Developmental changes and novelties in ceratophryid frogs
© Fabrezi et al. 2016
Received: 4 January 2016
Accepted: 11 February 2016
Published: 27 February 2016
The Neotropical frog genera Ceratophrys, Chacophrys and Lepidobatrachus form the monophyletic family Ceratophryidae. Although in- and out-group relationships are not fully resolved, the monophyly of the three genera is well supported by both morphological and molecular data. Much is known about the morphology of the ceratophryids, but there is little comparative information on how modification of a common ancestral developmental pathway played a role in shaping their particular body plans. Herein, we review morphological variation during ceratophryid ontogeny in order to explore the role of development in their evolution. The ceratophryids are collectively characterized by rapid larval development with respect to other anurans, yet the three genera differ in their postmetamorphic growth rates to sexual maturity. Derived traits in the group can be divided into many homoplastic features that evolved in parallel with those of anurans with fossorial/burrowing behaviors in semiarid environments, and apomorphies. Morphological novelties have evolved in their feeding mechanism, which makes them capable of feeding on exceptional large prey. Lepidobatrachus is unusual in having reduced the ecomorphological differences between its larvae and adults. As a result, both the larvae and the frog are similarly able to capture large prey underwater. Some unique features in Lepidobatrachus are differentiated in the tadpole and then exaggerated in the adult (e.g., the posterior displaced jaw articulation) in a manner unobserved in any other anurans.
KeywordsGrowth Development Morphological novelty Metamorphosis Anurans
Based on morphological and molecular data, the South American anuran genera Chacophrys Reig and Limeses 1963 (one species), Ceratophrys Wied-Neuwied 1824 (eight species) and Lepidobatrachus Budgett 1899 (three species) constitute a monophyletic clade, the Ceratophryidae. Ceratophrys species are distributed in tropical areas with Ceratophrys cranwelli living with Lepidobatrachus spp. and Chacophrys pierottii in the semiarid lowlands of the Chaco region.
The monophyly of the group, often referred to as horned frogs, was proposed by early researchers [1–5] and ratified by more recent cladistic analyses [6–10]. However, two controversies remain regarding the relationships of the group: (1) the relationships between the three genera and (2) the group’s relationship with other anurans.
When the relationship of the Ceratophryidae to other anurans has been examined, the South American horned frogs have been variously proposed as: a basal taxon within Bufonidae ; related to Leptodactylidae [2, 4, 5] or to certain hylids, but with only weak support ; a basal group of Neobatrachia ; the sister group of Odontophrynus ; the sister group of Batrachyilinae ; the sister group of Telmatobiinae ; a sister lineage of a large clade within Hyloides  (Fig. 1b); and even a basal group of Hyloides .
Two Cretaceous fossils have been attributed to the Ceratophryidae and are the oldest fossils associated with the family. These are Beelzebufo ampinga from the Upper Cretaceous (Maastrichtian) Maevarano Formation of Madagascar [13, 14] and Baurubatrachus pricei from the Upper Cretaceous of Brazil . Other more recent fossils have been placed within the Ceratophryidae. Specimen assigned to Wawelia geroldhi, from Miocene sediments of northern Patagonia in Argentina , seems to represent a juvenile anuran with some features like extant ceratophryids. Other late Miocene specimens have been attributed to Ceratophrys [17–20] and Lepidobatrachus [21, 22]. Those specimens, plus independent molecular data [5, 23], indicated that both genera were well differentiated by the Miocene.
Despite much data supporting ceratophryid monophyly, the evolution of these anurans remains enigmatic. Although much is known about their morphology, there is little comparative information on how development played a role in shaping the divergent ceratophryid body plans. What in particular has not been explored is the interplay between pre- and postmetamorphic development. Uninvestigated is how these developmental pathways have influenced each other to arrive at their variously shared and unique features of adult and larval ceratophryids.
Here, we review information on variation among ceratophryid ontogenies to address two interrelated questions: (1) How did modification of development pathways play a role in the differentiation of ceratophryid genera? and (2) How did those developmental pathways contribute to the evolutionary history that distinguishes the ceratophryid from the other hyloid lineages? We provide data to (1) illustrate how development can evolve and (2) present a case study of how the detailed knowledge of morphological variation during development strengthens evolutionary studies.
Developmental and growth rates
From an ontogenetic approach, heterochrony has become a focal concept that integrates many areas of evolutionary biology . Different definitions, however, have been used to explain heterochrony (cf. “Appendix”), and controversies have emerged since heterochronic patterns cannot be unequivocally classified without information of the timing (age) of developmental events in the ancestral and descendant ontogenies .
The importance of growth heterochrony for distinguishing ceratophryids from other anurans was demonstrated in a comparison of the larvae from 20 species (five anuran families) that co-occurred with ceratophryids in the Chaco in South America. Data on size at metamorphosis and duration of the larval period for most non-ceratophryid species in this sample suggested similar growth rates , i.e., with development to metamorphosis taking between 20 and 75 days for 15 of those 20 species and larval body sizes varying between 9 and 25 mm. By comparison tadpoles of Chacophrys pierotii and Lepidobatrachus spp. reach metamorphosis between 15–18 days and Ceratophrys cranwelli in 20–24 days, with body sizes ranging from 25 to 45 mm  (Fig. 4).
Precise data on age at sexual maturity and postmetamorphic growth rates are not available for any ceratophryids in the wild. However, it is possible to infer the age of reproductive adults from wild-caught specimens from lines of arrested growth. Such data suggest that developmental and growth rates after metamorphosis differ greatly among ceratophryids. In Lepidobatrachus spp., sexually mature individuals of 5–6 years are considerably larger than sexually mature C. pierottii of the same age . The ages for mature males of Ce. cranwelli vary between 11 and 14 years old with sizes slightly larger than those of Lepidobatrachus laevis at 6 years .
Morphological evolution related to the postaxial skeleton indicative of homoplasy
In anurans, with the exception of axial musculature that changes with metamorphosis, the appendicular musculoskeletal system develops and grows independently of the larval body plan . This can be understood within the context of modular organization of development [41, 55]. For developing anurans, the postaxial musculoskeletal system is divided into two separate units: (1) the trunk and tail that collectively serve for swimming and (2) the appendicular system that develops to serve adult tetrapod locomotion.
In ceratophryids, there are a few derived features in the postaxial skeleton (Fig. 1b). These include the absence of a crest on the ilium, the presence of a very short muscle iliacus externus [54, 56], a strong prehallical element for digging and the presence of dorsal shields in some species of Ceratophrys and Lepidobatrachus [10, 24, 57].
These postcranial morphological traits of ceratophryids are homoplastic and, as already noted, are commonly associated with terrestrial/fossorial habits and resistance to desiccation in anurans (Fig. 1b). Consistent with that is the fact that Chacophrys and Lepidobatrachus are the only anuran genera solely endemic to the semiarid South American Chaco region . Furthermore, the presence of a cocoon as a mechanism to prevent water loss during estivation, even in Ceratophrys spp. from humid environments, supports the idea that the Ceratophryidae originated and diversified in a semiarid environment comparable to what occurs in the contemporary Chaco .
Morphological evolution related to the visceral arches and feeding indicative of synapomorphies
The analysis of the derived characters in the horned frogs (Fig. 1), both in larvae and adults, and particularly those distinct to Lepidobatrachus, reveals many developmental changes. In Lepidobatrachus, new ontogenetic trajectories are associated with a wealth of anatomical structures associated with the organisms’ pre- and postmetamorphic feeding mechanism. These changes result variously from developmental variation that is recognized as heterochrony, heterometry, heterotopy, and heterotypy or some combination of these developmental processes (Fig. 3; “Appendix”). The occurrence of heterochrony, heterotopy and heterometry may be detected by comparisons between ontogenies and/or adult traits where these processes have consequences in the final shape. For example, heterotopy and heterometry are identified in adult Leptidobatrachus characters in which spatial relationships (e.g., nerves in relation to muscles) are distinct, or morphometric differences appear (e.g., allometry in lower jaw length, ossification of hyoid plate). Heterochrony may occur without morphological consequence in adult traits and requires developmental sequences for interpretations (e.g., sexual maturity). In contrast, heterotypy is observed in unique traits that have their own developmental sequence. Heterotypy, as a developmental phenomenon, is a new ontogenetic trajectory and represents an autapomorphy in a monophyletic lineage.
One of the most remarkable features in horned frogs is the caudal placement of the articulation of the lower jaw up to or beyond the craniovertebral joint (i.e., heterotopy and heterometry). In Lepidobatrachus, the jaw articulation is far behind the craniovertebral joint [7, 50]. This provides them with an enormous gape. Indeed, ceratophryids, and in particular Ceratophrys and Lepidobatrachus, have about the widest mouth openings known in extant anurans.
Skeletal deviations in the ceratophryid hyoid are concomitant with changes in the hyoid musculature implying reduction in the geniohyoideus, omohyoideus and petrohyoidei posteriores muscles  (Fig. 12). All of these features appear to be related to a global reduction in the ceratophryids of the tongue protrusion and retraction mechanism (see additional discussion below) compared with that of more generalized frogs, which feed on smaller and faster moving prey.
Additional developmental changes indicative of autapomorphies, heterotypy and morphological novelties
The concept of morphological novelty (i.e., heterotypy and autapomorphy) refers to new anatomical features that may acquire new functions [47, 48], and two alternative pathways for the origin of such evolutionary novelties have been proposed . One pathway is the emergence of a new adaptive peak that could initially coexist with a preexisting one, which implies a change in role or function for a preexisting structure. The other involves the breaking of a developmental constraint that facilitates structural and functional integration. This would lead to a distinctive, viable and potentially unique morphology. Both processes evidently have occurred in the evolution of the Ceratophyridae and can account for much of their morphological diversity.
The evolutionary shift in the Ceratophryidae toward feeding on such large prey may, in part, account for their high growth rates. The most extreme shift in form and function is seen in Lepidobatrachus. The genus has a number of unique features in the hyoid skeleton, such as discontinuous ceratohyalia and a dermal bone attached to the dorsal face of the cartilaginous corpus of the hyoid that has not been described in other anurans (Fig. 12). There is as well a reduced number of fibers in the buccal floor muscles, and muscles that attach to the hyoid are similarly reduced in L. llanensis and lost in L. laevis (Fig. 12).
Reduction in the tongue increases room on the oral cavity to contain large prey. It is also true that, given the density and viscosity of water, prey capture with a projectile tongue is relatively inefficient. It appears that Lepidobatrachus has evolved a small tongue with simplified musculature as part of distinctive functional complex for aquatic suction feeding . This represents a new adaptive peak (Fig. 13). Notably the unique features related to feeding in Lepidobatrachus are similar in both the larvae and adults; both life stages are exceptional compared with other tadpoles and adults in their ability to subdue and ingest very large, active aquatic prey.
Among ceratophryids, the increased developmental and growth rates affect all major organ systems of their larvae. Arguably, the most remarkable morphological novelties are seen in the visceral arches (e.g., the lower jaw, hyoid and brachial arches), which are essential for feeding in anuran larvae. Many of the derived features of ceratophryid larvae carryover past metamorphosis to the adults and are thus central to the overall morphological evolution of Ceratophryidae.
Anuran metamorphosis is a constrained ontogenetic period regulated mainly by thyroid hormones (THs). Each tissue responds in a selective manner to TH, with varying degrees of sensitivity to the hormones, but in general metamorphic changes are coordinated and fast [87, 88]. Several studies have shown that TH have multiple effects on organisms and evolutionary changes may occur through physiological changes in tissue sensitivity to TH, which are manifest as heterochronic changes during development [89, 90]. Thyroid glands may themselves evolve. The thyroid glands of ceratophryid larvae show signs of low glandular activity without a manifest peak at metamorphic climax as is characteristic of anurans in general . In addition, different sources of TH or TH precursors from the tadpoles’ diet may influence their developmental and growth rates . Many of the heterochronic changes seen in ceratophyrids appear to be due to shifts in both the concentration of TH and TH tissue sensitivity.
Anuran larvae have historically been classified into four morphological types reflecting intraordinal macroevolution [26, 92]. Other authors [36, 37], however, have argued that the Lepidobatrachus tadpole is unique enough to justify labeling it as a separate morphological type. Commonly in anurans, when there has been an evolutionary departure from the classic four intraordinal types, it is by the suppression of the larval stage resulting in anurans with direct development. The ceratophryids represent, in contrast, a case where developmental variation has favored a different departure from larval constraints. This has resulted in Lepidobatrachus having megalophagous tadpoles unlike the larvae of any other anuran genera. The Lepidobatrachus body plan and life style is thus built upon morphological novelties unique among the Anura.
Despite the fact that the extant ceratophryids share numerous synapomorphies, and abundant molecular data have supported their phylogeny, they remain a monophyletic taxon with controversial in- and out-group relationships. In part, this reflects the fact that there are new structures in the Ceratophryidae that have no homology in their ancestors (i.e., autapomorphies, heterotypies or morphological novelties).
The ceratophryid frogs represent an excellent model to elucidate phenotypic variation through ontogeny, and witness the many ways that heterochrony, and the breaking of developmental constraints, can yield ecomorphological novelties. The influence of this ontogenetic variation is most pronounced in the genus Lepidobatrachus. Indeed, because of its large size and rapid development, Lepidobatrachus laevis has recently been proposed as a model species in experimental studies undertaken to address a wealth of classic questions in amphibian embryogenesis . Furthermore, because of its sympatry with several other ceratophyrid species (in the Gran Chaco of South America) and its well established phylogenetic relationship to those species , Lepidobatrachus stands out, not only as model species for studying developmental processes per se, but exceptional for studying the very evolution of those processes.
distal prehallical element
muscle levatorae mandibulae longus
muscle levatorae mandibulae anterior
muscle levatorae mandibulae externus
muscle levatorae mandibulae internus
muscle levatorae mandibulae lateralis
muscle levatorae mandibulae longus profundus
muscle levatorae mandibulae longus superficialis
proximal prehallical element
- V 1 :
ramus ophthalmicus of trigeminus
- V 2 :
ramus maxillaris of trigeminus
- V 3 :
ramus mandibularis of trigeminus
MF conceived, designed and performed this revision and wrote the manuscript. SIQ participated in many studies about the morphological variation among ceratophryids and contributed with interpretation and discussion on patterns of heterochrony and heterometry. She also participated in the design and helped to draft the manuscript. JG contributed with interpretation and discussion on patterns on growth and development in anurans and helped to draft the manuscript. JCC is doctoral student in the laboratory of MF studying developmental variation in thyroid glands in anurans and provided data on ceratophryids. MCP is doctoral student in the laboratory of MF studying developmental variation in postaxial skeleton in anurans and participated in discussion on habitat and lifestyles. RJW contributed with discussion and interpretation of data and wrote the manuscript. All authors read and approved the manuscript.
This work was supported by FONCyT PICT 616 and 510 to MF, FONCyT PICT 2718 to SIQ, CONICET PIP 497 to MF and NSERC Grant to RJW.
The authors declare that they have no competing interests.
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