SciCombinator

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Concept: Tetrapod

215

Fossorialism is a beneficial adaptation for brooding, predator avoidance and protection from extreme climate. The abundance of fossilised burrow casts from the Early Triassic of southern Africa is viewed as a behavioural response by many tetrapods to the harsh conditions following the Permo-Triassic mass-extinction event. However, scarcity of vertebrate remains associated with these burrows leaves many ecological questions unanswered. Synchrotron scanning of a lithified burrow cast from the Early Triassic of the Karoo unveiled a unique mixed-species association: an injured temnospondyl amphibian (Broomistega) that sheltered in a burrow occupied by an aestivating therapsid (Thrinaxodon). The discovery of this rare rhinesuchid represents the first occurrence in the fossil record of a temnospondyl in a burrow. The amphibian skeleton shows signs of a crushing trauma with partially healed fractures on several consecutive ribs. The presence of a relatively large intruder in what is interpreted to be a Thrinaxodon burrow implies that the therapsid tolerated the amphibian’s presence. Among possible explanations for such unlikely cohabitation, Thrinaxodon aestivation is most plausible, an interpretation supported by the numerous Thrinaxodon specimens fossilised in curled-up postures. Recent advances in synchrotron imaging have enabled visualization of the contents of burrow casts, thus providing a novel tool to elucidate not only anatomy but also ecology and biology of ancient tetrapods.

Concepts: Evolution, Tetrapod, Synapsid, Paleontology, Frog, Dinosaur, Triassic

206

Amphibians, a class of animals in global decline, are present in agricultural landscapes characterized by agrochemical inputs. Effects of pesticides on terrestrial life stages of amphibians such as juvenile and adult frogs, toads and newts are little understood and a specific risk assessment for pesticide exposure, mandatory for other vertebrate groups, is currently not conducted. We studied the effects of seven pesticide products on juvenile European common frogs (Rana temporaria) in an agricultural overspray scenario. Mortality ranged from 100% after one hour to 40% after seven days at the recommended label rate of currently registered products. The demonstrated toxicity is alarming and a large-scale negative effect of terrestrial pesticide exposure on amphibian populations seems likely. Terrestrial pesticide exposure might be underestimated as a driver of their decline calling for more attention in conservation efforts and the risk assessment procedures in place do not protect this vanishing animal group.

Concepts: Species, Animal, Pesticide, Tetrapod, Risk assessment, Amphibian, Frog, Toad

191

Salamanders are the only tetrapods capable of fully regenerating their limbs throughout their entire lives. Much data on the underlying molecular mechanisms of limb regeneration have been gathered in recent years allowing for new comparative studies between salamanders and other tetrapods that lack this unique regenerative potential. By contrast, the evolution of animal regeneration just recently shifted back into focus, despite being highly relevant for research designs aiming to unravel the factors allowing for limb regeneration. We show that the 300-million-year-old temnospondyl amphibian Micromelerpeton, a distant relative of modern amphibians, was already capable of regenerating its limbs. A number of exceptionally well-preserved specimens from fossil deposits show a unique pattern and combination of abnormalities in their limbs that is distinctive of irregular regenerative activity in modern salamanders and does not occur as variants of normal limb development. This demonstrates that the capacity to regenerate limbs is not a derived feature of modern salamanders, but may be an ancient feature of non-amniote tetrapods and possibly even shared by all bony fish. The finding provides a new framework for understanding the evolution of regenerative capacity of paired appendages in vertebrates in the search for conserved versus derived molecular mechanisms of limb regeneration.

Concepts: Developmental biology, Regeneration, Tetrapod, Amphibian, Lissamphibia, Salamander, Labyrinthodontia

181

gen. et sp. nov. is described from the Famennian Worange Point Formation; the holotype is amongst the largest tristichopterids and sarcopterygians documented by semi-articulated remains from the Devonian Period. The new taxon has dentary fangs and premaxillary tusks, features assumed to be derived for large Northern Hemisphere tristichopterids (, , ). It resembles in ornament, but is distinguished by longer proportions of the parietal compared to the post-parietal shield, and numerous differences in shape and proportions of other bones. Several characters (accessory vomers in the palate, submandibulars overlapping ventral jaw margin, scales ornamented with widely-spaced deep grooves) are recorded only in tristichopterids from East Gondwana (Australia-Antarctica). On this evidence gen. nov. is placed in an endemic Gondwanan subfamily Mandageriinae within the Tristichopteridae; it differs from the nominal genotype in its larger size, less pointed skull, shape of the orbits and other skull characters. The hypothesis that tristichopterids evolved in Laurussia and later dispersed into Gondwana, and a derived subgroup of large Late Devonian genera dispersed from Gondwana, is inconsistent with the evidence of the new taxon. Using oldest fossil and most primitive clade criteria the most recent phylogeny resolves South China and Gondwana as areas of origin for all tetrapodomorphs. The immediate outgroup to tristichopterids remains unresolved - either from Greenland as recently proposed, or from Gondwana, earlier suggested to be the sister group to all tristichopterids. Both taxa combine two characters that do not co-occur in other tetrapodomorphs (extratemporal bone in the skull; non-cosmoid round scales with an internal boss). Recently both ‘primitive’ and ‘derived’ tristichopterids have been discovered in the late Middle Devonian of both hemispheres, implying extensive ghost lineages within the group. Resolving their phylogeny and biogeography will depend on a comprehensive new phylogenetic analysis.

Concepts: Phylogenetic nomenclature, Phylogenetics, Cladistics, Vertebrate, Sarcopterygii, Tetrapod, Carboniferous, Devonian

176

Because of its close relationship to tetrapods, Eusthenopteron is an important taxon for understanding the establishment of the tetrapod body plan. Notably, it is one of the earliest sarcopterygians in which the humerus of the pectoral fin skeleton is preserved. The microanatomical and histological organization of this humerus provides important data for understanding the evolutionary steps that built up the distinctive architecture of tetrapod limb bones. Previous histological studies showed that Eusthenopteron’s long-bone organization was established through typical tetrapod ossification modalities. Based on a three-dimensional reconstruction of the inner microstructure of Eusthenopteron’s humerus, obtained from propagation phase-contrast X-ray synchrotron microtomography, we are now able to show that, despite ossification mechanisms and growth patterns similar to those of tetrapods, it also retains plesiomorphic characters such as a large medullary cavity, partly resulting from the perichondral ossification around a large cartilaginous bud as in actinopterygians. It also exhibits a distinctive tubular organization of bone-marrow processes. The connection between these processes and epiphyseal structures highlights their close functional relationship, suggesting that either bone marrow played a crucial role in the long-bone elongation processes or that trabecular bone resulting from the erosion of hypertrophied cartilage created a microenvironment for haematopoietic stem cell niches.

Concepts: Bone, Bone marrow, Skeletal system, Cartilage, Bird, Tetrapod, Long bone, Ichthyostega

172

IN RESOLVING THE VERTEBRATE TREE OF LIFE, TWO FUNDAMENTAL QUESTIONS REMAIN: 1) what is the phylogenetic position of turtles within amniotes, and 2) what are the relationships between the three major lissamphibian (extant amphibian) groups? These relationships have historically been difficult to resolve, with five different hypotheses proposed for turtle placement, and four proposed branching patterns within Lissamphibia. We compiled a large cDNA/EST dataset for vertebrates (75 genes for 129 taxa) to address these outstanding questions. Gene-specific phylogenetic analyses revealed a great deal of variation in preferred topology, resulting in topologically ambiguous conclusions from the combined dataset. Due to consistent preferences for the same divergent topologies across genes, we suspected systematic phylogenetic error as a cause of some variation. Accordingly, we developed and tested a novel statistical method that identifies sites that have a high probability of containing biased signal for a specific phylogenetic relationship. After removing putatively biased sites, support emerged for a sister relationship between turtles and either crocodilians or archosaurs, as well as for a caecilian-salamander sister relationship within Lissamphibia, with Lissamphibia potentially paraphyletic.

Concepts: Evolution, Species, Reptile, Phylogenetics, Cladistics, Tetrapod, Amphibian, Amniote

154

A major challenge in understanding the origin of terrestrial vertebrates has been knowledge of the pelvis and hind appendage of their closest fish relatives. The pelvic girdle and appendage of tetrapods is dramatically larger and more robust than that of fish and contains a number of structures that provide greater musculoskeletal support for posture and locomotion. The discovery of pelvic material of the finned elpistostegalian, Tiktaalik roseae, bridges some of these differences. Multiple isolated pelves have been recovered, each of which has been prepared in three dimensions. Likewise, a complete pelvis and partial pelvic fin have been recovered in association with the type specimen. The pelves of Tiktaalik are paired and have broad iliac processes, flat and elongate pubes, and acetabulae that form a deep socket rimmed by a robust lip of bone. The pelvis is greatly enlarged relative to other finned tetrapodomorphs. Despite the enlargement and robusticity of the pelvis of Tiktaalik, it retains primitive features such as the lack of both an attachment for the sacral rib and an ischium. The pelvic fin of Tiktaalik (NUFV 108) is represented by fin rays and three endochondral elements: other elements are not preserved. The mosaic of primitive and derived features in Tiktaalik reveals that the enhancement of the pelvic appendage of tetrapods and, indeed, a trend toward hind limb-based propulsion have antecedents in the fins of their closest relatives.

Concepts: Fish, Pelvis, Sarcopterygii, Tetrapod, Sacrum, Coelacanth, Ischium, Fin

152

Of the nearly 6,800 extant frog species, most have weak jaws that play only a minor role in prey capture. South American horned frogs (Ceratophrys) are a notable exception. Aggressive and able to consume vertebrates their own size, these “hopping heads” use a vice-like grip of their jaws to restrain and immobilize prey. Using a longitudinal experimental design, we quantified the ontogenetic profile of bite-force performance in post-metamorphic Ceratophrys cranwelli. Regression slopes indicate positive allometric scaling of bite force with reference to head and body size, results that concur with scaling patterns across a diversity of taxa, including fish and amniotes (lizards, tuatara, turtles, crocodylians, rodents). Our recovered scaling relationship suggests that exceptionally large individuals of a congener (C. aurita) and extinct giant frogs (Beelzebufo ampinga, Late Cretaceous of Madagascar) probably could bite with forces of 500 to 2200 N, comparable to medium to large-sized mammalian carnivores.

Concepts: Reptile, Mammal, Cretaceous, Tetrapod, Amphibian, Frog, Dinosaur, Amniote

147

Ranaviruses are pathogens of ectothermic vertebrates, including amphibians. We reviewed patterns of host range and virulence of ranaviruses in the context of virus genotype and postulate that patterns reflect significant variation in the historical and current host range of three groups of Ranavirus: FV3-like, CMTV-like and ATV-like ranaviruses. Our synthesis supports previous hypotheses about host range and jumps: FV3s are amphibian specialists, while ATVs are predominantly fish specialists that switched once to caudate amphibians. The most recent common ancestor of CMTV-like ranaviruses and FV3-like forms appears to have infected amphibians but CMTV-like ranaviruses may circulate in both amphibian and fish communities independently. While these hypotheses are speculative, we hope that ongoing efforts to describe ranavirus genetics, increased surveillance of host species and targeted experimental assays of susceptibility to infection and/or disease will facilitate better tests of the importance of hypothetical evolutionary drivers of ranavirus virulence and host range.

Concepts: DNA, Genetics, Evolution, Species, Tetrapod, Amphibian, Frog, Most recent common ancestor

74

Darwin’s frogs (Rhinoderma darwinii and R. rufum) are two species of mouth brooding frogs from Chile and Argentina that have experienced marked population declines. Rhinoderma rufum has not been found in the wild since 1980. We investigated historical and current evidence of Batrachochytrium dendrobatidis (Bd) infection in Rhinoderma spp. to determine whether chytridiomycosis is implicated in the population declines of these species. Archived and live specimens of Rhinoderma spp., sympatric amphibians and amphibians at sites where Rhinoderma sp. had recently gone extinct were examined for Bd infection using quantitative real-time PCR. Six (0.9%) of 662 archived anurans tested positive for Bd (4/289 R. darwinii; 1/266 R. rufum and 1/107 other anurans), all of which had been collected between 1970 and 1978. An overall Bd-infection prevalence of 12.5% was obtained from 797 swabs taken from 369 extant individuals of R. darwinii and 428 individuals representing 18 other species of anurans found at sites with current and recent presence of the two Rhinoderma species. In extant R. darwinii, Bd-infection prevalence (1.9%) was significantly lower than that found in other anurans (7.3%). The prevalence of infection (30%) in other amphibian species was significantly higher in sites where either Rhinoderma spp. had become extinct or was experiencing severe population declines than in sites where there had been no apparent decline (3.0%; x (2) = 106.407, P<0.001). This is the first report of widespread Bd presence in Chile and our results are consistent with Rhinoderma spp. declines being due to Bd infection, although additional field and laboratory investigations are required to investigate this further.

Concepts: Evolution, Extinction, Tetrapod, Amphibian, Frog, Chytridiomycosis, African clawed frog, Darwin's Frog