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k k k k Phenotypic Variation through Ontogeny: Ceratophryid Frogs as a Model how shifts in developmental patterns have led to a novel way of life for both larval and adult Lepidobatrachus spp
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Abstract
The South American frogs of the family Cer-atophryidae (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 Lepidoba-trachus 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 artic-ulation) in a manner unseen in other anurans. Both the larvae and the frog are similarly able to capture large prey underwater.
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The peripheral nervous system of anuran larvae has traditionally been assumed to be largely invariant. Here, we describe the organization of cranial, spinal, and lateral line nerves at different larval stages of Lepidobatrachus spp. based on whole mounts. This is the first detailed description of cranial, spinal, and lateral lines innervation at premetamorphic stages of anuran larvae with notes on temporal variation. We distinguish three sources of morphological variation with respect to other anuran larvae: (a) the loss or reduction of some exclusively larval elements (i.e., the absence of the middle lateral line nerve); (b) spatial changes in the lateral line system (i.e., the supralabial arrangement of component of the anteroventral lateral line nerve); and (c) temporal changes in the disappearance of most of the lateral line system and in the premetamorphic repatterning of the spatial relationships of mandibularis ramus of the trigeminal (V) and hyomandibularis ramus of facial (VII). The innervation of limbs is achieved during late larval stages. Furthermore, comparisons among selected anurans reveal differences in tadpole brain morphology. The spatial and temporal variation found in the peripheral nerves of Lepidobatrachus larvae testifies to previously unappreciated variation in anuran larval morphology.
The aquatic-to-terrestrial shift in the life cycle of most anurans suggests that the differences between the larval and adult morphology of the nose are required for sensory function in two media with different physical characteristics. However, a better controlled test of specialization to medium is to compare adult stages of terrestrial frogs with those that remain fully aquatic as adults. The Ceratophryidae is a monophyletic group of neotropical frogs whose diversification from a common terrestrial ancestor gave rise to both terrestrial (Ceratophrys, Chacophrys) and aquatic (Lepidobatrachus) adults. So, ceratophryids represent an excellent model to analyze the morphology and possible changes related to a secondary aquatic life. We describe the histomorphology of the nose during the ontogeny of the Ceratophryidae, paying particular attention to the condition in adult stages of the recessus olfactorius (a small area of olfactory epithelium that appears to be used for aquatic olfaction) and the eminentia olfactoria (a raised ridge on the floor of the principal cavity correlated with terrestrial olfaction). The species examined (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, and L. llanensis) share a common larval olfactory organ composed by the principal cavity, the vomeronasal organ and the lateral appendix. At postmetamorphic stages, ceratophryids present a common morphology of the nose with the principal, middle, and inferior cavities with characteristics similar to other neobatrachians at the end of metamorphosis. However, in advanced adult stages, Lepidobatrachus laevis presents a recessus olfactorius with a heightened (peramorphic) development and a rudimentary (paedomorphic) eminentia olfactoria. Thus, the adult nose in Lepidobatrachus laevis arises from a common developmental ‘terrestrial’ pathway up to postmetamorphic stages, when its ontogeny leads to a distinctive morphology related to the evolutionarily derived, secondarily aquatic life of adults of this lineage.
Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed. Here we generate testable predictions for coupling versus uncoupling of phenotypic evolution of tadpole and adult life-history phases, and for the underlying expression of genes related to morphological feature formation. We test these predictions by combining evidence from gene expression in two distantly related frogs, Xenopus laevis and Mantidactylus betsi-leanus, with patterns of morphological evolution in the entire radiation of Madagascan mantellid frogs. Genes linked to morphological structure formation are expressed in a highly phase-specific pattern, suggesting uncoupling of phenotypic evolution across life-history phases. This gene expression pattern agrees with uncoupled rates of trait evolution among life-history phases in the mantellids, which we show to have undergone an adaptive radiation. Our results validate a prevalence of uncoupling in the evolution of tadpole and adult phenotypes of frogs.
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.
The anuran lower jaw is composed of three pairs of bones: dentaries, angulosplenials and mentomeckelians. Although the lower jaw is toothless, except in Gastrotheca guentheri, enlarged fangs or odontoids have evolved at least four times independently in some myobatrachids, hylids, ranids and leptodactylids through both parallel and convergent evolutionary events. Fangs seem to represent the single best design solution to enable an anuran to inflict a bite-like wound, but the biological role of biting varies among species. Fangs are projections of the dentaries in ranids, but in the hylid frog Hemiphractus and in ceratophryine leptodactylids, they form a sinosteotic unit with the dentaries and mentomeckelians. Comparisons of morphology, behaviour and diet among frog taxa with enlarged fangs reveal that the fangs may be the result of either sexual or natural selection. Those fangs that evolved in response to sexual selection seem to be relatively larger than those that resulted of natural selection.
The larval morphology and captive breeding of Lepidobatrachus laevis (Leptodactylidae, Ceratophryinae) from the Paraguayan Chaco is described. The larvae are obligate carnivores that swallow large, living prey whole. The larva has a large dorsoventrally flattened head with a beakless wide mouth. By means of buccal suction they can ingest tadpoles that are nearly equal to themselves in size. The chondrocranial cartilages are simple in comparison to microphagous larvae, and the chondrocranium is wider than long. Larval development is rapid, and some tadpoles reach metamorphosis in 20 d. The brachial chambers are like those of Type IV (Orton, 1953) larvae, but the paired branchial openings are lateral and different from the spiracles of other anuran larvae. The branchial chambers show asymmetrical development with the opercular fold closing the right branchial opening prior to the formation of the left branchial opening. The right branchial chamber reopens and the fully developed larva has two large symmetrical branchial openings. The digestive tract is adult-like and the stomach has a large fundic portion that distends to accept the large prey, a typical muscular pyloric region and sphincter, and a short intestine less than 2× the SVL of the larva. In many of its characteristics the larva of Lepidobatrachus resembles the adult.
The horned frog family, Ceratophryidae, currently comprises three genera and 12 extant species, distributed from the Caribbean lowlands to the Pampean grasslands. Horned frogs are fossorial species that are remarkable in terms of their adult and larval morphology,
karyotype, behavior, and other aspects of their biology. In this paper we present a molecular phylogenetic analysis with the goals of: (1) exploring the relationships among the species of Ceratophryidae; (2) studying the evolution of polyploidy; (3) studying the evolution of cocoon
formation and larval development duration associated with surviving in semiarid environments; and (4) reviewing the ceratophryid fossil record that could be relevant as calibration points in molecular divergence estimations. The analysis included 11 of the 12 extant species and,
when possible, multiple exemplars per species, as well as multiple outgroups. Sequence data were obtained on seven mitochondrial and six nuclear genes for up to 8200 bp per specimen. Our results indicate that the individual monophyly of Ceratophrys and Lepidobatrachus is well
corroborated. The monotypic Chacophrys is recovered as the sister taxon of Lepidobatrachus, but with Jackknife frequency < 50%. Lepidobatrachus asper is the sister taxon of L. laevis + L. llanensis. Relationships within Ceratophrys are congruent with an earlier proposal, with a clade
composed of the species possessing a dorsal bony shield (Ce. aurita, Ce. cranwelli, Ce. joazeirensis, and Ce. ornata), and another clade composed of Ce. stolzmanni, Ce. calcarata, and Ce. cornuta. Unlike earlier proposals, the octoploid species (Ce. aurita, Ce. joazeirensis, and Ce. ornata) are not monophyletic, as the diploid Ce. cranwelli, and Ce. ornata are sister taxa. This result implies an ambiguous optimization of ploidy levels, with either a single origin of octoploidy with a subsequent reversal to diploidy, or two independent origins of octoploidy being equally parsimonious; both alternatives are quite unusual from the perspective of chromosome evolution. Our results suggest that ceratophryids diversified in semiarid environments and three independent events resulted in three species subsequently occupying temperate or tropical humid areas. This early diversification in semiarid areas explains the retention of characteristics associated with these environments (like the production of a cocoon of dead skin during estivation, and possibly an accelerated larval period and development) in species present in humid areas. A revision of the fossil record of this family of frogs indicates that there are only two fossil remains that could serve as calibration
points for molecular clock estimation, but a number of issues associated with them preclude their use.
The role of thyroid hormone (TH) in anuran metamorphosis has been documented from a variety of
approaches, but the sequence of morpho-histological development of the thyroid glands that produce the secretion of the hormone was assumed invariant from studies of relatively few species even when the effects of environmental influences on larval development and metamorphosis have been largely documented. There are anurans in which developmental and growth rates diverge, and the resulting heterochrony in growth and development produces giant/miniature tadpoles, and or rapid/delayed metamorphosis suggesting changes of the activity of the thyroid glands during larval development. Herein, we analyze the morpho-histological variation of the thyroid glands in larval series of Ceratophrys cranwelli, Chacophrys
pierottii, Lepidobatrachus laevis and L. llanensis that share breeding sites along semiarid environments of
the Chaco in South America, belong to a monophyletic lineage, and present accelerated patterns in growth and development in order to have a morphological evidence about a possible shift of TH physiology. We describe gross morphology and histology of the thyroid glands and find features shared by all studied species such as the presence of supernumerary heterotopic follicles; changes in the volume and number of follicles towards the metamorphic climax, and cuboidal epithelia with occasional intra-cellular vacuoles as signs of low glandular activity without a manifest peak at the climax as it was assumed for anurans. We discuss different lines of evidence to interpret sources of extra supplement of TH to support the rapid
metamorphosis. These interpretations highlight the necessity to design a research program to investigate the endocrine variation during development of ceratophryids taking in account their morphology, physiology and ecology in order to learn more about the effects of environmental and developmental interactions involved in the anuran evolution.
We report the emission of underwater sounds in the tadpoles of a second member of the family Ceratophryidae, Ceratophrys cranwelli. These tadpoles produce a short metallic-like sound, which consists of short trains of pulses at Gosner stages 25, 28, and 37. Experiment I was designed to record underwater sounds and their characteristics. Experiment II was designed to test: (i) if at higher densities (total number of tadpoles/L) but fixed predator–prey proportions C. cranwelli larvae are cannibalistic, (ii) if cannibalism increases at higher proportions of predators at a fixed density, and (iii) if tadpoles display a mechanism of intraspecific recognition that may diminish the frequency of cannibalism. Each treatment combines larvae of C. cranwelli (predator) with those of Rhinella arenarum (prey). The number of live and dead individuals was recorded during 72 h, and the following variables were calculated: time to eat the first and second prey, time without eating, time to eat a congener, and number of events of cannibalism. The results indicate that relative predator–prey availability affects the frequency of predation between conspecifics. We consider that an antipredator mechanism exists in C. cranwelli tadpoles and that the underwater sound is part of it.
Heterochrony refers to those permutations in timing of differentiation events, and those changes in rates of growth and development
through which morphological changes and novelties originate during phyletic evolution. This research analyzes morphological
variation during the ontogeny of 18 different anuran species that inhabit semi-arid environments of the Chaco in South America.
I use field data, collection samples, and anatomical methods to compare larval growth, and sequences of ontogenetic events.
Most species present a similar pattern of larval development, with a size at metamorphosis related to the duration of larval
period, and disappearance and transformations of larval features that occur in a short period between forelimb emergence and
tail loss. Among these 18 species, Pseudis
paradoxa has giant tadpole and long larval development that are the results of deviations of rates of growth. In this species events
of differentiation that usually occur at postmetamorphic stages have an offset when tail is still present. Tadpoles of Lepidobatrachus spp. reach large sizes at metamorphosis by accelerate developmental rates and exhibit an early onset of metamorphic features.
The uniqueness of the ontogeny of Lepidobatrachus indicates that evolution of anuran larval development may occasionally involve mid-metamorphic morphologies conserving a
free feeding tadpole and reduction of the morphological-ecological differences between tadpoles and adults.
There is widespread recognition of a recent coming together of developmental and evolutionary biology in the study of problems of mutual interest. Contemporary studies into the development and evolution of the head largely comprise two parallel approaches, or research strategies the model systems approach and the comparative approach. The two strategies share the same general goal-greater understanding of cranial development and evolution-but typically emphasize different problems, ask different questions, and employ different methods, reflecting the contrasting backgrounds and biases of each group of investigators, there has been relatively little true synthesis. Each strategy is making important and valid contributions, but both have limitations. Resolution of many fundamental and long-standing problems in cranial development and evolution will require a combined approach that incorporates the technical and conceptual strengths of each discipline.
Istock (1967) argued on theoretical grounds that "complex life cycles are inherently unstable over evolutionary time," yet the vast majority of frogs have distinct adult and larval forms. The maintenance of complex life cycles in anurans seems related to the unusual morphology and feeding ecology of the larval stage.An argument is presented that tadpoles are highly specialized suspension feeders adapted for utilizing rapid rises in primary production as a food source. Such resources are likely coupled to environmental fluctuations and available for only a limited amount of time during any year. In being adapted to feed on a temporary resource, tadpoles are obliged to change their feeding habits after a certain length of time. From a general consideration of matters such as predator susceptibility, feeding behavior, and growth patterns for suspension feeders, a case is made for why neotenic tadpoles have never been found and are unlikely to occur.The argument presented here links complex life cycles with short term environmental perturbation. Frog species with direct development tend to occur in relatively aseasonal environments, supporting this conclusion. The oldest known fossil frog is found in a seasonal rock formation. There has been a gradual trend toward increased seasonality since the early Mesozoic, apparently due to continental drift. This phenomenon may have some indirect and long-term bearing on the general maintenance of complex life cycles throughevolutionary time.Understanding larval ecology is fundamental to understanding the process of metamorphosis and the maintenance of complex life cycles.
En este trabajo se presenta una descripción detallada de la morfología de la larva del escuerzo Chacophrys pierottii. La descripción incluye una revisión de la morfología externa, el patrón de distribución de los órganos del sistema de la línea lateral y comentarios de la biología larval. Se describe la variación en el apén-dice nasal de la larva de Chacophrys, una característica única entre los anuros. Se realizan comparaciones con larvas de dos géneros relacionados, Ceratophrys y Lepidobatrachus. La larva de Chacophrys pierottii exhibe caracteres típicos de la mayoría de los re-nacuajos de aguas quietas de Tipo IV, sin las modificaciones que presentan las larvas especializadas de Ceratophrys y Lepidobatrachus aunque comparte con ellos la presencia de papilas marginales continuas en el disco oral.
Anurans (frogs and toads) are unique among land vertebrates in possessing a free-living larval stage that, parallel to adult frogs, diversified into an impressive range of ecomorphs. The tempo and mode at which tadpole morphology evolved through anuran history as well as its relationship to lineage diversification remain elusive. We used a molecular phylogenetic framework to examine patterns of morphological evolution in tadpoles in light of observed episodes of accelerated lineage diversification. Our reconstructions show that the expansion of tadpole morphospace during the basal anuran radiation in the Triassic/Early Jurassic was unparalleled by the basal neobatrachian radiation in the Late Jurassic/Early Cretaceous or any subsequent radiation in the Late Cretaceous/Early Tertiary. Comparative analyses of radiation episodes indicate that the slowdown of morphospace expansion was caused not only by a drop in evolutionary rate after the basal anuran radiation but also by an overall increase in homoplasy in the characters that did evolve during later radiations. The overlapping sets of evolving characters among more recent radiations may have enhanced tadpole diversity by creating unique combinations of homoplastic traits, but the lack of innovative character changes prevented the exploration of fundamental regions in morphospace. These complex patterns transcend the four traditionally recognized tadpole morphotypes and apply to most tissue types and body parts.
What determines the direction of evolutionary change? This book provides a revolutionary answer to this question. Many biologists, from Darwin's day to our own, have been satisfied with the answer 'natural selection'. Professor Wallace Arthur is not. He takes the controversial view that biases in the ways that embryos can be altered are just as important as natural selection in determining the directions that evolution has taken, including the one that led to the origin of humans. This argument forms the core of the book. However, in addition, the book summarizes other important issues relating to how embryonic (and post-embryonic) development evolves. Written in an easy, conversational style, this is the first book for students and the general reader that provides an account of the exciting new field of Evolutionary Developmental Biology ('Evo-Devo' to its proponents).
The Chaco is one the most neglected and least studied regions of the world. This highly-seasonal semiarid biome is an extensive continuous plain without any geographic barrier, and in spite of its high species diversity, the events and processes responsible have never been assessed. Miocene marine introgressions and Pleistocene glaciations have been mentioned as putative drivers of diversification for some groups of vertebrates in adjacent biomes of southern South America. Here we used multilocus data (one mitochondrial and six nuclear loci) from the three species of the endemic frog genus Lepidobatrachus (Lepidobatrachus asper, Lepidobatrachus laevis, and Lepidobatrachus llanensis) to determine if any of the historical events suggested as drivers of vertebrate diversification in southern South America are related to the diversification of the genus and if the Chaco is indeed a biome without barriers. Using fossil calibration in a coalescent framework we estimated that the genus diversified in the second half of the Miocene, coinciding with marine introgressions. Genetic patterns and historical demography suggest an important role of old archs and cratons as refuges during floods. In one species of the genus, L. llanensis, genetic structure reveals some breaks along the landscape, the main one of which corresponds to an area of the central Chaco that may act as a climatic barrier. Additionally, we found differential effects of the main Chacoan rivers on species of Lepidobatrachus that could be related to the time of persistence of populations in the areas influenced by these rivers.
I examined the evolutionary factors maintaining two environmentally induced morphs in ponds of variable duration. Larvae of New Mexico spadefoot toads (Scaphiopus multiplicatus) often occur in the same pond as a large, rapidly developing carnivorous morph and as a smaller, more slowly developing omnivorous morph. Previous studies revealed that carnivores can be induced by feeding tadpoles live fairy shrimp and that morph determination is reversible. Field and laboratory experiments indicated that the ability of an individual to become a carnivore or an omnivore is maintained evolutionarily as a response to variability in pond longevity and food abundance. Carnivores survived better in highly ephemeral artificial ponds, because they developed faster. Omnivores survived better in longer-duration artificial ponds, because their larger fat reserves enhanced postmetamorphic survival. The two morphs also occupy different trophic niches. Experimental manipulations of morph frequency in ponds of intermediate duration revealed that increased competition for food among individuals of the more common morph made the rarer form more successful. Morph frequency within each pond was stabilized at an equilibrium by frequency-dependent morph reversal, which reflected frequency-dependent natural selection on size at metamorphosis: larger metamorphs had higher survival, and individuals reared at a frequency above the pond's equilibrium frequency were smaller at metamorphosis than were individuals of that morph reared at a frequency below the pond's equilibrium. Because neighboring ponds often differed in pond longevity and food abundance, each pond possessed a unique equilibrium morph frequency. This implies that morph determination in Scaphiopus is a locally adjusted evolutionarily stable strategy (ESS).
The large size and rapid development of amphibian embryos has facilitated ground-breaking discoveries in developmental biology. Here, we describe the embryogenesis of the Budgett's frog (Lepidobatrachus laevis), an unusual species with eggs that are over twice the diameter of laboratory Xenopus, and embryos that can tolerate higher temperatures to develop into a tadpole four times more rapidly. In addition to detailing their early development, we demonstrate that, like Xenopus, these embryos are amenable to explant culture assays and can express exogenous transcripts in a tissue-specific manner. Moreover, the steep developmental trajectory and large scale of Lepidobatrachus make it exceptionally well-suited for morphogenesis research. For example, the developing organs of the Budgett's frog are massive compared to those of most model species, and are composed of larger individual cells, thereby affording increased subcellular resolution of early vertebrate organogenesis. Furthermore, we found that complete limb regeneration, which typically requires months to achieve in most vertebrate models, occurs in a matter of days in the Budgett's tadpole, which substantially accelerates the pace of experimentation. Thus, the unusual combination of the greater size and speed of the Budgett's frog model provides inimitable advantages for developmental studies-and a novel inroad to address the mechanisms of spatiotemporal scaling during evolution.
Copyright © 2015 Elsevier Inc. All rights reserved.
Anuran larvae have been classified into four morphological types which reflect intraordinal macroevolution. At present, complete characterizations of the lateral line system are only available for Xenopus laevis (Type I) and Discoglossus pictus (Type III). We analyzed the morphology, arrangement, and innervation of neuromasts related to the anterodorsal and anteroventral lateral line nerves in 10 anuran species representing Types I, II, and IV with the aim of interpreting the existing variation and discussing the evolution of the lateral line in anuran larvae. We found: (1) the presence of two orbital and three mandibular neuromast lines in all anuran larvae studied, (2) the ventral arrangement of mandibular neuromast lines appears to have evolved convergently in Larval Types I and II, and the lateroventral arrangement of mandibular lines of neuromasts appears to have evolved in Larval Types III and IV; (3) interspecific variation in the organization, size, and number of sensory cells per neuromast within the lines; and (4) the supralabial extension of the Angular line in Lepidobatrachus spp. and the tentacular location of the Oral neuromasts in X. laevis are concomitant with their particular morphologies. Based on the variation described we find that the lateral line system in anuran larvae seems to have been maintained without significant changes, with the exception of Lepidobatrachus spp. and Xenopus. These unique features added to other of Lepidobatrachus tadpoles are sufficient to propose a new Larval Type (V). Anat Rec, 2014. © 2014 Wiley Periodicals, Inc.
Phenotypic variation is a prerequisite for evolution by natural selection, yet the processes that give rise to the novel morphologies upon which selection acts are poorly understood. We employed a chemical genetic screen to identify developmental changes capable of generating ecologically relevant morphological variation as observed among extant species. Specifically, we assayed for exogenously applied small molecules capable of transforming the ancestral larval foregut of the herbivorous Xenopus laevis to resemble the derived larval foregut of the carnivorous Lepidobatrachus laevis. Appropriately, the small molecules that demonstrate this capacity modulate conserved morphogenetic pathways involved in gut development, including downregulation of retinoic acid (RA) signaling. Identical manipulation of RA signaling in a species that is more closely related to Lepidobatrachus, Ceratophrys cranwelli, yielded even more similar transformations, corroborating the relevance of RA signaling variation in interspecific morphological change. Finally, we were able to recover the ancestral gut phenotype in Lepidobatrachus by performing a reverse chemical manipulation to upregulate RA signaling, providing strong evidence that modifications to this specific pathway promoted the emergence of a lineage-specific phenotypic novelty. Interestingly, our screen also revealed pathways that have not yet been implicated in early gut morphogenesis, such as thyroid hormone signaling. In general, the chemical genetic screen may be a valuable tool for identifying developmental mechanisms that underlie ecologically and evolutionarily relevant phenotypic variation.
Tadpoles of spadefoot toads are polymorphic in nature; juveniles that feed on detritus develop into herbivorous omnivores, while those that feed on fairy shrimp sometimes become carnivores that are cannibalistic. Three experiments studied the kin recognition abilities of both larval morphotypes. In laboratory tests, omnivores preferentially associated with siblings, while carnivores from the same clutch preferentially associated with nonsiblings. In follow-up studies, carnivorous tadpoles were observed to nip at conspecifics and then either eat them if they were nonsiblings or release them unharmed if they were siblings. Carnivores became less selective when hungry, demonstrating that their level of kin discrimination was context-dependent. Three evolutionary hypotheses for avoidance of siblings by the carnivore morph are considered. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Ceratophryidae represent a monophyletic group of terrestrial and aquatic frogs inhabiting lowlands of South America where they are more diverse in semiarid environments of the Chaco region. Adult morphology of ceratophryids presents some features associated to terrestrial and fossorial life such as hyper-ossified skulls, spade feet for digging, among others. For anurans, different mineralized structures have been described in the integument as calcium reservoirs and related to the terrestrial life and water balance (e.g., the calcified layer and dermal ossifications). We describe the ontogeny of the integument in the three genera of ceratophryids (Chacophrys, Ceratophrys, and Lepidobatrachus) that inhabit in semiarid environments. Data obtained demonstrated the early acquisition of metamorphic transformations in the integument layers in larvae of Ceratophrys cranwelli and Lepidobatrachus spp. and a continuous increment in the thickness of them up to old postmetamorphic stages. The integument of ceratophryids develops calcium deposits as the calcified layer during postmetamorphic stages. Furthermore, dorsal shields are also present in adult stages independently of terrestrial versus aquatic lifestyles. While the calcified layer seems to be a feature of a fully developed integument, in which their layers have acquired the adult thickness, dorsal shields develop at premetamorphic stages in L. llanensis and postmetamorphic individuals of C. cranwelli. In ceratophryids, similar to other studied taxa (e.g., Brachycephalus spp.) dorsal shields develop via an intramembranous ossification in which the calcified layer does not precede its differentiation. Within anurans, the occurrence of dorsal shields in the monophyletic ceratophryids suggested a distinctive evolutionary history in the lineage. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.
Body form is one of the major consequences of development, and diversification of body shapes implies developmental changes among species. In anurans, changes in the timing of developmental events or heterochrony, have been emphasized as a source of variation in the patterns of development that has lead to diverse morphology. Herein, different approaches are used to explore morphological traits in members of the Ceratophryinae (Anura: Leptodactylidae), a group of frogs with some features produced by overdevelopment. Cladistic analyses were conducted in order to distinguish the shared history of Ceratophrys, Chacophrys and Lepidobatrachus and other anurans. From these studies, morphological variation of selected skeletal features in ceratophryines reveals the presence of ancient structures, which have been considered lost in the neobatrachian phylogeny, integrated in particular designs. Thin-plate spline morphometric analyses of skull shapes among ceratophryines describe Lepidobatrachus as the most distinctive shape. Moreover, thin-plate spline morphometric analyses among anurans show divergent skull shapes between ceratophryines and other anurans, reflecting that the skull shapes of ceratophryines are a result of peramorphosis (increase of developmental rates). This study represents the first detailed examination of the role of peramorphosis in a clade of anurans.
Heterochrony produces morphological change with effects in shape, size, and/or timing of developmental events of a trait related to an ancestral ontogeny. This paper analyzes heterochrony during the ontogeny of Ceratophryinae (Ceratophrys, Chacophrys, and Lepidobatrachus), a monophyletic group of South American frogs with larval development, and uses different approaches to explore their morphological evolution: (1) inferences of ancestral ontogenies and heterochronic variation from a cladistic analysis based on 102 morphological larval and adult characters recorded in ten anuran taxa; (2) comparisons of size, morphological variation, and timing (age) of developmental events based on a study of ontogenetic series of ceratophryines, Telmatobius atacamensis, and Pseudis platensis. We found Chacophrys as the basal taxon. Ceratophrys and Lepidobatrachus share most derived larval features resulting from heterochrony. Ceratophryines share high rates of larval development, but differ in rates of postmetamorphic growth. The ontogeny of Lepidobatrachus exhibits peramorphic traits produced by the early onset of metamorphic transformations that are integrated in an unusual larval morphology. This study represents an integrative examination of shape, size, and age variation, and discusses evolutionary patterns of metamorphosis. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 752–780.
Organisms exhibit an incredible diversity of form, a fact that makes the evolution of novelty seemingly self-evident. However, despite the "obvious" case for novelty, defining this concept in evolutionary terms is highly problematic, so much so that some have suggested discarding it altogether. Approaches to this problem tend to take either an adaptation- or development-based perspective, but we argue here that an exclusive focus on either of these misses the original intent of the novelty concept and undermines its practical utility. We propose instead that for a feature to be novel, it must have evolved both by a transition between adaptive peaks on the fitness landscape and that this transition must have overcome a previous developmental constraint. This definition focuses novelty on the explanation of apparently difficult or low-probability evolutionary transitions and highlights how the integration of developmental and functional considerations are necessary to evolutionary explanation. It further reinforces that novelty is a central concern not just of evolutionary developmental biology (i.e., "evo-devo") but of evolutionary biology more generally. We explore this definition of novelty in light of four examples that range from the obvious to subtle.
Many traits of the skull of ceratophryines are related to the capture of large prey independently of aquatic or terrestrial feeding. Herein, detailed descriptions of the development of hyoid skeleton and the anatomy of muscles responsible for hyoid and tongue movements in Lepidobatrachus laevis and L. llanensis are provided and compared with those of other neobatrachians. The aquatic Lepidobatrachus has special features in its hyoid skeleton that integrates a set of derived features convergent with the conditions observed in non-neobatrachian anurans and morphological novelties (e.g., dorsal dermal hyoid ossification) that deviate from the generalized pattern found in most frogs. Further, reduction of fibers of muscles of buccal floor, reduction or loss of hyoid muscles (m. geniohyoideus rama lateralis, anterior pair of m. petrohyoideus posteriores), small tongue, and simplified tongue muscles are also morphological deviations from the pattern of terrestrial ceratophryines, and other aquatic ceratophryids (e.g., Telmatobius) that seem to be related to feeding underwater. The historical derived features shared with Chacophrys and Ceratophrys involved in megalophagy are conserved in Lepidobatrachus and morphological changes in the hyoglossal apparatus define a unique functional complex among anurans.
This study analyzes the structure of the mandibular arch musculature in larval, metamorphic, and postmetamorphic anurans of 26 species and makes comparisons with larvae of three caudate and one gymnophione species. Major transformations in early evolution of anuran larvae comprise, for example, the powering of the larval upper jaw cartilages by relocating insertion sites of mandibular arch levators; splitting of some larval muscles into two muscles or muscle heads (m. intermandibularis, m. lev. mand. externus, m. lev. mand. longus); evolution of a muscle invading the lower lip of the oral disk (m. mandibulolabialis), and shift of origin of the internus and longus muscles from dorsal on the cranium to sites on the ventral otic capsule and palatoquadrate, respectively. In all these characters, Ascaphus truei shares the plesiomorphic conditions with caudates. The larva of Xenopus laevis is remarkable because the insertion pattern of three larval mandibular muscles anticipates the postmetamorphic condition of frogs in general and also resembles the caudate condition. Discoglossids, bombinatorids, pelobatids, and neobatrachians are largely similar in their muscle arrangements. The filter-feeding microhylids, however, have most clearly modified the general neobatrachian pattern. Past conflicts in the interpretation and naming of muscles can be attributed to the implicit or explicit homology assumptions used. In particular, the muscles' relations to the branches of the trigeminal nerve have been the dominant criteria for inferring homology and has led to inconsistencies. This concept is questioned herein. It is observed that the relative position of the ramus mandibularis (V(3)) is more variable interspecifically in anuran larvae than previously thought. The relations of the nerve branches and muscles in larvae are maintained during metamorphosis. Considering the muscle pattern to be more conserved in interspecific comparisons than the position of the nerve branches results in a new interpretation of muscle homologies and a hypothesis of jaw muscle evolution in amphibians that is more parsimonious than earlier views. A new, simplified terminology for the jaw musculature is proposed that is applicable for larvae and adults. It maximizes information content and reflects the hypothesized homologies of amphibian jaw muscles.
Cooption and modularity are informative concepts in evolutionary developmental biology. Genes function within complex networks that act as modules in development. These modules can then be coopted in various functional and evolutionary contexts. Hormonal signaling, the main focus of this review, has a modular character. By regulating the activities of genes, proteins and other cellular molecules, a hormonal signal can have major effects on physiological and ontogenetic processes within and across tissues over a wide spatial and temporal scale. Because of this property, we argue that hormones are frequently involved in the coordination of life history transitions (LHTs) and their evolution (LHE). Finally, we promote the usefulness of a comparative, non-model system approach towards understanding how hormones function and guide development and evolution, highlighting thyroid hormone function in echinoids as an example.
Atlas climático digital de la República Argentina
- A R Bianchi
- Sac Cravero
Bianchi AR and Cravero SAC (2010) Atlas climático digital de la
República Argentina. https://inta.gob.ar/sites/default/files/scripttmp-texto_atlas_climtico_digital_de_la_argentina_110610_2
.pdf.
Amphibian Species of the World: an Online Reference
- D R Frost
Frost DR (2018) Amphibian Species of the World: an Online Reference. American Museum of Natural History, New York, USA.
http://research.amnh.org/herpetology/amphibia/index.html.
New material of Beelzebufo, a hyperossified Frog (Amphibia: Anura) from the Late Cretaceous of Madagascar
- S E Evans
- J R Groenke
- Meh Jones
Evans SE, Groenke JR, Jones MEH, et al. (2014) New material
of Beelzebufo, a hyperossified Frog (Amphibia: Anura) from the
Late Cretaceous of Madagascar. PLoS ONE. DOI: 10.1371/journal.pone.0087236.
Cannibalism by large tadpoles of Rhinophrynus dorsalis (Anura: Rhinophrynidae)
- J L Stynoski
- M Sasa
Stynoski JL and Sasa M (2018) Cannibalism by large tadpoles
of Rhinophrynus dorsalis (Anura: Rhinophrynidae). Herpetology
Notes 11: 1047-1049.