Carboniferous tetrapod biostratigraphy, biochronology and evolutionary events

Tetrapod (amphibian and amniote) fossils of Carboniferous age are known almost exclusively from the southern part of a paleoequatorial Euramerican province. The stratigraphic distribution of Carboniferous tetrapod fossils is used to identify five land-vertebrate faunachrons: (1) Hortonbluffian (Givetian-early Visean), the time between the FAD of tetrapods to the beginning of the Doran; (2) Doran (late Visean-early Bashkirian), the time between the FAD of the baphetid Loxomma and the beginning of the Nyranyan; (3) Nyranyan (late Bashkirian-Moscovian), the time between the FAD of the eureptile Hylonomus and the beginning of the Cobrean; (4) Cobrean (Kasimovian-late Gzhelian), the time between the FAD of the eupelycosaur Ianthasaurus and the beginning of the Coyotean; and (5) Coyotean (late Gzhelian-early Permian), the time between the FAD of the eupelycosaur Sphenacodon and the beginning of the Seymouran. This biochronology provides insight into some important evolutionary events in Carboniferous tetrapod evolution.

Description of the metoposaurid Anaschisma browni from the New Oxford Formation of Pennsylvania

Metoposaurids are a widespread and ubiquitous constituent of Late Triassic non-marine paleoenvironments. In North America, this group is practically the only large-bodied temnospondyl clade, and is particularly well documented from the American southwest and south-central regions (Arizona, New Mexico, Texas). However, metoposaurids are poorly documented from eastern North America, with fragmentary, doubtfully diagnostic historical material such as “Dictyocephalus elegans” Leidy, 1856 and “Eupelor durus” Cope, 1866. The Zions View (early Norian?) locality in Pennsylvania preserves more-complete material, which previous workers noted as belonging to “Buettneria perfecta” Case, 1922 (=Anaschisma browni Branson, 1905). However, the material has never been described in a fashion that characterizes the anatomy or that justifies the taxonomic assignment, yet it would represent the most complete material in eastern North America and a substantial expansion of this taxon's geographic range. Here we redescribe the Zions View metoposaurid material in detail, differentiating it from Calamops paludosus Sinclair, 1917, the only other Late Triassic temnospondyl from the eastern seaboard, and demonstrating confident affinities with A. browni. Our study is the first to properly justify the taxonomic referral, underscoring the broader importance of proper documentation of voucher specimens, especially for potential geographic outliers. Anaschisma browni is thus the most widely dispersed metoposaurid. Its easternmost documentation underscores the importance of the undersampled and understudied metoposaurid record on the eastern seaboard for understanding the development of a metoposaurid zone of exclusivity in North America and demonstrates the need for further exploration to refine conceptualizations of Late Triassic tetrapod evolution.

Recurrent evolution of vertebrate transcription factors by transposase capture

Genes with novel cellular functions may evolve through exon shuffling, which can assemble novel protein architectures. Here, we show that DNA transposons provide a recurrent supply of materials to assemble protein-coding genes through exon shuffling. We find that transposase domains have been captured—primarily via alternative splicing—to form fusion proteins at least 94 times independently over the course of ~350 million years of tetrapod evolution. We find an excess of transposase DNA binding domains fused to host regulatory domains, especially the Krüppel-associated box (KRAB) domain, and identify four independently evolved KRAB-transposase fusion proteins repressing gene expression in a sequence-specific fashion. The bat-specific KRABINER fusion protein binds its cognate transposons genome-wide and controls a network of genes and cis-regulatory elements. These results illustrate how a transcription factor and its binding sites can emerge.

The feeding system of Tiktaalik roseae: an intermediate between suction feeding and biting

Changes to feeding structures are a fundamental component of the vertebrate transition from water to land. Classically, this event has been characterized as a shift from an aquatic, suction-based mode of prey capture involving cranial kinesis to a biting-based feeding system utilizing a rigid skull capable of capturing prey on land. Here we show that a key intermediate, Tiktaalik roseae, was capable of cranial kinesis despite significant restructuring of the skull to facilitate biting and snapping. Lateral sliding joints between the cheek and dermal skull roof, as well as independent mobility between the hyomandibula and palatoquadrate, enable the suspensorium of T. roseae to expand laterally in a manner similar to modern alligator gars and polypterids. This movement can expand the spiracular and opercular cavities during feeding and respiration, which would direct fluid through the feeding apparatus. Detailed analysis of the sutural morphology of T. roseae suggests that the ability to laterally expand the cheek and palate was maintained during the fish-to-tetrapod transition, implying that limited cranial kinesis was plesiomorphic to the earliest limbed vertebrates. Furthermore, recent kinematic studies of feeding in gars demonstrate that prey capture with lateral snapping can synergistically combine both biting and suction, rather than trading off one for the other. A “gar-like” stage in early tetrapod evolution might have been an important intermediate step in the evolution of terrestrial feeding systems by maintaining suction-generation capabilities while simultaneously elaborating a mechanism for biting-based prey capture.

An Annotated Chromosome-Level Reference Genome of the Red-Eared Slider Turtle (Trachemys scripta elegans)

Among vertebrates, turtles have many unique characteristics providing biologists with opportunities to study novel evolutionary innovations and processes. We present here a high-quality, partially phased, and chromosome-level Red-Eared Slider (Trachemys scripta elegans, TSE) genome as a reference for future research on turtle and tetrapod evolution. This TSE assembly is 2.269 Gb in length, has one of the highest scaffold N50 and N90 values of any published turtle genome to date (N50 = 129.68 Mb and N90 = 19 Mb), and has a total of 28,415 annotated genes. We introduce synteny analyses using BUSCO single-copy orthologs, which reveal two chromosome fusion events accounting for differences in chromosome counts between emydids and other cryptodire turtles and reveal many fission/fusion events for birds, crocodiles, and snakes relative to TSE. This annotated chromosome-level genome will provide an important reference genome for future studies on turtle, vertebrate, and chromosome evolution.

Subdivision of ancestral scale genetic program underlies origin of feathers and avian scutate scales

Birds and other reptiles possess a diversity of feather and scale-like skin appendages. Feathers are commonly assumed to have originated from ancestral scales in theropod dinosaurs. However, most birds also have scaled feet, indicating birds evolved the capacity to grow both ancestral and derived morphologies. This suggests a more complex evolutionary history than a simple linear transition between feathers and scales. We set out to investigate the evolution of feathers via the comparison of transcriptomes assembled from diverse skin appendages in chicken, emu, and alligator. Our data reveal that feathers and the overlapping ‘scutate’ scales of birds share more similar gene expression to each other, and to two types of alligator scales, than they do to the tuberculate ‘reticulate’ scales on bird footpads. Accordingly, we propose a history of skin appendage diversification, in which feathers and bird scutate scales arose from ancestral archosaur body scales, whereas reticulate scales arose earlier in tetrapod evolution. We also show that many “feather-specific genes” are also expressed in alligator scales. In-situ hybridization results in feather buds suggest that these genes represent ancestral scale genes that acquired novel roles in feather morphogenesis and were repressed in bird scales. Our findings suggest that the differential reuse, in feathers, and suppression, in bird scales, of genes ancestrally expressed in archosaur scales has been a key factor in the origin of feathers – and may represent an important mechanism for the origin of evolutionary novelties.

An enigmatic braincase from Five Points, Ohio (Westphalian D) further supports a stem tetrapod position for aïstopods

ABSTRACTWe describe a new specimen of the aïstopodOestocephalusfrom Five Points, Ohio, which preserves much of the posterior braincase. The specimen, the largest aïstopod skull described, preserves the postorbital region to the occiput. The posterior braincase has coossified the basioccipital, exoccipitals, and opisthotic. The parasphenoid is rostrally restricted, toothless, and highly vaulted along the cultriform process. The lateral walls of the cultriform process are further reinforced by large longitudinally running, ventral flanges from the parietals. Two large endochondral ventral projections from the basioccipital, previously interpreted as basal tuberosities for hypaxial muscle insertion, are here instead interpreted as articulations for the branchial skeleton. This interpretation is further supported by traces of vasculature that is consistent with what is seen in gill-bearing species. A model for the reorganisation of the basicranial region on the transition from hyomandibula to stapes is proposed, which suggests that gills, or gill-support skeletal elements, might be further distributed along the tetrapod stem than previously thought. These data further support the placement of aïstopods in the tetrapod stem group and require a reconsideration of our understanding of early tetrapod evolution.

The evolution of the tetrapod humerus: morphometrics, disparity, and evolutionary rates

ABSTRACTThe present study explores the macroevolutionary dynamics of shape changes in the humeri of all major grades and clades of early tetrapods and their fish-like forerunners. Coordinate point eigenshape analysis applied to humeral outlines in extensor view reveals that fish humeri are more disparate than those of most early tetrapod groups and significantly separate from the latter. Our findings indicate sustained changes in humeral shape in the deepest portions of the tetrapod stem group and certain portions of the crown. In the first half of sampled tetrapod history, subclades show larger than expected humeral disparity, suggesting rapid diffusion into morphospace. Later in tetrapod evolution, subclades occupy smaller and non-overlapping morphospace regions. This pattern may reflect in part increasing specialisations in later tetrapod lineages. Bayesian shifts in rates of evolutionary change are distributed discontinuously across the phylogeny, and most of them occur within rather than between major groups. Most shifts with the highest Bayesian posterior probabilities are observed in lepospondyls. Similarly, maximum likelihood analyses of shifts support marked rate accelerations in lepospondyls and in various subclades within that group. In other tetrapod groups, rates either tend to slow down or experience only small increases. Somewhat surprisingly, no shifts are concurrent with structural, functional, or ecological innovations in tetrapod evolution, including the origin of digits, the water–land transition and increasing terrestrialisation. Although counterintuitive, these results are consistent with a model of continual phenotypic innovation that, although decoupled from key evolutionary changes, is possibly triggered by niche segregation in divergent clades and grades of early tetrapods.

Evolutionary changes in the orbits and palatal openings of early tetrapods, with emphasis on temnospondyls

ABSTRACTOpen palates with large interpterygoid vacuities are a diagnostic characteristic of temnospondyl amphibians, the most species-rich group of early tetrapods. Aside from their functional roles, several other aspects of such vacuities, such as their variation and spatial relationships relative to the orbits, have received only scarce attention. The present work examines patterns of shape and size changes in the orbits and vacuities of temnospondyls using a time-calibrated phylogeny of 69 temnospondyl taxa and 13 additional early tetrapod ‘outgroups' (colosteids, an embolomere, ‘microsaurs' and nectrideans). Orbit and vacuity outlines are quantified in a comparative framework using standard eigenshape analyses. In addition, we employ a series of ratios of linear measurements of both orbits and vacuities, and subject them to a phylogenetic principal component analysis in order to evaluate their proportional changes relative to the skull and to one another. Finally, we examine rates of evolutionary change and their associated shifts for shape and size for both structures, and assess the strength and significance of the correlations between these two variables using phylogenetic generalised least squares analyses. Although orbits and vacuities have fairly simple outlines, they both reveal complex models of proportional change across the temnospondyl phylogeny. These changes exhibit strong phylogenetic signal, that is, trait covariance among taxa is predicted by tree topology. We discuss the hypothesis that, early in tetrapod evolution, the functional role of the vacuities was related to the accommodation of the anterior jaw muscles. Only later in evolution did such vacuities serve to accommodate the eye muscles only.