Phenotypic Variation through Ontogeny: Ceratophryid Frogs as a Model

Abstract

The South American frogs of the family Ceratophryidae (three genera, twelve extant species) display unusual larval diversity and developmental variation despite rather similar adults. Many adult features of ceratophryids are associated with terrestrial/fossorial habits and resistance to desiccation; however, adults of the genus Lepidobatrachus are aquatic. Morphological novelties have evolved in the ceratophryid feeding mechanism that makes them capable of feeding on exceptional large prey (i.e. megalophagy). Lepidobatrachus is unusual in having less ecomorphological differences between its larvae and adults than virtually all other anurans. Some unique features are differentiated in the tadpole and then exaggerated in the adult (e.g., a posterior displaced jaw articulation) in a manner unseen in other anurans. Both the larvae and the frog are similarly able to capture large prey underwater. The article reviews how shifts in developmental patterns have led to a novel way of life for both larval and adult Lepidobatrachus spp.

Key Concepts

  • Derived features of ceratophryid larvae carry over metamorphosis to the adults and are central to the overall morphological evolution of Ceratophryidae.
  • Ceratophryidae shows how evolution can act upon development to produce organisms with novel structures and ecology.
  • Megalophagy is associated with a wealth of other specialisations that are products of shifts in development.
  • The origin of evolutionary novelties in Lepidobatrachus's ontogeny has produced a dramatic and unique larval ecomorphology.
  • Lepidobatrachus has broken metamorphic constraints to achieve common and shared larval and adult adaptations for megalophagy and feeding underwater.

Keywords: evolution; tadpole; metamorphosis; development; megalophagy; anurans

Figure 1. A formalism to represent the morphology (x axis) and ecology (y axis) of the anuran biphasic lifestyle. Larval morphology and ecology occupy the negative quadrant (red polygon). Adult morphology and ecology are in the positive quadrant (blue polygon). Metamorphosis is represented by the region around where the two axes cross. (a). The scheme for two genera of Ceratophryidae (Chacophrys and Ceratophrys) with adults of similar ecomorphology, but with different larvae. The arrows point to where larval and adult ecology and morphology differ. (b). The scheme for Lepidobatrachus spp. illustrates the relatively minor ecomorphological differences between larvae and adults (as shown in a). The fast developmental rate and the precocious metamorphic morphologies of Lepidobatrachus tadpoles have led to a unique larval body plan, with the free‐living Lepidobatrachus spp. larvae similar to the metamorphic larval stages (between forelimb emergence and complete tail loss) of most anurans. Furthermore, in Lepidobatrachus some larval features, such as the lateral line system, are conserved during the whole ontogeny, with adults retaining features normally lost at metamorphosis. Because of the similarity in the lifestyle of the Lepidobatrachus larvae and adults, the typically precarious and brief metamorphic period of other anurans is now protracted. This is represented in the figure by not just the greater overlap in adult and larval polygons, but the convergence of those polygons around where the two axes cross at metamorphosis (Fabrezi et al., ). Source: Fabrezi, https://evodevojournal.biomedcentral.com/articles/10.1186/s13227‐016‐0043‐9. Licensed under CC by 4.0.
Figure 2. The well‐supported monophyly for the family Ceratophryidae and the relationships of the extant species within the family make it possible to see how changes in development have led to morphological diversity in the family (Faivovich et al., ). A common feature in the family is the ability to form a cocoon that prevents water loss during estivation. This trait occurs even in Ceratophrys spp. from humid habitats (C. aurita, C. cornuta and C. ornata) and supports the idea that the Ceratophryidae originated in a semi‐arid environment comparable to what occurs in the contemporary semi‐arid South American Chaco region (Argentina, Bolivia, Paraguay and Brazil). In addition, Chacophrys and Lepidobatrachus are the only anuran genera solely endemic in those environments. Red marks on the map indicate the oldest (Miocene‐Pleistocene) ceratophryid fossils from South America (Faivovich et al., ).
Figure 3. Distinctive traits of ceratophryids frogs. (a) The nasal appendix in Chacophrys tadpole. (b) Tadpole's gut differences in ventral view. Chacophrys (left) with the long and spiralled gut without regional differentiation and a proximal gastroduodenal loop. Lepidobatrachus laevis (right) stomach differentiated, distal gastroduodenal loop (gdl) and short hind gut (hg) with irregular coiling. (c) Dorsal view of L. laevis tadpole. The flat body with two lateral flaps and the large mouth is distinctive. Long lungs are full of air bubbles (arrows). (d) Left, L. laevis very broad head, large gape, reduced tongue mass (1) and fangs (2). Right, L. laevis skull displaying fangs (2), the firm mandibular symphysis, and sharp teeth in the upper jaw (3). (e) Adult features in L. laevis: protruding dorsal eyes (4), small tympanum (5), neuromasts of lateral line system (6), webbed foot (7) and the keratinous ‘spade foot’ used for burrowing (8). (f) Schematic drawing of the buccal floor in ceratophryids showing the tongue mass (1) and the position of glottis (gl). From left to right: C. cranwelli, Chacophrys, L. llanensis and L. laevis. (g) One of the most remarkable features in horned frogs is the caudal placement of the articulation of the lower jaw up. In Lepidobatrachus spp., the jaw articulation is far behind the craniovertebral joint. This provides them with an enormous gape, which makes it possible for them to eat very large prey including conspecifics. Fabrezi and Lobo . Reproduced with permission of John Wiley and Sons.
Figure 4. Plots showing variation in growth rates for Chacoan ceratophryid species indicative of heterochrony. These frogs all reproduce explosively and early in ephemeral pools. Chacophrys and Lepidobatrachus spp. have particularly large and fast growing tadpoles. C. cranwelli also has accelerated growth compared to non‐ceratophryids species. It is possible to infer the age of reproductive adults for wild‐caught specimens from the lines of arrested growth observed in serial sections of metatarsal IV (Fabrezi and Quinzio, ). Such data suggest that growth rates after metamorphosis differ greatly among ceratophryids. In Lepidobatrachus spp., sexually mature individuals of 5–6 years are considerably larger than sexually mature Chacophrys of the same age. Mature males of C. cranwelli vary between 11 and 14 years old with sizes slightly larger than those of L. laevis at 6–7 years. A plausible explanation for higher post‐metamorphic growth rates in Lepidobatrachus could be the fact that they remain in the ponds to feed before the ponds dry up. Sometimes, the large and longer lasting ponds house a rich fauna of tadpoles, other post‐metamorphic frogs, annual fish, snails and other animals. These all can provide food for the voracious Lepidobatrachus. The summarised sequence of larval and metamorphic stages of Lepidobatrachus laevis highlights the distinctiveness of these frogs: tadpoles with a flat head, dorsal eyes, large mouth, external forelimb development. These traits are not found in other anuran clades.
Figure 5. Evolutionary scenario for how changes in ontogeny within the Ceratophryidae lead to morphological novelties and innovation (see also: Evolution: Tempo and Mode; Hallgrímsson et al., ). The bell‐shaped curves are meant to illustrate the distribution of morphology (and new role) at any given time and the dashed lines the ancestor–descendant pathways. Earlier, the evolving linage shares some phenotypic adult traits including some morphological novelties (e.g. lower jaw fangs). The lateral shift in the bell curves reflects the emergence of other morphological novelties (such as a new bony element in the hyoid apparatus) and additional changes (reduced number of fibres in the buccal floor and hyoid muscles, reduced tongue mass) implying a small tongue with simplified musculature as part of the distinctive functional complex for aquatic suction feeding.
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Further Reading

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Fabrezi M and Emerson SB (2003) Parallelism and convergence in anuran fangs. Journal of Zoology 260: 41–51.

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Quinzio SI and Fabrezi M (2012) Ontogenetic and structural variation of mineralizations and ossifications in the integument within ceratophryid frogs (Anura, Ceratophryidae). Anatomical Record 295: 2089–2103.

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Fabrezi, Marissa, Quinzio, Silvia Inés, Goldberg, Javier, Cruz, Julio César, Pereyra, Mariana Chuliver, and Wassersug, Richard Joel(Apr 2019) Phenotypic Variation through Ontogeny: Ceratophryid Frogs as a Model. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028510]