Early amphibians evolved distinct vertebrae for habitat invasions

Living tetrapods owe their existence to a critical moment 360–340 million years ago when their ancestors walked on land. Vertebrae are central to locomotion, yet systematic testing of correlations between vertebral form and terrestriality and subsequent reinvasions of aquatic habitats is lacking, obscuring our understanding of movement capabilities in early tetrapods. Here, we quantified vertebral shape across a diverse group of Paleozoic amphibians (Temnospondyli) encompassing different habitats and nearly the full range of early tetrapod vertebral shapes. We demonstrate that temnospondyls were likely ancestrally terrestrial and had several early reinvasions of aquatic habitats. We find a greater diversity in temnospondyl vertebrae than previously known. We also overturn long-held hypotheses centered on weight-bearing, showing that neural arch features, including muscle attachment, were plastic across the water-land divide and do not provide a clear signal of habitat preferences. In contrast, intercentra traits were critical, with temnospondyls repeatedly converging on distinct forms in terrestrial and aquatic taxa, with little overlap between. Through our geometric morphometric study, we have been able to document associations between vertebral shape and environmental preferences in Paleozoic tetrapods and to reveal morphological constraints imposed by vertebrae to locomotion, independent of ancestry.

A Triassic stem-salamander from Kyrgyzstan and the origin of salamanders

The origin of extant amphibians remains largely obscure, with only a few early Mesozoic stem taxa known, as opposed to a much better fossil record from the mid-Jurassic on. In recent time, anurans have been traced back to Early Triassic forms and caecilians have been traced back to the Late JurassicEocaecilia, both of which exemplify the stepwise acquisition of apomorphies. Yet the most ancient stem-salamanders, known from mid-Jurassic rocks, shed little light on the origin of the clade. The gap between salamanders and other lissamphibians, as well as Paleozoic tetrapods, remains considerable. Here we report a new specimen ofTriassurus sixtelae, a hitherto enigmatic tetrapod from the Middle/Late Triassic of Kyrgyzstan, which we identify as the geologically oldest stem-group salamander. This sheds light not only on the early evolution of the salamander body plan, but also on the origin of the group as a whole. The new, second specimen is derived from the same beds as the holotype, the Madygen Formation of southwestern Kyrgyzstan. It reveals a range of salamander characters in this taxon, pushing back the rock record of urodeles by at least 60 to 74 Ma (Carnian–Bathonian). In addition, this stem-salamander shares plesiomorphic characters with temnospondyls, especially branchiosaurids and amphibamiforms.

What do ossification sequences tell us about the origin of extant amphibians?

The origin of extant amphibians has been studied using several sources of data and methods, including phylogenetic analyses of morphological data, molecular dating, stratigraphic data, and integration of ossification sequence data, but a consensus about their affinities with other Paleozoic tetrapods has failed to emerge. We have compiled five datasets to assess the relative support for six competing hypotheses about the origin of extant amphibians: a monophyletic origin among temnospondyls, a monophyletic origin among lepospondyls, a diphyletic origin among both temnospondyls and lepospondyls, a diphyletic origin among temnospondyls alone, and two variants of a triphyletic origin, in which anurans and urodeles come from different temnospondyl taxa while caecilians come from lepospondyls and are either closer to anurans and urodeles or to amniotes. Our datasets comprise ossification sequences of up to 107 terminal taxa and up to eight cranial bones, and up to 65 terminal taxa and up to seven appendicular bones, respectively. Among extinct taxa, only two or three temnospondyl can be analyzed simultaneously for cranial data, but this is not an insuperable problem because each of the six tested hypotheses implies a different position of temnospondyls and caecilians relative to other sampled taxa. For appendicular data, more extinct taxa can be analyzed, including some lepospondyls and the finned tetrapodomorph Eusthenopteron, in addition to temnospondyls. The data are analyzed through maximum likelihood, and the AICc (corrected Akaike Information Criterion) weights of the six hypotheses allow us to assess their relative support. By an unexpectedly large margin, our analyses of the cranial data support a monophyletic origin among lepospondyls; a monophyletic origin among temnospondyls, the current near-consensus, is a distant second. All other hypotheses are exceedingly unlikely according to our data. Surprisingly, analysis of the appendicular data supports triphyly of extant amphibians within a clade that unites lepospondyls and temnospondyls, contrary to all phylogenies based on molecular data and recent trees based on paleontological data, but this conclusion is not very robust.

The origin and early radiation of terrestrial vertebrates

The origin of tetrapods from sarcopterygian fish in the Late Devonian is one of the best known major transitions in the history of vertebrates. Unfortunately, extensive gaps in the fossil record of the Lower Carboniferous and Triassic make it very difficult to establish the nature of relationships among Paleozoic tetrapods, or their specific affinities with modern amphibians. The major lineages of Paleozoic labyrinthodonts and lepospondyls are not adequately known until after a 20–30 m.y. gap in the Early Carboniferous fossil record, by which time they were highly divergent in anatomy, ways of life, and patterns of development. An even wider temporal and morphological gap separates modern amphibians from any plausible Permo-Carboniferous ancestors. The oldest known caecilian shows numerous synapomorphies with the lepospondyl microsaur Rhynchonkos. Adult anatomy and patterns of development in frogs and salamanders support their origin from different families of dissorophoid labyrinthodonts. The ancestry of amniotes apparently lies among very early anthracosaurs.

Origin and early evolution of the amniote occiput

Reinterpretation of cranial materials of the diadectomorphs Limnoscelis and Diadectes has prompted a reconsideration of the origin and early evolution of the amniote occiput. The basic approach is a phylogenetic study of major groups of Paleozoic tetrapods based on the occiput and closely associated elements of the skull roof. A lack of adequate anatomical data has forced the elimination of only a few relevant higher-level taxa from consideration, and, using Acanthostega as the reference outgroup, a cladistic analysis of the interrelationships of the Lepospondyli, Temnospondyli, Seymouriamorpha, Baphetidae (= Loxommatidae), Anthracosauria, Diadectomorpha, Synapsida, and Reptilia has produced the following results: 1) the ingroup taxa exhibit a basal dichotomy in which one division consists of the unresolved relationships of Lepospondyli, Temnospondyli, and Seymouriamorpha; 2) the pattern of relationships of the second division of the ingroup taxa is a series of nested clades, terminating with the Diadectomorpha and Synapsida as sister taxa sharing a more recent common ancestor than either does with Reptilia. This relationship requires assignment of Diadectomorpha to Amniota; and 3) the Anthracosauria and Baphetidae are progressively more distant clades or sister taxa. On the basis of the cladistic analysis, the attainment of the amniote occiput is described as passing through four morphological grades of organization. Each grade of the series is characterized by a set of derived character states that defines the progressively more-derived nodes and from which branch a clade containing the unresolved trichotomy of Lepospondyli, Temnospondyli, and Seymouriamorpha; the Baphetidae clade; the Anthracosauria clade; and the Diadectomorpha + Synapsida and Reptilia clades, respectively.

The atlas-axis complex of the Late Paleozoic Diadectomorpha and basal amniotes: defining the primitive condition of the atlas-axis complex of amniotes

During the past decade, phylogenetic analyses of Late Paleozoic tetrapods have consistently demonstrated that the Permo-Pennsylvanian tetrapod suborder Diadectomorpha is closely related to more traditionally defined amniotes. Recent analyses provide two competing hypotheses of relationship: 1) the Diadectomoropha is the sister group of all amniotes, or 2) the Diadectomorpha and Synapsida comprise the most primitive clade within the Amniota. Subsequently more derived groups within the Amniota are: the reptilian family Captorhinidae, and the Protorothyrididae plus the Diapsida. The availability of well preserved atlas-axis complexes for all of the better known genera of diadectomorphs now allow a determination of the primitive condition of the atlas-axis complex for the Amniota. Further, accepted hypotheses of phylogenetic relationships among Late Paleozoic tetrapods allow mapping of features of the atlas-axis complex onto predefined topologies so that the transformations of the complex may be analyzed.The diadectomorph atlas-axis complex may be characterized in the following manner: paired, well developed proatlases and atlantal neural arches; lack of proatlantal and atlantal neural spines with only posteriorly directed epipophyses present; an extremely robust atlantal intercentrum; tight articulation of the atlantal pleurocentrum with the dorsal aspect of the axial intercentrum preventing exposure of the former on the ventral surface of the vertebral column; a large, anteriorly directed midline projection of the axial intercentrum; a tall and well-developed axial neural spine, presumably for attachment of strong occipital muscles and ligaments. Except for the anterior projection of the axial intercentrum (which is an autapomorphic feature of diadectomorphs), basal amniotes share all of these features with diadectomorphs. Shared, derived features of the atlas-axis complex of diadectomorphs plus other basal amniotes include: 1) fusion of the axial centrum and neural arch, 2) small epipophyses of the atlantal neural arch and, with the exception of Tseajaia, 3) fusion of the atlantal pleurocentrum to the dorsal surface of the axial intercentrum.The morphology of the atlas-axis complex alone is not sufficient to generate hypotheses of relationship between diadectomorphs and other basal amniotes. However, the atlas-axis complexes of diadectomorphs and other basal amniotes are clearly more similar to one-another than to those of other taxa.

The oldest microsaur (Amphibia)

Utaherpeton franklini n. gen. and sp., from the Manning Canyon Shale Formation of Utah, is the oldest known microsaur. The horizon is dated as equivalent to the lowermost Namurian B of Europe (transitional from Upper Mississippian into lowermost Pennsylvanian in North American terminology) on the basis of a rich assemblage of fossil plants. The specimen may be tentatively placed within the suborder Microbrachomorpha. It exhibits the primitive character state for many microsaur features, but no synapomorphies are recognized that support a specific sister-group relationship between microsaurs and any other group of Paleozoic tetrapods.

A tetrapod lower jaw from the Pennsylvanian (Westphalian A) of Nova Scotia

The left half of a tetrapod lower jaw, from the Parrsboro Formation (Pennsylvanian, Westphalian A) of Nova Scotia, is preserved as a natural mold in a sandstone. Most of the features of this lower mandible are primitive for tetrapods or non-ichthyostegalian tetrapods. Although the presence of an adsymphysial tooth plate in this specimen is regarded as the retention of an osteolepiform feature, the tusk and replacement pit on this dermal bone may be unique to this taxon. The poor preservation of the lower jaws associated with some previously described Paleozoic tetrapods, together with the unique features in other early tetrapod jaws, precludes the reference of this mandible to any known tetrapod taxon.