Oldest Pathology in a Tetrapod Bone Illuminates the Origin of Terrestrial Vertebrates

The origin of terrestrial tetrapods was a key event in vertebrate evolution, yet how and when it occurred remains obscure, due to scarce fossil evidence. Here, we show that the study of palaeopathologies, such as broken and healed bones, can help elucidate poorly understood behavioural transitions such as this. Using high-resolution finite element analysis, we demonstrate that the oldest known broken tetrapod bone, a radius of the primitive stem tetrapod Ossinodus pueri from the mid-Viséan (333 million years ago) of Australia, fractured under a high-force, impact-type loading scenario. The nature of the fracture suggests that it most plausibly occurred during a fall on land. Augmenting this are new osteological observations, including a preferred directionality to the trabecular architecture of cancellous bone. Together, these results suggest that Ossinodus, one of the first large (>2m length) tetrapods, spent a significant proportion of its life on land. Our findings have important implications for understanding the temporal, biogeographical and physiological contexts under which terrestriality in vertebrates evolved. They push the date for the origin of terrestrial tetrapods further back into the Carboniferous by at least two million years. Moreover, they raise the possibility that terrestriality in vertebrates first evolved in large tetrapods in Gondwana rather than in small European forms, warranting a re-evaluation of this important evolutionary event.     

The First Stem Tetrapod from the Lower Carboniferous of Gondwana

The first stem tetrapod from Gondwana, Ossinodus pueri gen. et sp. nov, is described from fragmentary material that includes a skull table and many important parts from the postcranial skeleton. It was recovered together with a typically non-marine to marginal (near) marine fish fauna from the Lower Carboniferous (mid Viséan) Ducabrook Formation, Queensland, Australia. Phylogenetic analysis hypothesises that Ossinodus belonged to a clade that includes Whatcheeria and Pederpes , positioned on the stem of the crown tetrapods, one step crownward of Tulerpeton . Hind limb morphology suggests that small specimens of Ossinodus were primarily aquatic but that larger ones were less so.     

Middle–Late Permian tetrapods from the Rio do Rasto Formation,Southern Brazil: a biostratigraphic reassessment

Dias‐da‐Silva, S. 2011: Middle–Late Permian tetrapods from the Rio do Rasto Formation, Southern Brazil: a biostratigraphic reassessment. Lethaia, Vol. 45, pp. 109–120. The Rio do Rasto Formation (Permian of Southern Brazil) was previously regarded as Guadalupian–early Lopingian age. Three tetrapod‐based localities are known: the Serra do Cadeado area, Aceguá and Posto Queimado. The latest tetrapod‐based biostratigraphic contribution considers that the Posto Queimado and Aceguá faunas are coeval and Wordian (middle Guadalupian) in age, correlated to the Isheevo faunas from Eastern Europe and to the Tapinocephalus Assemblage Zone of South Africa; whereas the Serra do Cadeado fauna is Capitanian (late Guadalupian), correlated to the Kotelnich fauna of Eastern Europe and, from bottom to top, to upper Pristerognathus, Tropidostoma and lower Cistecephalus assemblage zones of South Africa. A re‐evaluation of the tetrapods from the Rio do Rasto Formation and new fossil discoveries in the localities of Posto Queimado and Serra do Cadeado area (melosaurine and platyoposaurine temnospondyls, a basal anomodont, a dinocephalian and a basal dicynodont) supports a new tetrapod‐based biostratigraphic scheme for the Rio do Rasto Formation. Accordingly, the age of the fauna at Aceguá is late Roadian‐early Wordian, whereas the locality of Posto Queimado is late Wordian‐Capitanian. The Serra do Cadeado Area is correlated with both southernmost ones (Guadalupian) but also Wuchiapinghian (early Lopingian). □Paraná Basin, Passa Dois Group, tetrapod biostratigraphy, Western Gondwana.     

Getting a grip on tetrapod grasping: form,function, and evolution

Human beings have been credited with unparalleled capabilities for digital prehension grasping. However, grasping behaviour is widespread among tetrapods. The propensity to grasp, and the anatomical characteristics that underlie it, appear in all of the major groups of tetrapods with the possible exception of terrestrial turtles. Although some features are synapomorphic to the tetrapod clade, such as well‐defined digits and digital musculature, other features, such as opposable digits and tendon configurations, appear to have evolved independently in many lineages. Here we examine the incidence, functional morphology, and evolution of grasping across four major tetrapod clades. Our review suggests that the ability to grasp with the manus and pes is considerably more widespread, and ecologically and evolutionarily important, than previously thought. The morphological bases and ecological factors that govern grasping abilities may differ among tetrapods, yet the selective forces shaping them are likely similar. We suggest that further investigation into grasping form and function within and among these clades may expose a greater role for grasping ability in the evolutionary success of many tetrapod lineages.     

Postcranial stem tetrapod remains from the Devonian of Scat Craig, Morayshire, Scotland

The postcranial stem tetrapod remains from Scat Craig include a neural arch, humerus, tibia, femur, and incomplete pectoral girdles and ilia. These elements are all large or very large compared with the corresponding bones of other stem tetrapods. They correlate well in size with the proportions of Elginerpeton , the known stem tetrapod from Scat Craig, and probably belong to this genus. The neural arch has weak zygapophyses, and the ilia and shoulder girdles resemble those of Ichthyostega . The femur is strongly twisted, with the intercondylar fossa facing anteroventrally, so the hind limb probably functioned as a paddle. The tibia is broad, as in Acanthostega and Ichthyostega . The humerus is approximately intermediate in shape between those of osteolepiforms and later stem tetrapods, but seems to have a ventral radial facet like Ichthyostega . Overall, the postcranial bones combine apparent synapomorphies with Ichthyostega and characters which are uniquely primitive among stemgroup tetrapods. This character combination is incongruent. A recently discovered postorbital bone from the site is, strictly speaking, indeterminable but may belong to Elginerpeton ; it broadly resembles the postorbitals of Ichthyostega and Acanthostega , and demonstrates that the typical stem tetrapod facial morphology had evolved before the end of the Frasnian.     

The complete mitochondrial DNA sequence of the shark Mustelus manazo: evaluating rooting contradictions to living bony vertebrates

A remarkable example of a misleading mitochondrial protein tree is presented, involving ray-finned fishes, coelacanths, lungfishes, and tetrapods, with sea lampreys as an outgroup. In previous molecular phylogenetic studies on the origin of tetrapods, ray-finned fishes have been assumed as an outgroup to the tetrapod/lungfish/coelacanth clade, an assumption supported by morphological evidence. Standard methods of molecular phylogenetics applied to the protein-encoding genes of mitochondria, however, give a bizarre tree in which lamprey groups with lungfish and, therefore, ray-finned fishes are not the outgroup to a tetrapod/lungfish/coelacanth clade. All of the dozens of published phylogenetic methods, including every possible modification to maximum likelihood known to us (such as inclusion of site heterogeneity and exclusion of potentially misleading hydrophobic amino acids), fail to place the ray-finned fishes in a biologically acceptable position. A likely cause of this failure may be the use of an inappropriate outgroup. Accordingly, we have determined the complete mitochondrial DNA sequence from the shark, Mustelus manazo, which we have used as an alternative and more proximal outgroup than the lamprey. Using sharks as the outgroup, lungfish appear to be the closest living relative of tetrapods, although the possibility of a lungfish/coelacanth clade being the sister group of tetrapods cannot be excluded.      

Proposed habitats of early tetrapods: gills, kidneys, and the water-land transition

Recent finds of early tetrapods have established that the most primitive form, Acanthostega, retained internal gills and other fish-like features; this has led to the conclusion that it was a primarily aquatic animal. Other Late Devonian tetrapods, such as lchthyostega and Tulerpeton, provide no evidence of internal gills, but have also been interpreted as inhabiting an aquatic environment. The probable aquatic habits of a diversity of Devonian tetrapods has led to the suggestion that the entire early tetrapod radiation may have been an aquatic one, with terrestriality having evolved in later forms. However, consideration of the physiology of living amphibious vertebrates suggests that this scenario is unlikely. The use of the gills for the excretion of carbon dioxide and ammonia appears to be a fundamental feature of all primarily aquatic vertebrates. No living fish loses its internal gills, even if it excretes a significant portion of its nitrogenous waste as urea via the kidney in the water. Gills are simply too valuable to be lost by an aquatic animal, even in those air-breathing fishes that no longer use the gills for oxygen uptake. We suggest that the apparent loss of the gills in tetrapods more derived than Acanthostega signals their descent from a more terrestrial phase in tetrapod evolution, following the primary assumption by the kidney of the excretion of nitrogenous wastes. Without this new role of the kidney, loss of the gills would have been impossible. With this new kidney role, loss of the gills may have been advantageous in reducing desiccation on land.     

Fins to limbs: what the fossils say

A broad phylogenetic review of fins, limbs, and girdles throughout the stem and base of the crown group is needed to get a comprehensive idea of transformations unique to the assembly of the tetrapod limb ground plan. In the lower part of the tetrapod stem, character state changes at the pectoral level dominate; comparable pelvic level data are limited. In more crownward taxa, pelvic level changes dominate and repeatedly precede similar changes at pectoral level. Concerted change at both levels appears to be the exception rather than the rule. These patterns of change are explored by using afternative treatments of data in phylogenetic analyses. Results highlight a large data gap in the stem group preceding the first appearance of limbs with digits. It is also noted that the record of morphological diversity among stem tetrapods is somewhat worse than that of basal crown group tetrapods. The pre-limbed evolution of stem tetrapod paired fins is marked by a gradual reduction in axial segment numbers (mesomeres); pectoral fins of the sister group to limbed tetrapods include only three. This reduction in segment number is accompanied by increased regional specialization, and these changes are discussed with reference to the phylogenetic distribution of characteristics of the stylopod, zeugopod, and autopod.     

New discoveries of tetrapods (ichthyostegid‐like and whatcheeriid‐like) in the Famennian (Late Devonian) localities of Strud and Becco (Belgium)

The origin of tetrapods is one of the key events in vertebrate history. The oldest tetrapod body fossils are Late Devonian (Frasnian–Famennian) in age, most of them consisting of rare isolated bone elements. Here we describe tetrapod remains from two Famennian localities from Belgium: Strud, in the Province of Namur, and Becco, in the Province of Liège. The newly collected material consists of an isolated complete postorbital, fragments of two maxillae, and one putative partial cleithrum, all from Strud, and an almost complete maxilla from Becco. The two incomplete maxillae and cleithrum from Strud, together with the lower jaw previously recorded from this site, closely resemble the genus Ichthyostega, initially described from East Greenland. The postorbital from Strud and the maxilla from Becco do not resemble the genus Ichthyostega. They show several derived anatomical characters allowing their tentative assignment to a whatcheeriid‐grade group. The new tetrapod records show that there are at least two tetrapod taxa in Belgium and almost certainly two different tetrapod taxa at Strud. This locality joins the group of Devonian tetrapod‐bearing localities yielding more than one tetrapod taxon, confirming that environments favourable to early tetrapod life were often colonized by several tetrapod taxa.     

Radiation and functional diversification of alpha keratins during early vertebrate evolution

The conquest of land was arguably one of the most fundamental ecological transitions in vertebrates and entailed significant changes in skin structure and appendages to cope with the new environment. In extant tetrapods, the rigidity of the integument is largely created by type I and type II keratins, which are structural proteins essential in forming a strong cytoplasmic network. It is expected that such proteins have undergone fundamental changes in both stem and crown tetrapods. Here, we integrate genomic, phylogenetic, and expression data in a comprehensive study on the early evolution and functional diversification of tetrapod keratins. Our analyses reveal that all type I and type II tetrapod keratins evolved from only two genes that were present in the ancestor of extant vertebrates. Subsequently, the water-to-land transition in the stem lineage of tetrapods was associated with a major radiation and functional diversification of keratin genes. These duplications acquired functions that serve rigidity in integumental hard structures and were the prime for subsequent independent keratin diversification in tetrapod lineages.     

Links between global taxonomic diversity,ecological diversity and the expansion of vertebrates on land

Tetrapod biodiversity today is great; over the past 400 Myr since vertebrates moved onto land, global tetrapod diversity has risen exponentially, punctuated by losses during major extinctions. There are links between the total global diversity of tetrapods and the diversity of their ecological roles, yet no one fully understands the interplay of these two aspects of biodiversity and a numerical analysis of this relationship has not so far been undertaken. Here we show that the global taxonomic and ecological diversity of tetrapods are closely linked. Throughout geological time, patterns of global diversity of tetrapod families show 97 per cent correlation with ecological modes. Global taxonomic and ecological diversity of this group correlates closely with the dominant classes of tetrapods (amphibians in the Palaeozoic, reptiles in the Mesozoic, birds and mammals in the Cenozoic). These groups have driven ecological diversity by expansion and contraction of occupied ecospace, rather than by direct competition within existing ecospace and each group has used ecospace at a greater rate than their predecessors.     

Devonian climate change, breathing, and the origin of the tetrapod stem group

The diversification of the tetrapod stem group occurred duringthe late Middle through the Late Devonian, that is from theGivetian to Famennian stages about 385–365 million yearsago. The relationships between the known taxa representing thisradiation have currently reached a reasonable consensus so thatinterpretations of the order of appearance of tetrapod charactersis possible. The immediate fish relatives of the earliest limbedtetrapods show what is interpreted as a progressive increasein the spiracular chamber and its opening to the outside. Here,this is inferred to be associated with an increased capacityfor air-breathing. Lungs are thought to have been present inmost early bony fishes, and were most likely ventilated by air-gulping.This could have brought about a facultative capacity for air-breathing,which the tetrapod stem group exploited to the greatest degree.These adaptations are shown not only in freshwater forms butalso in estuarine and marginal marine forms. Estimates of oxygenlevels during this period suggest that they were unprecedentedlylow during the Givetian and Frasnian periods. At the same time,plant diversification was at its most rapid, changing the characterof the landscape and contributing, via soils, soluble nutrients,and decaying plant matter, to anoxia in all water systems. Theco-occurrence of these global events may explain the evolutionof air-breathing adaptations in at least two lobe-finned groups,contributing directly to the rise of the tetrapod stem group.In contrast to recent studies, low atmospheric oxygen is notconsidered to be a causal factor in the lack of fossils documentingthe evolution of Early Carboniferous tetrapods.     

Two Perspectives on the Evolution of the Tetrapod Limb

SYNOPSIS. The evolution of the tetrapod limb is examined fromtwo perspectives: structural and functional. Rosen et al. (1981)argued that lungfishes are the sister group of tetrapods, withlimb characteristics comprising an important subset of theirevidence. A re-analysis of the limb characters advocated byRosen et al. does not support their contention, but insteadsuggests that rhipidistian fishes of the family Osteolepidaeare the closest relatives of the tetrapods. In order to understandthe probable selective pressures leading to evolution of thetetrapod limb, a functional analysis of the fins of antennariidanglerfishes was performed. Antennariids use their limb-likefins to traverse underwater substrates. The analysis revealsa large number of functional and morphological convergencesbetween antennariid fins and tetrapod limbs. It is suggestedthat tetrapod limbs were evolved for underwater transport ratherthan for locomotion on dry land.     

The origin and early evolutionary history of amniotes

Recent phylogenetic analyses of Paleozoic tetrapods have yielded startling new insights into the origin and early evolutionary history of amniotes. The origin of this successful group involves evolutionary innovations that are associated with the development of the cleidoic egg and related reproductive strategies, and are therefore not represented directly in the fossil record. Despite this obvious difficulty, recent studies have been able to distinguish Paleozoic amniotes from their anamniotic tetrapod relatives to determine major patterns of interrelationships.     

Biogeography of Triassic tetrapods: evidence for provincialism and driven sympatric cladogenesis in the early evolution of modern tetrapod lineages

Triassic tetrapods are of key importance in understanding their evolutionary history, because several tetrapod clades, including most of their modern lineages, first appeared or experienced their initial evolutionary radiation during this Period. In order to test previous palaeobiogeographical hypotheses of Triassic tetrapod faunas, tree reconciliation analyses (TRA) were performed with the aim of recovering biogeographical patterns based on phylogenetic signals provided by a composite tree of Middle and Late Triassic tetrapods. The TRA found significant evidence for the presence of different palaeobiogeographical patterns during the analysed time spans. First, a Pangaean distribution is observed during the Middle Triassic, in which several cosmopolitan tetrapod groups are found. During the early Late Triassic a strongly palaeolatitudinally influenced pattern is recovered, with some tetrapod lineages restricted to palaeolatitudinal belts. During the latest Triassic, Gondwanan territories were more closely related to each other than to Laurasian ones, with a distinct tetrapod fauna at low palaeolatitudes. Finally, more than 75 per cent of the cladogenetic events recorded in the tetrapod phylogeny occurred as sympatric splits or within-area vicariance, indicating that evolutionary processes at the regional level were the main drivers in the radiation of Middle and Late Triassic tetrapods and the early evolution of several modern tetrapod lineages.     

The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev

Postcranial remains of the Russian Late Devonian tetrapod Tulerpeton include the hexadactylous fore limb, hind limb, anocleithral pectoral girdle, squamation, and associated disarticulated postcranial bones. A cladistic analysis indicates that Tulerpeton is a reptiliomorph stem-group amniote and the earliest known crown-group tetrapod: Acanthostega and Ichthyostega are successively more derived plesion stem-group tetrapods and do not consititute a monophyletic ichthyostegalian radiation. Previous analyses suggesting a profound split in tetrapod phylogeny are thereby corroborated, and likewise the interpretation of Westlothiana as a stem-group amniote. The divergence of reptiliomorphs from batrachomorphs occurred before the Devonian-Carboniferous boundary. Tulerpeton originates from an entirely aquatic environment with a diverse fish fauna. The morphologies of its limbs and those of Devonian stem-tetrapods suggest that dactyly predates the elaboration of the carpus and tarsus, and that Polydactyly persisted after the evolutionary divergence of the principal lineages of living tetrapods. The apparent absence of a branchial lamina and gill skeleton suggests that Tulerpeton was primarily air-breathing, whereas contemporary stem-group tetrapods and more recent batrachomorphs retained greater emphasis on gill-breathing.     

Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins‐to‐limbs transition

The question of how tetrapod limbs evolved from fins is one of the great puzzles of evolutionary biology. While palaeontologists, developmental biologists, and geneticists have made great strides in explaining the origin and early evolution of limb skeletal structures, that of the muscles remains largely unknown. The main reason is the lack of consensus about appendicular muscle homology between the closest living relatives of early tetrapods: lobe‐finned fish and crown tetrapods. In the light of a recent study of these homologies, we re‐examined osteological correlates of muscle attachment in the pectoral girdle, humerus, radius, and ulna of early tetrapods and their close relatives. Twenty‐nine extinct and six extant sarcopterygians were included in a meta‐analysis using information from the literature and from original specimens, when possible. We analysed these osteological correlates using parsimony‐based character optimization in order to reconstruct muscle anatomy in ancestral lobe‐finned fish, tetrapodomorph fish, stem tetrapods, and crown tetrapods. Our synthesis revealed that many tetrapod shoulder muscles probably were already present in tetrapodomorph fish, while most of the more‐distal appendicular muscles either arose later from largely undifferentiated dorsal and ventral muscle masses or did not leave clear correlates of attachment in these taxa. Based on this review and meta‐analysis, we postulate a stepwise sequence of specific appendicular muscle acquisitions, splits, and fusions that led from the ancestral sarcopterygian pectoral fin to the ancestral tetrapod forelimb. This sequence largely agrees with previous hypotheses based on palaeontological and comparative work, but it is much more comprehensive in terms of both muscles and taxa. Combined with existing information about the skeletal system, our new synthesis helps to illuminate the genetic, developmental, morphological, functional, and ecological changes that were key components of the fins‐to‐limbs transition.     

Evolution of monogenean parasites across vertebrate hosts illuminated by the phylogenetic position of Euzetrema Combes, 1965 within the Monopisthocotylea

The Monogenea, which is divided into two clades, namely the Monopisthocotylea and Polyopisthocotylea, is a highly diversified group of platyhelminth parasites that infest mainly actinopterygian and chondrichthyan fishes but also, to a lesser extent, freshwater sarcopterygian hosts. Euzetrema knoepffleri Combes, 1965 (Monogenea: Iagotrematidae), which is specific to the salamander Euproctus montanus Savi, 1838 is among the rare monopisthocotylean parasites infesting tetrapod hosts. We sequenced the complete 18S rRNA gene of this parasite to infer its phylogenetic position within the Monopisthocotylea. Our results provide a new insight for coevolutionary scenarios between monopisthocotyleans and gnathostomatan hosts. Indeed, the basal position of E. knoepffleri within a subgroup of the Monopisthocotylea which comprises two clusters that both include parasites of the Actinopterygii and Chondrichthyes, suggests a very old association between the Iagotrematidae and tetrapods. Furthermore, if we take into account a recent view of Gnathostomata evolution where bony and cartilaginous fishes are regarded as a monophyletic group, it could be argued that the Iagotrematidae arose very early, during the fish–tetrapod transition, as did the Polystomatidae, the only monogenean family of the Polyopisthocotylea that infests sarcopterygian hosts.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 727–734.     

Development and evolution of the muscles of the pelvic fin

Locomotor strategies in terrestrial tetrapods have evolved from the utilisation of sinusoidal contractions of axial musculature, evident in ancestral fish species, to the reliance on powerful and complex limb muscles to provide propulsive force. Within tetrapods, a hindlimb-dominant locomotor strategy predominates, and its evolution is considered critical for the evident success of the tetrapod transition onto land. Here, we determine the developmental mechanisms of pelvic fin muscle formation in living fish species at critical points within the vertebrate phylogeny and reveal a stepwise modification from a primitive to a more derived mode of pelvic fin muscle formation. A distinct process generates pelvic fin muscle in bony fishes that incorporates both primitive and derived characteristics of vertebrate appendicular muscle formation. We propose that the adoption of the fully derived mode of hindlimb muscle formation from this bimodal character state is an evolutionary innovation that was critical to the success of the tetrapod transition.