrich & Amaral; Brazil, Serra do Tepequem] with showy flowers pollinated by insects. (B) Polypleurum dichotomum (Tul.) Cusset [Source: Rutish. & Huber; India, Kerala]: inconspicuous wind-pollinated flowers, arising from endogenous buds of free-floating root. (C) Hydrobryum japonicum Imamura s.l. [Source: Rutish.; Japan, Kyushu]: crustose green root, firmly attached to rock, resembling foliose lichen. (D and E) Griffithella hookeriana (Tul.) Cusset [Source: Rutish. & Huber; India, Kerala]: broad and narrow ribbon-like roots, attached to rock, an example of intraspecific variation.

Open in a separate window

Fig. 2.

Basal members of tristichoid river-weeds. (A–E) Tristicha trifaria (Bory ex Willd.) Spreng. [Novelo & Philbrick s.n. March 1992: Mexico, Jalisco]. (A) Floral shoot with terminal flower (arrow) and three photosynthetic shootlets (S), called ‘ramuli’, with scale-like leaves along three rows. (B) Tip region of 12mm long vegetative shoot with four ramuli (S1–S4). Note additional scale-like leaves inserted along stem (X). (C) Upper portion of fully grown ramulus (total length 3cm). (D) Lateral view of meristematic ramulus tip (slightly curved). (E) Ribbon-like root with capless tip, seen from below. Note presence of adhesive hairs (‘root hairs’) on lower surface. (F) Terniopsis malayana (Dransfield & Whitmore) M.Kato [Dransfield KEW#30762: Malaysia, Malaya]: Creeping root (R), seen from above, with young ramulus, showing scale-like leaves in three rows. Scale bars=1mm in A, B, C–F; 0·05mm in D.

Open in a separate window

Fig. 3.

Tristichoid river-weed Indotristicha ramosissima (Wight) van Royen [Rutish. & Huber #27/185: India, Kerala]. (A) Seedling with two cotyledons (C) and short-lived plumule, adventitious root (R) as exogenous outgrowth of hypocotyl. Note adhesive hairs replacing radicle. (B) Flower in anthesis, perianth (P) overtopped by three stamens and stigma (arrow). (C) Tip of nearly mature ramulus (total length 12mm), showing scale-like leaves in helical arrangement. (D) Portion of creeping, ribbon-like root (R), seen from above. Note endogenous origin of disk-like holdfast (H), fixing the shoot bud (black arrow) to the rock. (E) Transversal section of growing ramulus tip. Note spiral arrangement of broad scale-like leaves, consisting of a single cell layer each. (F) Meristematic tip of young ramulus giving rise to ligulate leaves (asterisks). Apical meristem (M) conical and slightly curved. Scale bars=1mm in B, C, E; 0·5mm in A, D; 0·1mm in F.

Open in a separate window

Fig. 4.

Tristichoid river-weed Dalzellia zeylanica (Gardner) Wight [Rutish. & Huber #25/181: India, Kerala]. (A) Crustose creeping shoot (resembling foliose lichen) in vegetative stage, as seen from above; scale-like leaves inserted on upper surface and along margin. (B) Mature stage of crustose creeping shoot, as seen from above; most scale-like leaves dropped. Note reproductive short shoot with floral bud (asterisk), embedded in a fringed cup (cupule). (C) Young short shoot with floral bud (asterisk), showing endogenous origin in cortical tissue of crustose shoot. (D and E) Marginal portion of two young crustose shoots, as seen from below. Arrow points to ‘shoot meristems’ where new marginal leaves are initiated. Note scale-like leaves (with midrib) of variable shape. (F) Flower (prior to anthesis) with three tepals (T), three stamens (A), trimerous ovary. Scale bars=1mm in A, B; 0·3mm in C–E; 0·2mm in F.

Open in a separate window

Fig. 5.

Tristichoid river-weed Indodalzellia gracilis (Mathew, Jäger-Zürn & Nileena) Koi & M. Kato [C.R.Mathew #MRPII/430&II/470: India, Kerala]. (A) Cross-section of ribbon-like root (R), giving rise to root-borne crustose shoot on the left flank. (B) Close-up (see insert in A); arrow points to shoot meristem. Note scale-like leaves (L) that mainly consist of one cell layer. (C) Cross-section of root (R) with two finger-like holdfasts (H), growing downwards to reach the substrate. (D) Close-up of holdfast epidermis (see insert in C), showing adhesive hairs. (E) Close-up of crustose shoot, seen from above; dorsal leaves (dL) smaller than marginal leaves (mL). Scale bars=0·5mm in A,C; 0·1mm in B, D, E.

Open in a separate window

Fig. 6.

Brazilian podostemoid river-weed Diamantina lombardii Novelo, Philbrick & Irgang [Philbrick #5647/5783: Brazil, Rio do Peixe near Diamantina]. (A) Ribbon-like creeping root (R) giving rise to stem (X) with disk-like holdfast (H). (B) Ribbon-like root with capped tip (Rc). (C) Upper portion of vegetative shoot, digitate leaves, each with elongate middle finger and much shorter lateral ones. Numerals 1–4 indicate distichous phyllotaxis. (D and E) Two views of shoot tip with two flowers. Sub-terminal flower with ovary (O) and two stigmas, subtended by open bract (arrows). Terminal flower (F) covered by tubular spathella. Scale bars 1mm in A, C; 0·5mm in B, D, E.

Open in a separate window

Fig. 7.

African podostemoid river-weed Ledermanniella linearifolia Engl. [Ghogue #1415: Cameroon, Lobé Falls]. (A–C) Transversal sections of crustose roots, with endogenous root-borne shoots (carrying leaves L) arising from upper surface; arrow in close-up (B) indicates position of indistinct shoot meristem. Cell rows inside crustose roots result from thickening growth. Note remnants of adhesive layer (black) on lower root surface. (D–F) Cross-sections of floral bud inside spathella (Fc), with two stamens (A), hanging ovary (O) and pedicel (Fp). Details: (E) anther with pollen dyads; (F) non-septate ovary with ovules on central placenta. Scale bars=0·5mm in A–D, F; 0·1mm in E.

Open in a separate window

Fig. 8.

African podostemoid river-weed Stonesia ghoguei E. Pfeifer & Rutish. [Ghogue #1665/1668: Cameroon, Adamaoua]. (A) Tip of ribbon-like root, lacking root cap. Note adhesive hairs on lower (inner) root surface, and root-borne shoot with forked leaf. (B) Tips of exogenously branching root ribbon, seen from above. (C) Inverted flower bud (spathella removed), with stamen (A), ovary (G), tepal (T). (D) Transversal stem section, with two lateral short shoots containing floral buds (asterisks). (E and F) Leaf (L) and flowers (asterisks) as epiphyllous outgrowths, arising from angles of forked mother leaf (M). Scale bars=1mm in A, B, D–F; 0·5mm in C.

Open in a separate window

Fig. 9.

Schemes of stolon branching in various bladderworts (Utricularia), showing dorsiventral symmetry. Mother stolons (runners) with dorsiventral branching pattern: green=upper stolon sector, blue=lower sector. Stolon tips (apical meristems) straight or coiled (‘circinate’), depending on the subgenus (and section) in Utricularia: U. alpina (sect. Orchidioides) as epiphytic member, U. longifolia (sect. Foliosa) as epilithic member, U. sandersonii (sect. Calpidisca) as terrestrial member of subgenus Bivalvaria, U. vulgaris s.l. (sect. Utricularia) as aquatic member of Utricularia subgenus Utricularia. Stolon outgrowths (as seen from distal end) are abbreviated as follows: R, rosette of various appendages; L, leaf; A and a, thick and thin daughter stolons; L/A, daughter stolon and leaf arise from same position (homotopic); u, trap (bladder); J (red arrow), inflorescence. All outgrowths (appendages) are inserted along dorsal (green) and lateral stolon sectors, none along ventral (blue) sector. Rosettes in U. longifolia and U. sandersonii are inserted in proximal (‘wrong’) axil of foliage leaf (L) along dorsal sector of mother stolon (A).

Open in a separate window

Fig. 10.

Aquatic bladderworts (section Utricularia in subgenus Utricularia): (A and B) Utricularia australis R.Br. [Rutish. #88710: Switzerland]. (A) Compound leaf with two branched lobes (immature), both with many traps. (B) Mature trap with lateral mouth, two dorsal appendages (branched) and lateral setae (simple). (C–F) Utricularia aurea Lour. [Rutish. & Huber #8907036: India, Kerala]. (C and D) Coiled (‘ciricinate’) meristematic tips (white arrows) of stolons (watershoots), with lateral insertion of bilobed leaf primordia (L), each with upper (u) and lower (l) lobe; inflorescence bud (J) arising from upper stolon sector. (E) Curved tip of air-shoot. (F) Distal portion of stolon (W, watershoot) after removal of leaves; inflorescence buds (J) and air-shoots (E) inserted along upper (dorsal) stolon sector. (G) Branching scheme, as valid for many aquatic bladderworts (section Utricularia): stolon portion of watershoot (W, seen from distal end), showing dorsiventral symmetry (us, upper sector; ls, lower sector); laterally inserted leaf (L) with upper (u) and lower (l) lobe; inflorescence (J), accompanied by branch watershoot (BW) and anchor stolons (S; ‘rhizoids’ or ‘floats’); extra-axillary air-shoot (E) inserted along dorsal stolon sector. See Fig. 9 (bottom right) for a more generalized branching scheme of U. vulgaris s.l. Scale bars=1mm in A, F; 0·3mm in B, D, E; 0·1mm in C.

Open in a separate window

Fig. 11.

Float-bearing aquatic bladderwort Utricularia stellaris Linn.f. [CDK Cook s.n.: India, Rajastan]. (A) Tip of stolon (W, watershoot) with inflorescence apex (J), floral meristems (F) subtended by bracts (T); S, float primordia (replacing anchor stolons). (B and C) Immature and (nearly) mature whorls of spongy floats (S), respectively; note aerenchyma inside. (D) Portion of stolon (watershoot) with branch watershoot (BW). Asterisks indicate stipule-like auricles. Abbreviations of other appendages as in Fig. 10. (E) Cross-section of inflorescence axis (peduncle), showing vascular ring. (F) Young flower, subtended by bract (T); with two sepals (S), two stamens (A) and lower corolla lip (P, upper lip hidden). Scale bars=1mm in B–D; 0·1mm in A, E, F.

Open in a separate window

Fig. 12

Terrestrial bladderwort Utricularia sandersonii Oliv. [cultivated material: Bot. Garden Zurich]. (A and B) Two views of same plant portion, with young inflorescence axis (J), capillary runner stolons (A) giving rise to petiolate leaves (L) with cuneate blades. Asterisk indicates young daughter stolon. (C) Close-up of young rosette inserted in proximal (‘wrong’) axil of foliage leaf (L) along dorsal sector of runner stolon (A). Arrows indicate growth direction of both runner stolon and inflorescence (J) axis. Asterisk indicates primordial daughter stolon. Note trap stalk (U) as lateral stolon appendage. (D) Stolon (A) carrying stalked young traps (U). (E) Nearly mature trap with stipitate glands around terminal mouth. (F) Quadrifid gland inside trap. Scale bars=1mm in A, B; 0·5mm in C–E; 0·1mm in F.

Open in a separate window

Fig. 13

Rheophytic bladderwort Utricularia neottioides A.St.Hilaire & Girard [Vogel s.n.: Brazil. (A) Basal portion of inflorescence stalk (J) with claw-like anchor stolons (‘rhizoids’) fixing plant to rock. (B) Another portion with creeping main stolon (A) giving rise to minor claw-like stolons. (C) Close-up of branched tip of claw-like anchor stolon, seen from below. Note adhesive hairs. Scale bars 1mm in A, B; 0·1mm in C.

Open in a separate window

Fig. 14

Corkscrew plant Genlisea repens Benj. [Bütschi s.n.: Venezuela, Auyan Tepui]. (A) Seedling with rosette of green leaves. (B) Shoot meristem of seedling with putative leaf primordium (L?) and putative eel trap primordium (U?). (C) Peltate (ascidiate) eel trap primordium with transversal slit. (D) Young foliage leaf with spoon-like blade. (E) Proximal portion of nearly mature eel trap (‘rhizophyll’), artificially opened. Note bulb (with digestive glands) and tube (with bristles inside, arranged in rings). (F) Proximal portion of nearly mature eel trap (‘rhizophyll’), showing one of the two twisted arms (corkscrews) with helical slit. (G) Close-up of bristly slit (see insert in F), as entrance path for prey. Scale bars=1mm in A, E, F; 0·1mm in B, C, D, G.

Molecular systematics

The family is sister to Hypericaceae (within clusioid Malpighiales, eudicots) based on molecular phylogenetic evidence (Ruhfel et al., 2011). The three river-weed subfamilies can be distinguished by floral and capsule structures. There are three carpels (capsule valves) in the Tristichoideae and two carpels in Podostemoideae and Weddellinoideae. The Podostemoideae have their flowers enclosed by a sack-like or tubular cover (‘spathella’) that is lacking in Weddellina, the only genus in Weddellinoideae (Cook and Rutishauser, 2007; Koi and Kato, 2007; Kato, 2013). Molecular phylogenies strongly improved our knowledge of the evolutionary and biogeographical history of river-weeds, leading to many taxonomic changes and proposals for regrouping (Kita and Kato, 2001; Moline et al., 2007; Thiv et al., 2009; Ruhfel et al., 2011; Tippery et al., 2011; Koi et al., 2012; Khanduri et al., 2014). Promising studies published from the Japanese schools of Imaichi and Kato allow deeper insights into the developmental genetics of various Podostemaceae. Because the two main subfamilies, Tristichoideae and Podostemoideae, are morphologically divergent, we will present them in separate sections below.

Tristicha and Terniopsis as related genera with similar morphologies (Fig. 2)

Tristicha and Terniopsis (also Indotristicha) possess photosynthetic short-lived shootlets (called ‘ramuli’, singular ‘ramulus’). These ramuli are fine axes (up to a few centimetres long) that carry scale-like leaves along three rows (Tristicha and Terniopsis, Fig. 2A–F; Fujinami and Imaichi, 2009). Young ramuli show conical, slightly curved apical meristems (Fig. 2D). Dalzellia and Indodalzellia, however, lack ramuli (see next paragraphs). All tristichoid genera (except Tristicha) are restricted to Asia (Kato, 2006, 2013). Tristicha is the only genus that occurs with one polymorphic species (T. trifaria) in both the New World (America from Mexico South to Northern Argentina) and the Old World (Africa, Madagascar and the Mascarene Islands). Before molecular data were available, even populations (forms) from East Asia to North-Eastern Australia were added to Tristicha because they all share ‘ramuli’ with scale-like leaves in three lines (Fig. 2F). Due to molecular data showing paraphyly (e.g. Koi et al., 2012), it became obvious that the Tristicha-like Asian to Australian taxa need to be separated as genera (Cussetia, Terniopsis). Tristicha differs from Terniopsis: usually one (rarely two) stamen per flower and a capless root in Tristicha (Fig. 2E), and usually two (rarely three) stamens per flower and a capped root in Terniopsis. In the polymorphic Tristicha trifaria sensu lato (s.l.), some African populations (accepted as T. alternifolia until 1950, e.g. in Angola) show elongated and branched tristichous ramuli whereas other African and all New World populations [accepted as T. hypnoides, syn. T. trifaria sensu stricto (s.s.) in earlier days] have rather short ramuli with dense rows of scale-leaves (Fig. 2A–C). Fujinami et al. (2013) studied the developmental morphology of T. trifaria s.l., showing the complex formation of a basal shoot disk that is closely attached to the substrate. Fujinami et al. (2013) accepted for the basal disks of Tristicha congenital fusion of various shoot axes orders, as will be discussed below under Dalzellia.

Dalzellia–Indotristicha lineage: saltational loss of root–shoot bauplan in Dalzellia with a crustose vegetative shoot, as compared with the closely related Indotristicha with roots and shoots (Figs 3 and ​and44)

Dalzellia and Indotristicha are sister genera in Asian Tristichoideae with distinctly different morphologies. The best known example is represented by the two species Dalzellia zeylanica and Indotristicha ramosissima from South Asia (especially South India and Sri Lanka). Both Dalzellia and Indotristicha are closely related genera forming a sub-clade: the monotypic genus Indotristicha is sister to the genus Dalzellia that contains five species (Koi et al., 2012; Kato, 2013).

Indotristicha ramosissima appears to be a rather conventional flowering plant with regard to its vegetative bauplan. Like Tristicha and allies (see above), Indotristicha has short-lived photosynthetic shootlets (‘ramuli’). Unlike Tristicha, the scale-like leaves in the I. ramuli are inserted spirally or irregularly (Fig. 3C, ​,E,E, ​,F).F). The plant body of I. ramosissima consists of ribbon-like adhesive roots (with cap) and root-borne, branched shoots up to 64cm long (Rutishauser and Huber, 1991). Seedlings of I. ramosissima have secondary roots arising exogenously from the hypocotyl (Fig. 3A). The radicle stops growth after the formation of some adhesive hairs. The plumule usually is short-lived. The secondary roots elongate and branch before giving rise to root-borne shoots. They arise from endogenous buds together with flattened holdfasts that fix the outgrowing leafy stems to the rock (Fig. 3D).

Dalzellia zeylanica s.l. (including closely related species such as D. ubonensis) deviates strongly from the conventional bauplan of flowering plants. The shoot is crustose (foliose) and adheres to the rocky substrate like a foliose lichen, whereas the root is lacking (Fig. 4A, ​,B,B, ​,D,D, E; Imaichi et al., 2004; Fujinami and Imaichi, 2015). The crustose shoot shows dorsiventral construction: scaly leaves are restricted to its margin (‘marginal leaves’) and its upper surface (‘dorsal leaves’). No leaves are found on the lower surface that is attached to the substrate. The crustose shoot of D. zeylanica was explained as a result of congenital fusion of various shoot axes orders (‘coenosome’ sensu Jaeger-Zuern, 1992, 1995, 1997, 2003). This interpretation was taken over by Imaichi et al. (2004), Fujinami et al. (2013) and Fujinami and Imaichi (2015). According to Jaeger-Zuern (2003), the shoot apical meristem (shorter: shoot meristem) of D. zeylanica is not conical (in contrast to T. trifaria and I. ramosissima), but wide and flat. The crustose shoot of D. ubonensis (D. zeylanica s.l.) appears to be formed by zonal growth in the common region behind several shoot meristems, as well as by marginal meristems that spread among the shoot meristems (Fujinami and Imaichi, 2015). Flowers in D. zeylanica arise from endogenous buds in the cortex of the dorsiventrally flattened shoots. When the crustose shoots start to emerge at the end of the monsoon, most of the exogenous scale-like leaves are dropped (erased). Then there is meristematic activity inside the shoot cortex below the upper surface, giving rise to rosettes of scale-like leaves and finally to flower buds, each of which is surrounded by a fringed cup (‘cupule’) (Fig. 4B, ​,CC).

Indodalzellia gracilis (Fig. 5) as the missing link between Dalzellia and Indotristicha?

Indodalzellia gracilis was discovered and described as a new taxon by Mathew et al. (2001). This species, endemic to South India (Kerala), was first thought to be a member of Dalzellia (as D. gracilis). In agreement with molecular findings, it was put into a genus on its own (Koi et al., 2009). Phylogenetically it is sister to the sub-clade consisting of Indotristicha and Dalzellia. Indodalzellia is derived from the paraphyletic Tristicha and Terniopsis but sister to the Dalzellia–Indotristicha lineage (Koi et al., 2012). With respect to its morphological features, I. gracilis can be regarded as intermediate between Indotristicha and Dalzellia. Indodalzellia (Fig. 5A) has ribbon-like creeping roots, being convex on the upper side and slightly concave or planar below, similar to Indotristicha, Tristicha and Terniopsis (Figs 2E, ​,FF and ​and3D).3D). The Indodalzellia root is capless like the Tristicha root. When the roots cannot directly fix to the rocky substrate, finger-like holdfasts grow out along the root flanks turning downwards until they reach the substrate (Fig. 5C). They stick to the rock by adhesive hairs (Fig. 5D). The root-borne shoots of Indodalzellia arise from the root flanks (probably from endogenous buds, as indicated by Koi et al., 2009). Finally, the strongly flattened shoots (stems) are fixed to the substrate on the lower side. They carry dimorphic scale-like leaves on their upper surface, larger ones along the margin and smaller ones on the dorsal surface (Fig. 5E). This pattern with two kinds of scales is identical to what is known from D. zeylanica s.l. (Fig. 4).

Podostemoideae with rather stable floral bauplans: from polyandrous flowers in the New World to oligostemonous flowers elsewhere

Podostemoid flowers show some variation with respect to the number of stamens and tepals, the latter being inconspicuous throughout. Various American podostemoids have insect-pollinated (and even scented) flowers with a whorl of 6–12 showy (white to pink) stamens and as many inconspicuous tepals (as observable in several species of Apinagia or Marathrum, Fig. 1A). Other entomophilous podostemoids increase the number of showy stamens per flower up to 40 (e.g. various species of Apinagia, Marathrum, Mourera and Rhyncholacis; see Tavares, 1997; Cook and Rutishauser, 2007, Kato, 2013).

In many New World Podostemoideae (e.g. Podostemum) and all Old World genera (mainly Africa and Asia) the flowers become dorsiventral by stamen loss on one side, finally leading to flowers with one stamen (e.g. Fig. 8C) or two stamens. All podostemoids having only 1–2(–4) stamens per flower depend on wind pollination (i.e. flowers less conspicuous, without scent). If two stamens per flower are present, their filaments usually have a common base (‘andropodium’), leading to a Y-shaped structure with two anthers (e.g. Figs 1B and ​and7D).7D). The family name ‘Podostemaceae’ (based on the genus Podostemum) refers to this distinctive feature. Perhaps as an adaptation to anemogamy, various African podostemoids (but none outside Africa) evolved firm (i.e. non-decaying) pollen dyads instead of having single pollen grains (e.g. Ledermanniella linearifolia, Fig. 7E; Ameka et al., 2003; Grob et al., 2007b; Moline et al., 2007).

All podostemoid flowers have superior ovaries with two fused carpels forming two locules, or only one due to septum loss, as typical for several derived African genera (e.g. Fig. 7F: Ledermanniella; Ameka et al. 2003). In all non-African groups, the flower buds are upright and sessile (Fig. 6D, E), whereas in most African Podostemoideae the flower buds are completely inverted (Figs 7D and ​and8C).8C). An inverted floral bud inside the spathella may be seen as an adaptation that increases the speed of spathella rupture and the quick onset of anthesis once the plants emerge from the water (Cook and Rutishauser, 2007).

Continuum from ribbon-like to crustose roots

Root ribbons (width up to 10mm) with endogenous shoot formation along the root margins are found in many Podostemoideae, e.g. Stonesia ghoguei (Fig. 8A). The ribbon-like roots of several podostemoids may have tips covered by a dorsiventral root cap (Fig. 6B). Capped roots in Podostemoideae usually show the endogenous origin of lateral roots. In other podostemoids with ribbon-like roots the tips lack caps, and root branching happens exogenously (Fig. 8A, ​,B).B). Various Old World podostemoids possess even broader roots (up to several centimetres wide) with endogenous shoots arising from the upper surface (e.g. Figs 1C and ​and7A,7A, ​,B).B). These disk-like roots in Podostemoideae are usually labelled as ‘crustose’ or ‘thalloid’, also ‘foliose’ because they resemble foliose lichens (Ota et al., 2001; Hiyama et al., 2002; Kato, 2004). Crustose roots in Africa and Asia may have evolved three or four times independently from groups having ribbon-like roots (Koi et al., 2006; Moline et al., 2007). Possible root transformation series in Podostemoideae were illustrated in Rutishauser and Moline (2005, their fig. 6).

Prominent shoots with non-axillary branching and terminal double-sheathed leaves

In most angiosperms, axillary branching along stems entails the production of a lateral shoot bud in the distal axil of a subtending leaf. Conventional axillary branching as known from typical angiosperms occurs only rarely in Podostemoideae, e.g. in Saxicolella submersa (Ameka et al., 2002). In many Podostemoideae (e.g. Ledermanniella bowlingii and Podostemum ceratophyllum) there are leaves with two sheaths that are inserted laterally and opposite each other. Such leaves have been called double-sheathed or ‘dithecous’ by Warming (e.g. 1891) and others (Rutishauser, 1997; Rutishauser and Grubert, 2000; Ameka et al., 2003; Rutishauser et al., 2003; Moline et al., 2006; Ghogue et al., 2009). The occurrence of double-sheathed leaves among conventional (i.e. single-sheathed) leaves allows the stem to branch by a peculiar process that, due to the absence of a more appropriate term, may be called ‘bifurcation’. As long as a stem is developing single-sheathed leaves, it grows in a monopodial manner. Then, a double-sheathed leaf appears in the terminal position, giving rise to new shoot modules (daughter shoots) in each sheath, or one of the two sheaths is replaced by a flower instead of a daughter shoot. The many-flowered sword-like inflorescences (up to 60cm long, including the stalk) of Mourera fluviatilis from northern South America consist of two rows of double-sheathed bracts that are initiated in a basipetal order (Rutishauser and Grubert, 1999). The double-sheathed leaves in podostemoids resemble to some degree laterally flattened (i.e. ensiform) leaves in more typical angiosperms such as Acorus and Iris (Jäger-Zürn, 2000, 2003, 2007).

Floral sites along roots, shoots and leaves in Podostemoideae

Unlike conventional flowering plants, floral buds in several Podostemoideae are initiated nearly everywhere on the vegetative body. Flowers arise from endogenous buds on the upper surface of flattened roots (e.g. in Ledermanniella linearifolia, Fig. 7A, ​,B),B), or they are initiated along the stems (e.g. Stonesia ghoguei, Fig. 8D), starting as endogenous buds by dedifferentiation of parenchyma cells inside the stem cortex. The buds finally protrude the stem periphery, rupturing the outer cortical layers and epidermis (Pfeifer et al., 2009). Endogenous formation inside the undamaged stem protects the flower buds from the rushing and damaging water. They protrude and open quickly when the water level has dropped sufficiently. A few African Podostemoideae show epiphyllous flowers that are inserted on leaves. In S. ghoguei they are initiated in the clefts (angles) of forked leaves (Fig. 8E, ​,F;F; Moline et al., 2007; Pfeifer et al., 2009). Both epiphyllous flowers and endogenous bud formation inside the stem may be understood as the result of ectopic expression of flower identity (Rutishauser and Moline, 2005; Rutishauser et al., 2008; Tsukaya, 2014).

Shoot apical meristems cryptic or even lacking in Podostemoideae

Tristichoideae and Weddellinoideae usually have obvious SAMs that produce laminar leaves on their flank (Figs 2D and ​and3F;3F; for Weddellina, see Koi and Kato, 2007). On the other hand, in the more derived subfamily Podostemoideae, the shoots lack recognizable SAMs with permanent stem cells. They are cryptic (indistinct) and difficult to observe in the vegetative shoots of Podostemoideae (Rutishauser et al., 2003; Jäger-Zürn, 2007). According to Japanese studies (e.g. Imaichi et al., 2005; Katayama et al., 2008, 2010, 2013; Koi and Kato, 2010), the leaf primordium in vegetative shoots develops from the base of the opposing second youngest leaf primordium. The initiation of a new leaf primordium appears to be associated with degeneration of neighbouring cells, as shown by Imaichi et al. (2005), Koi et al. (2005), and Koi and Kato (2010) for Asian Podostemoideae. Such leaf formation is repeated, resulting in a chain of leaves.

Flowers in Lentibulariaceae with stable bauplans (Fig. 11F)

The three genera (Genlisea, Pinguicula and Utricularia) in this family have flowers with a stable (developmentally robust) bauplan (Lloyd, 1942; Degtjareva and Sokoloff, 2012). As typical for several families of the Lamiales (Asteridae) within eudicots, the zygomorphic insect-pollinated flowers consist of a bilabiate sympetalous corolla, made up of five connate petals with a spur usually containing nectar (Hobbhahn et al., 2006; Fleischmann, 2012a; Clivati et al., 2014). The resulting flower type is called a masked flower (snap-dragon type blossom) because the entrance to the throat and nectar spur is sealed to some degree. In all Lentibulariaceae, the androecium consists of two stamens that are hidden inside the upper corolla lip. The gynoecium consists of a superior ovary topped by a two-lobed stigma (being sensitive in various Utricularias). Its arrangement relative to the androecium usually prevents autogamy (self-pollination) although some Utricularias are known to be self-compatible or even cleistogamous inbreeders (Jérémie, 1989; Khosla et al., 1998; Clivati et al., 2014). The main difference in Lentibulariaceae is found in sepal number: Pinguicula and Genlisea with five calyx lobes per flower, Utricularia subgenus Polypompholyx with four calyx lobes and all remaining bladderworts with two sepals per flower (Fig. 11F; Grob et al., 2007a; Degtjareva and Sokoloff, 2012; Fleischmann, 2012a, his fig. 103). If there is more than one flower per raceme (as typical for Genlisea and Utricularia), the lateral ones are subtended by a bract (Fig. 11A, ​,F).F). Along the inflorescence axes all Utricularias behave like typical angiosperms, showing axillary branching. Therefore, bladderworts can be viewed as one phase only misfits (cf. Minelli, 2015b) because they return to the conventional branching pattern while forming flowers (Rutishauser and Isler, 2001).

Released bauplans in the vegetative (non-flowering) parts of Utricularia and (less so) in Genlisea

Kaplan (1998, Vol. 3, p. 75) wrote on the unusual morphologies in Utricularia: ‘While its flowers and inflorescences are fairly stereotypical, its species exhibit an incredible polymorphism vegetatively, which superficially, at least, seems to defy all the principles of vascular plant organography and have caused no end of interpretive problems and arguments.’ Axillary shoot branching as typical for conventional seed plants (with daughter modules arising from the distal axils of subtending leaves) is still found in leaf rosettes of Pinguicula (Grob et al., 2007a). Axillary branching, however, is lacking or less obvious during vegetative growth of Genlisea and Utricularia (Lloyd, 1942). Genlisea (usually regarded as rootless) and Pinguicula (still with roots) can be viewed as slight modifications of the CRS model, whereas strongly released (decanalized) body plans are typical in the vegetative parts of all bladderworts (Jobson and Albert, 2002; Jobson et al., 2004). Lloyd (1942, p. 213) was aware of this fact while writing on Utricularia in general: ‘They represent a complex and puzzling morphology. They are entirely rootless, even in the embryonic condition. The distinction between stem and leaf is vague. Only in the inflorescence and in certain shoots (air-shoots of U. vulgaris etc.) is the morphology easily recognizable.’ Within the Lentibulariaceae, the loss of the CRS bauplan in bladderworts was not correlated to a switch from terrestrial to aquatic habitats because the released bauplans occurred already in basal Utricularias (including subgenus Polypompholyx) that are terrestrial taxa although their bladders need to be water-filled for firing and catching prey (Taylor, 1989; Reut and Fineran, 2000).

Vagueness (fuzziness) of organ identities in Utricularia (bladderworts): ‘stolons’ and ‘leaves’ as neutral terms for describing the vegetative bodies in the Genlisea–Utricularia lineage

Taylor (1989, p. 6) wrote in the introduction to his Utricularia monograph: ‘For taxonomic and descriptive purposes, whatever their true or theoretical nature, it is desirable to have a consistent terminology for the various organs.’ Most Utricularias produce root-like organs or runners that were called ‘stolons’ (horizontal shoots) and ‘rhizoids’ (anchoring organs) by Taylor (1989) and Adlassnig et al. (2005). They are labelled as ‘runner stolons’ and ‘anchor stolons’, respectively, by Reut and Fineran (2000). In addition there is a range of leaf-like organs (called ‘leaves’ by Taylor 1989). The vagueness (fuzziness) of organ identities in Utricularia allowed contradictory interpretations, as already discussed by Arber (1920). Stolons and rhizoids have been viewed as stem homologues, including phyllomorphic shoots (Troll and Dietz, 1954; Fleischmann, 2012a), as leaf homologues (Goebel, 1891; Kumazawa, 1967; Kaplan, 1998) or even as ‘fuzzy organs’ blending (amalgamating) the developmental programmes of leaves and shoots (Rutishauser and Sattler, 1989; Sattler and Rutishauser, 1990; Rutishauser, 1999; Rutishauser and Isler, 2001). Thus, it is still a question of biophilosophical outlook if botanists choose a classical or a fuzzy perspective for describing and interpreting the vegetative bodies in bladderworts (although the fuzzy view accords more with what is observable). In order to obtain an impression of the vast morphogenetic possibilities found in the Genlisea–Utricularia lineage, the developmental morphology of some Utricularia members (Figs 9–13) and one Genlisea species (Fig. 14) will be presented below.

Branching patterns and structural units as observable in the vegetative bodies of aquatic bladderworts (subgenus Utricularia – section Utricularia, see branching schemes Figs 9 and 10G)

The developmental morphology of aquatic bladderworts (section Utricularia) such as Utricularia aurea, U. australis, U. foliosa, U. gibba, U. macrorhiza, U. stellaris and U. vulgaris (Figs 9–11) is quite well known (Arber, 1920; Lloyd, 1942; Troll and Dietz, 1954; Rutishauser and Sattler, 1989; Sattler and Rutishauser, 1990; Rutishauser, 1993; Chormansky and Richards, 2012). I give here a short overview of the branching patterns of aquatic bladderworts because both Utricularia species with published genome (transcriptome) analyses belong to this group: U. gibba and U. vulgaris (Ibarra-Laclette et al., 2011, 2013; Veleba et al., 2014; Bárta et al., 2015; Carretero-Paulet et al., 2015a, b). Each ‘leaf’ or leaf-like organ in the aquatic bladderworts (sect. Utricularia) consists of two branched lobes that can be equal in size, both carrying several bladders, as observable in U. australis (Fig. 10A). Alternatively, the two ‘leaf’ lobes are different in size and trap number, with the upper lobe short, photosynthetic and provided with few bladders, whereas the lower lobe lacks chlorophyll, elongates and turns downwards into deeper water and mud, and is provided with many bladders (as found in U. foliosa; Sattler and Rutishauser, 1990). The bladders (traps) of aquatic bladderworts (sect. Utricularia) carry two branched dorsal appendages near the mouth, besides a few additional bristles (Fig. 10B). Growing stolon tips are coiled upwards, showing circinate vernation, with bifid leaf primordia inserted in a distichous phyllotaxis pattern along the two lateral sectors (stolon flanks, Fig. 10C). The growing tips of young ‘leaf’ lobes resemble the stolon tips, although they are less coiled (Fig. 10D). Thus, the stolons (also called ‘watershoots’) and the two-lobed ‘leaves’ have similar developmental pathways, indicating leaf–shoot indistinction (Sattler and Rutishauser, 1990; Rutishauser et al., 2008). The dorsiventral stolon symmetry is obvious with respect to the positional arrangement of inflorescence buds and (in some but not all aquatic Utricularias) so-called ‘air-shoots’ which are tiny filamentous stolons (with scale-like leaves) reaching the water surface. Both inflorescence buds and air-shoots arise from the dorsal (upper) sector of the main stolon in aquatic Utricularias (e.g. U. australis, U. aurea and U. stellaris, Figs 10D–G and 11D). The main stolons give rise to daughter stolons (branch watershoots), usually from near the inflorescence base (Fig. 10D, ​,G).G). Several aquatic Utricularias (e.g. U. australis, U. aurea and U. gibba) show additional stolon-like or root-like appendages arising from the lower end of the peduncle (inflorescence stalk), without being subtended by bracts or leaves. They were labelled as ‘anchor stolons’ or ‘rhizoids’, because they serve as anchoring organs in order to keep the inflorescence upright (Arber, 1920; Lloyd, 1942; Taylor, 1989). In a few aquatic species such as U. stellaris, the anchor stolons (rhizoids) at the peduncle base are replaced by a whorl of spongy floats (inflated buoys, Fig. 11B, ​,C),C), again helping to keep the inflorescence in an upright position during anthesis (Lloyd, 1942; Khosla et al., 1998). In aquatic species such as U. aurea, some populations produce floats whereas others have anchor stolons (Rutishauser, 1993). Various aquatic Utricularias living in cold-temperate climates (e.g. U. australis, U. macrorhiza and U. vulgaris) are perennial by surviving with turions (winter-buds) at the bottom of ponds and lakes (Taylor, 1989; Guisande et al., 2007; Adamec, 2010; Plachno et al., 2014b). Some of these are vegetative apomicts (e.g. U. australis and U. bremii) producing flowers but no seeds.

The developmental architecture of Utricularia gibba (also belonging to the aquatic bladderworts of section Utricularia) was illustrated by Chormanski and Richards (2012, their fig. 19). Their ‘architectural model’ for U. gibba needs improvement. Chormanski and Richards (2012) described the ‘leaves’ (leaf-like structures) in U. gibba as arranged spirally along the stolon; and they accepted daughter stolons (secondary stolons) and inflorescences as axillary outgrowths subtended by ‘leaves’ (leaf-like structures). According to Lloyd (1942) and Rutishauser (unpubl. data), U. gibba shows a distichous arrangement of the ‘leaves’, inserted along both flanks (lateral sectors) of the stolons. They show dorsiventral symmetry, with secondary stolons (lateral branches) and inflorescences arising from near the upper edge of the leaf insertion, but not in the leaf axil (Figs 9 and 10G).

Terrestrial Utricularias, e.g. Utricularia sandersonii, showing runner stolons with a dorsal row of ‘leaves’ (Fig. 12)

Utricularia sandersonii (from South Africa) belongs (together with U. livida and approximately another nine species) to the mainly African section Calpidisca within Utricularia subgenus Bivalvaria (Taylor, 1989; Veleba et al., 2014). They all are small terrestrial annuals, with capillary runner stolons (approx. 0·2mm thick), with petiolate entire leaves (total length up to 15mm, including obovate lamina in U. sandersonii, Fig. 12A, ​,B).B). Most of the bladder traps are inserted along the capillary stolons (Fig. 12D) or arise from the midrib and petiole on the lower leaf sides (Brugger and Rutishauser, 1989; Rutishauser and Isler, 2001, their fig. 15). The traps have their mouth fringed with radiating rows of gland-tipped hairs (Fig. 12E). As usual for all Utricularia traps, there are mainly four-armed glands (so-called quadrifids) covering the inner bladder wall (Fig. 12F). The branching scheme of the stolons (Fig. 9) illustrates the situation found in U. sandersonii and other Calpidisca members (Brugger and Rutishauser, 1989): the stolon tips are straight (i.e. not coiled as in aquatic members of sect. Utricularia, Figs ​Figs1010 and ​and11).11). The stolons nevertheless show a dorsiventral symmetry with respect to their morphogenetic potential of producing appendages: all leaves are inserted (‘riding’) along the upper (dorsal) sector (Figs 9 and 12A, B) whereas traps are inserted along the lateral sectors only (Fig. 12D). All additional outgrowths (such as inflorescences and daughter stolons) originate from buds along the upper stolon sector. The ‘leaves’ and their ‘axillary buds’ (rosettes) seem to be twisted 180° when compared with the axillary branching of conventional seed plants. The subtending leaf is in a more distal position along the stolon, whereas its axillary bud originates in a more proximal position (Fig. 12C). This inverse axillary (‘wrong’) position of rosettes along dorsal stolon sectors is also known from other non-aquatic Utricularias, e.g. U. dichotoma of subgenus Polypompholyx, and U. longifolia of subgenus Utricularia (Reut and Fineran, 2000; Rutishauser and Isler, 2001; see next paragraph).

Epilithic to epiphytic Utricularias, e.g. U. longifolia and U. alpina (Fig. 9)

Unlike the tiny U. sandersonii, there are (mainly in tropical America) epilithic to epiphytic species that are much larger with respect to flower size (up to 6cm) as well as size of vegetative parts such as leaves (up to 30cm long) and stolons (tubers in U. alpina with diameter >1cm). They belong to two sections within Utricularia subgenus Utricularia. Most epiphytic species (including U. alpina, U. humboldtii and U. reniformis) are members of section Orchidioides because their flowers resemble showy orchids (Jérémie, 1989; Taylor, 1989; Clivati et al., 2014). Utricularia longifolia belongs to sect. Foliosa s.l. (including Psyllosperma) as sister of sect. Orchidioides (Müller and Borsch, 2005; Veleba et al., 2014). Branching analyses of the vegetative bodies of these rather large plants were published by Troll and Dietz (1954), Brugger and Rutishauser (1989) and Rutishauser and Isler (2001). Members of sect. Orchidioides (e.g. Utricularia alpina) have coiled stolon tips (Fig. 9) whereas they are straight in U. longifolia. With respect to stolon branching and leaf position, all studied epiphytic (epilithic) Utricularias clearly exhibit stolon dorsiventrality, without outgrowths along the lower (ventral) sector and only tiny appendages (such as stalked bladders) along the lateral stolon sectors. Utricularia longifolia behaves similarly to U. sandersonii (Fig. 12C) with respect to the positions of leaves and axillary buds along the upper (dorsal) stolon sector, again with inverse position of the axillary bud and subtending leaf (Rutishauser and Isler, 2001, their figs 17 and 18). In U. alpina, both leaves as well as daughter stolons and inflorescences originate from extra-axillary meristematic buds (rosettes) along the upper (dorsal) stolon sector, not being associated with subtending leaves. The primordia arising from these meristematic buds show a delay with respect to their developmental fate. Thus, in early stages, it is not possible to decide if a primordium grows into a daughter stolon or into a foliage leaf (Brugger and Rutishauser, 1989; Rutishauser and Isler, 2001).

Haptophytic Utricularias, e.g. Utricularia neottioides, coming close to the habit of Podostemaceae (Fig. 13)

There are a few bladderworts adapted to river habitats as Podostemaceae, growing as affixed perennials (haptophytes) in swiftly flowing water, with their feet attached to submerged rocks. Taylor (1989) added these rheophytic species to his sections Avesicaria, Avesicarioides and Mirabiles, which do not form a clade in molecular phylogenies (Müller and Borsch, 2005; Guisande et al., 2007). Thus, the haptophytic habit evolved more than once in the genus Utricularia. As illustrated by U. neottioides (section Avesicaria; Fig. 13A–C), rheophytic Utricularias produce claw-like anchor stolons (rhizoids) that are provided with adhesive hairs (trichomes) along their lower (ventral) side. This is a nice example of convergence to the holdfasts in Podostemaceae, Hydrostachyaceae (eudicots) and seagrasses (monocots) such as Posidonia and Phyllospadix (Lloyd, 1942; van Steenis, 1981; Jäger-Zürn, 1998; Schäferhoff et al., 2010; Badalamenti et al., 2015).

Genlisea, the corkscrew plants, as sister genus to bladderworts (Fig. 14)

With only 29 species Genlisea is the smallest of the three lentibulariaceous genera, occurring in tropical America, Africa and Madagascar. Because Genlisea and Utricularia are sister genera (Veleba et al., 2014), a short introduction to the vegetative Genlisea body will be given here, using Genlisea repens (from Brazil and adjacent countries) as an example. It grows with often submerged rosettes and stolons in shallow acidic water (Fleischmann, 2012a). Its vegetative body consists of spathulate green leaves (up to 4cm long) and Y-shaped eel traps (up to 7cm long) that function in wet soil (Fig. 14A, ​,E,E, ​,F).F). Because these traps resemble roots (at least to some degree) they were labelled as ‘rhizophylls’ (i.e. root-leaves) by Goebel (1891). They attract and trap soil protozoa as well as invertebrates and even algae (Plachno et al., 2007, 2008). Both green leaves and eel traps in Genlisea arise as exogenous primordia from the same SAM (Fig. 14B). As typical for heterophyllous plants, some primordia turn into green leaves above the water level or mud (Fig. 14D), whereas others give rise to one eel trap each (Fig. 14C). An early developmental stage of a Genlisea trap consists of a stalk with a distal mouth-like cavity and two embryonal bulges (Fig. 14C). These bulges will elongate and twist, leading to the two catching arms (‘corkscrews’) with a longitudinal slit each (Fig. 14F, ​,G).G). In the meantime, the lower tube (including the digestion bulb) is formed (Fig. 14E).

Trap evolution in Lentibulariaceae

Plachno et al. (2007) found similarities in the digestive hairs and their fine structural features of the traps in Pinguicula, Genlisea and Utricularia. Nevertheless, it is difficult to imagine evolutionary transitions between the immobile traps of Pinguicula and Genlisea (Fig. 14E, ​,F)F) and the active traps in Utricularia (Figs 10B and 12D; Fleischmann, 2012a, his fig. 200). As already recognized by Darwin, the suction traps of the bladderworts belong functionally and architecturally to the most complex structures known from the plant kingdom (Lloyd, 1942; Reifenrath et al., 2006; Vincent et al., 2011; Adamec, 2011, 2013). Fleischmann (2012, p. 245) wrote: ‘It is hard to imagine how such bladder traps could evolve morphologically in a phylogenetic series, but this evolutionary step is certain to have happened quickly as a key innovation, rather than gradually.’ Both trap types of the Genlisea–Utricularia lineage (i.e. eel traps of Genlisea, and sucking traps in Utricularia) have an early developmental stage in common; they start as peltate (ascidiate) outgrowths (Figs 12D, ​,EE and 14C). Jobson et al. (2004) presented evidence that the key adaptation in the common ancestor of the Genlisea–Utricularia lineage ‘lies in molecular energetic changes that buttressed the mechanisms responsible for the bladderworts’ radical morphological evolution.’ There may be a link between faster reaction kinetics of Utricularia traps and a Utricularia-specific mutation in COX (cytochrome c oxidase) to obtain enough ATP energy (Jobson et al., 2004; Laakkonen et al., 2006; but see for criticism Adamec, 2011; Król et al., 2012).

‘Loss-of-root’ hypothesis vs. ‘root–stolon transformation’ hypothesis in the Genlisea–Utricularia lineage

It is commonly accepted that Pinguicula possesses true roots whereas the Genlisea–Utricularia lineage has lost them (Albert et al., 2010; Fleischmann, 2012a; Carretero-Paulet, 2015a, b). According to continuum plant morphologists (Brugger and Rutishauser, 1989; Rutishauser and Isler, 2001; Kirchoff et al., 2008), the roots were not completely lost in the Genlisea–Utricularia lineage. The ancestral roots (as still present in Pinguicula) evolved exogenous green appendages that can be called ‘leaves’ again (an idea anticipated by Arber, 1920). Thus, the developmental pathways for roots and shoots were blended (amalgamated) to some degree, perhaps due to co-option of genes usually acting in stems and leaves but not in roots. Arguments in favour of this ‘root–stolon transformation’ hypothesis are as follows. (1) Several Pinguicula have roots without caps (e.g. P. moranensis). (2) Various Utricularias (e.g. U. longifolia and U. sandersoniii) have straight stolon tips which look similar (including anatomy) to capless root tips of Pinguicula. (3) Although the Genlisea–Utricularia lineage has lost several root-specific genes, there are still some left in their vegetative bodies (see paragraph below). (4) Conversion of root meristems to shoot meristems are known from other angiosperms such as Nasturtium (Brassicaceae) and Neottia (Orchidaceae), pointing to some homology between root and shoot (as discussed by Guédès, 1979). (5) There are common genetic mechanisms that regulate both root and shoot meristems (Friedman et al., 2004; Stahl and Simon 2010; Hofhuis et al., 2013).

The two seemingly exclusive hypotheses on ‘loss-of-root’ vs. ‘root–stolon transformation’ in the Genlisea–Utricularia lineage will probably merge into one if developmental processes and gene actions are emphasized instead of mind-born and arbitrary structural categories (see paragraph below on ‘process morphology and morphospace’).

Increased mutation rates in Lentibulariaceae may have facilitated the evolution of species richness

The unusual lifestyle of the Lentibulariaceae coincides with genomic peculiarities such as the smallest genomes within angiosperms and extremely high nucleotide substitution rates of their genomes. The two sister genera Genlisea and Utricularia show the highest DNA mutation rates known amongst all flowering plants (Jobson and Albert, 2002; Jobson et al., 2004; Müller et al., 2004, 2006; Wicke et al., 2013; Carretero-Paulet et al., 2015a, b). Genome and transcriptome analyses were done in three ‘model’ species of Lentibulariaceae: Genlisea aurea, Utricularia gibba and U. vulgaris. Genome size appears highly variable in Genlisea and Utricularia, and occasionally with miniaturized genomes as low as 1C=63·4 Mbp, in spite of ancient polyploidization cycles (Ibarra-Laclette et al., 2011, 2013; Wicke et al., 2013; Veleba et al., 2014; Bárta et al., 2015). This fast molecular evolution could be connected to the fast speciation and diversification in this group, meaning that genetic shifts are frequent, directly influencing the morphological appearance and therefore the rapid evolution of traps (Jobson and Albert, 2002; Jobson et al., 2004, Albert et al., 2010; Fleischmann, 2012a).

Fuzzy concepts in plant morphology and evolutionary developmental biology

Morphological misfits as described for bladderworts and river-weeds transcend traditional structural categories, and cannot be placed fully into one category or the other. In these cases it becomes very difficult, or even impossible, to accept just one name for an organ or appendage. Here a continuum or fuzzy approach could be heuristically fruitful in which structural categories are used as ‘fuzzy sets’, allowing some degree of overlap with related terms (Rutishauser, 1999; Rutishauser et al., 2008). A fuzzy approach to plant morphology fits perfectly with the idea, propounded by Darwin (1859), that organisms were formed by gradual transitions between types (Kirchoff et al., 2008). This approach is similar to the concepts of partial homology and homeosis that were championed by Sattler (1986, 1988, 1994). Several developmental geneticists seem to be aware of a certain degree of fuzziness in plant development. They used fuzzy concepts such as the ‘leaf–shoot continuum model’ (Sinha, 1999), and ‘mixed shoot–leaf identity’ (Baum and Donoghue, 2002) to describe odd plant structures somewhat intermediate between leaves and shoots (stems) in angiosperms. Eckardt and Baum (2010) wrote: ‘It is now generally accepted that compound leaves express both leaf and shoot properties and that this at least partly reflects ectopic expression of genes related to STM in the leaf.’ Tsukaya (2014, p. 214) concluded similarly with respect to a leaf–shoot continuum in angiosperms: ‘Accumulating evidence has suggested that simple leaves, compound leaves, and shoots share common gene regulatory networks (GRNs).’ For example, Tsukaya (2014) provided developmental genetic data on the shoots with green ‘needles’ in asparagus: ‘The phylloclade of Asparagus asparagoides is a leaf-like metamorph of the lateral shoot, ectopically expressing some leaf genes.’

Lack of one-to-one correspondence between structural categories and gene expression

If structural categories do not provide adequate descriptions of plant structure, perhaps it is possible to define structures based on developmental genetics. If there is a one-to-one correspondence between structural units (e.g. roots, leaves and flowers) and the ‘molecular players behind the characters’ (Koentges, 2008), it should be possible to identify the structural units by the expression of well-characterized marker genes. To do this, we need to look for organ identity genes in order to define the structural categories clearly. For example, the KNOX/ARP module (as used by Katayama et al., 2010, 2013 in Podostemaceae) helps with the determination of the leaf as a determinate unit, and the shoot as an indeterminate module. This approach seems to have promise in the cases where control genes for organ identity have been shown to exist (Kirchoff et al., 2008, Langdale and Harrison, 2008; Chormanski and Richards, 2012). Thus, Katayama et al. (2010, 2013) identified the ‘leaves’ in Podostemoideae as ‘stem–leaf mixed organs’. This appellation is meant to indicate that these structures have some features of leaves, and some of stems, probably due to their unusual gene expression pattern and the lack of obvious SAMs (Kato, 2013). However, genomic studies in the Genlisea–Utricularia lineage may show the opposite (Ibarra-Laclette et al., 2011, 2013; Veleba et al., 2014; Barta et al., 2015; Carretero-Paulet et al., 2015a, b). They pointed to the existence of root-specific genes in the Genlisea–Utricularia lineage although their roots were lost (at least seemingly).

The lack of one-to-one correspondence between structural categories and gene expression may arise from the re-use of existing genetic resources in novel contexts. Transcription and signalling factors are often used multiple times in context-specific combinations within an organism (Weiss, 2005; Arthur, 2011). The case studies on bladderworts and river-weeds in the present paper point to plant structures that are difficult to explain by a simple one-to-one correspondence between structure and gene function (Kirchoff et al., 2008). Further genetic studies of these organisms will show that at least some of their phenotypic fuzziness results from overlapping or partially indistinct developmental genetic networks.

Process morphology: morphospace using a set of developmental processes, e.g. in aquatic Utricularias

Wardlaw (1965, p. 371), while pointing to the geologist Charles Lyell, came to the conclusion: ‘Organization is a continuum in the physical world. Organization is also a continuum in the ontogenesis and reproduction of the individual organism and in the phyletic line of which it is a component.’ Therefore, we may ask as a more specific question with respect to the bladderworts and river-weeds having unusual morphologies: is the recognition of developmental processes (e.g. branching patterns and growth patterns) more important than proper definition of structural units, i.e. plant organs such as roots, stems and leaves? Process morphology (or dynamic morphology) sensu Sattler (1994) and Jeune et al. (2006) allows us to dispense with all structural categories and characterize phenotypes by sets of developmental processes. The living forms we perceive and conceive of in the realms of multicellular organisms (animals, plants, fungi) ‘are only a small subset of the possible forms we could imagine’ (Minelli, 2015c). The theoretical morphospace includes all possible process combinations for seed plants, whereas the empirical morphospace contains only those process combinations that are realized in nature (Niklas, 1997, p. 215). Each axis of the morphospace corresponds to a variable that describes some developmental processes of an organism, or its parts. The use of a single morphospace to which gene expression can be annotated is appealing, especially so since its use would remove most, if not all of the terminological problems described above. Unlike rigid categorical vocabularies, process morphology should allow better hypotheses about the ‘molecular players behind the characters’ (Koentges, 2008). Thus, Sattler and Rutishauser (1990), Jeune et al. (2006) and Kirchoff et al. (2008) represented the vegetative bodies of aquatic Utricularias (e.g. U. foliosa) and other morphological misfits as combinations of developmental processes using multivariate statistical analyses. Plant organs (e.g. watershoots, leaves or bracts of U. foliosa) are identified in the morphospace as specific process combinations. No doubt the use of process combinations to describe plant structures makes communication among scientists difficult. Nevertheless, one of the great strengths of this approach is that the categorical terms (e.g. ‘leaf’ and ‘shoot’) serve only as placeholders for combinations of developmental processes that locate the organs in the morphospace. Gene expression patterns of the ‘model’ bladderworts (such as U. vulgaris and U. gibba) and related Genliseas may finally be annotated to the morphospace by associating the expression pattern with the combination of processes that are found in the part in which the gene is expressed (Kirchoff et al., 2008; Chormansky and Richards, 2012; Carretero-Paulet et al., 2015a, b).

Adaptive value of bauplan features vs. patio ludens

While introducing ‘adaptive walks in aquatic and terrestrial landscapes’ Niklas (1997) assigned a relative fitness to each phenotype in a morphospace, although this task is far from simple. Niklas (1997, p. 218) explained why: ‘The phenotypic plasticity of plants appears to be extremely high in comparison with that of most animals.’ According to Willis (1914), the unique features in which the various genera and species in Podostemaceae differ from one another cannot be explained as simply adaptational. This hypothesis was taken over by van Steenis (1981) who proposed the concept of ‘patio ludens’ (evolutionary playground). Plants in certain habitats evolved forms that are difficult to explain by adaptive occupation of species-specific ecological niches. According to Willis and van Steenis, the river-weeds evolved, in the more or less homogenous environments of waterfalls and river-rapids, new and fanciful mutants that did not (yet) become erased by natural selection. Some of these mutants, perhaps resulting from saltational evolution, became stabilized, leading to new species (see also Arber, 1920; Rutishauser, 1997). As expressed by Wardlaw (1965, p. 392ff) ‘patio ludens’ ideas are difficult to confirm, although it is also difficult to support the opposite, i.e. to assign a relative fitness (adaptive value) to each phenotype. Patio ludens coincides to some degree with what is labelled as ‘evolutionary freedom’ by Minelli (2015b, p. 335).

Physiological adaptations

With respect to bladderworts and river-weeds, one should keep in mind that physiological parameters such as seedling establishment, mineral nutrient uptake, photosynthesis, mitochondrial respiration and sexual vs. clonal reproduction may be more important than vegetative bauplan characters for successful speciation (survival of the fittest). Both families exhibit extreme physiological adaptations with respect to habitats. The unfavourable environmental conditions (including nutrient-poor habitats) of Lentibulariaceae and Podostemaceae may have been counterbalanced by efficient carnivory and symbiosis with cyanobacteria, respectively (Jäger and Grubert, 2000; Mohan Ram and Sehgal, 2001; Jobson et al., 2004; Laakkonen et al., 2006; Vincent et al., 2011; Król et al., 2012; Adamec 2013; Wicke et al., 2013; Plachno et al., 2014a).

Hopeful monsters and saltational evolution

Until recently, most evolutionary biologists were convinced that gradualism (cf. Darwin, 1859) reflects the most frequent mode of evolution. Drastic (saltational) evolutionary innovations of new phenotypes were regarded as highly improbable by most evolutionary biologists (Niklas, 1997; Arthur, 2011). However, in some cases, profound (saltational) changes may have occurred within one or a few generations. Organisms with a profound mutant phenotype that have the potential to establish a new evolutionary lineage have been termed ‘hopeful monsters’ (Goldschmidt, 1952; Bateman and DiMichele, 2002; Theissen, 2006, 2009). Recent discoveries in genomics, epigenetics and evo-devo increased the credibility of saltational hypotheses. For example, Masel and Siegal (2009) gave hopeful monsters a new chance to survive. Their reasoning is based on new evolutionary concepts such as developmental robustness and evolvability of living systems (including evolutionary capacitance, genetic assimilation sensu Waddington, 1953). Masel and Siegal (2009) wrote: ‘Evolutionary capacitance, whether evolved or intrinsic, reopens the idea, introduced by Richard Goldschmidt, of “hopeful monsters” in evolution…A single capacitor mutation could have a large effect by phenotypically revealing a large number of pre-existing variants, each of small effect…Large-effect mutations that participate in adaptation might simply arise in genes encoding capacitors that normally provide robustness to many small-effect mutations at other sites.’ Thus, hopeful monsters and saltational evolution get a revival as valuable biological concepts. Far from being mutually exclusive scenarios, both gradualism and saltationism are required to explain the complexity and diversity of life on Earth (Theissen, 2006, 2009; Minelli, 2015a).

Bladderworts and river-weeds provide nice examples of hopeful monsters that are ‘here to stay’ (Theissen, 2009). For example, saltational evolution may have amplified the morphological diversity in Podostemaceae – Tristichoideae (Figs 2–5), especially in the Dalzellia–Indotristicha lineage, with Indodalzellia as their sister genus (Koi et al., 2012; Fujinami and Imaichi, 2015).

Floral vs. vegetative bauplans in angiosperms

In both eudicot families, Lentibulariaceae and Podostemaceae, floral and vegetative bauplans can be distinguished. Their floral bauplans appear to be rather stable (robust), reflecting their affiliation with euasterids (order Lamiales) and eurosids (order Malpighiales), respectively. When these two families are labelled as morphological misfits, it is due to their loss of important characters of the CRS bauplan as typical for most angiosperms (Rutishauser and Isler, 2001; Rutishauser et al., 2008). Loss of the CRS bauplan does not mean that the vegetative bodies of bladderworts and river-weeds tend to be chaotic. They just took over new rules of forms, i.e. new patterns of body syntax (Minelli, 2015c), leading to new vegetative bauplans that are specific for the various subgroups of, for example, Utricularia (Figs 9 and 10G).

Molecular genetic work will soon provide deeper insight into the developmental switches responsible for the (partial) loss of the CRS bauplan in bladderworts and river-weeds, as compared with more typical seed plants. Understanding what developmental patterns are followed in morphological misfits is a necessary prerequisite to discover the developmental genetic alterations that led to the establishment of these odd angiosperms having unusual morphologies.

I dedicate this paper to the biophilosophers Agnes Arber (1879–1960) and Rolf Sattler (still alive) who strongly influenced my way of biological thinking. For me as a ‘fuzzy’ plant morphologist it is satisfying to realize that many ideas on developmental and structural continua in vascular plants (Arber, 1950; Sattler, 1986, 1994, 1996; Rutishauser and Isler, 2001) are confirmed now by evolutionary developmental geneticists. I thank Rainer Melzer and Günter Theissen for having invited me to prepare this paper. The valuable comments of Rolf Sattler (Kingston, Ontario) and two anonymous referees are gratefully acknowledged. Lubomir Adamec (Trebon, Czech Republic) is acknowledged for having kept me aware of new publications on carnivorous plants. The technical assistance (microtome sectioning, scanning electron microscopy) of E. Pfeifer and U. Jauch (University of Zurich) is acknowledged.