Shell biomechanics suggests an aquatic palaeoecology at the dawn of turtle evolution.

The turtle shell is a remarkable structure that has intrigued not only evolutionary biologists but also engineering and material scientists because of its multi-scale complexity and various functions. Although protection is its most apparent role, the carapace and plastron are also related to many physiological functions and their shape influences hydrodynamics and self-righting ability. As such, analysing the functional morphology of the shell could help understanding the ecology of Triassic stem-turtles, which will contribute to the century-long debate on the evolutionary origins of turtles. Here, we used 3D imaging techniques to digitize the shells of two of the earliest stem-turtle taxa, Proganochelys and Proterochersis, and submitted their models to biomechanical and shape analyses. We analysed the strength performance under five predation scenarios and tested the function of two morphological traits found in stem-turtles, the epiplastral processes and an attached pelvic girdle. The latter, also present in the crown-lineage of side-necked turtles, has been suggested to increase load-bearing capacity of the shell or to improve swimming in pleurodires. Our results do not confirm the shell-strengthening hypothesis and, together with the results of our shape analyses, suggest that at least one of the first stem-turtles (Proterochersis) was an aquatic animal.

New insights into the early morphological evolution of sea turtles by re-investigation of Nichollsemys baieri, a three-dimensionally preserved fossil stem chelonioid from the Campanian of Alberta, Canada.

The early evolution of Pan-Chelonioidea (sea turtles) is poorly understood. This is in part due to the rarity of undeformed skulls of definitive early stem chelonioids. In this work, we redescribe the holotype of Nichollsemys baieri using µCT scans and segmentations of the skull. This fossil is the best 3D preserved skull of any Campanian sea turtle, and includes partial "soft tissue" preservation. Nichollsemys is morphologically similar but clearly distinct from Toxochelys spp., and both show a mosaic of plesiomorphic and derived chelonioid features. The internal cranial anatomy documents the presence of derived characters in Nichollsemys baieri that are absent in Toxochelys spp., such as the loss of the epipterygoids and the rod-like shape of the rostrum basisphenoidale. Among the numerous plesiomorphic characters is the presence of a splenial bone, which was unnoticed before. An updated phylogenetic analysis retrieves Nichollsemys baieri as a non-protostegid early stem chelonioid in a slightly more crownward position than Toxochelys latiremis. Our phylogeny includes macrobaenids and protostegids as pan-chelonioids, and we find unorthodox results for dermochelyids. Thus, although Nichollsemys baieri provides important new insights into the early morphological evolution of sea turtles, much work remains to be done. As a completely 3D preserved specimen, we included Nichollsemys baieri into a recent landmark-based skull shape dataset of turtles. Morphospace analysis reveals an intermediate position between cryptodires and crown chelonioids. Based on these data, we also predict that Nichollsemys baieri was still capable of neck retraction, constraining the loss of this trait to more crownward pan-chelonioids. Supplementary Information: The online version contains supplementary material available at 10.1186/s13358-024-00323-8.

A systematic comparative description of extant turtle humeri, with comments on humerus disparity and evolution based on fossil comparisons.

The humerus is central for locomotion in turtles as quadrupedal animals. Osteological variation across testudine clades remains poorly documented. Here, we systematically describe the humerus anatomy for all major extant turtle clades based on 38 species representing the phylogenetic and ecological diversity of crown turtles. Three Late Triassic species of shelled stem turtles (Testudindata) are included to establish the plesiomorphic humerus morphology. Our work is based on 3D models, establishing a publicly available digital database. Previously defined terms for anatomical sides of the humerus (e.g., dorsal, ventral) are often not aligned with the respective body sides in turtles and other quadrupedal animals with sprawling gait. We propose alternative anatomical directional terms to simplify communication: radial and ulnar (the sides articulating with the radius/ulna), capitular (the side bearing the humeral head), and intertubercular (opposite to capitular surface). Turtle humeri show low morphological variation with exceptions concentrated in locomotory specialists. We propose 15 discrete characters to summarize osteological variation for future phylogenetic studies. Disparity analyses comparing non-shelled and shelled turtles indicate that the presence of the shell constrains humerus variation. Flippered aquatic turtles are released from this constraint and significantly increase overall disparity. Ontogenetic changes of turtle humeri are related to increased ossification and pronunciation of the proximal processes, the distal articulation areas, and the closure of the ectepicondylar groove to a foramen. Some turtle species retain juvenile features into adulthood and provide evidence for paedomorphic evolution. We review major changes of turtle humerus morphology throughout the evolution of its stem group.

Independent origin of large labyrinth size in turtles.

The labyrinth of the vertebrate inner ear is a sensory system that governs the perception of head rotations. Central hypotheses predict that labyrinth shape and size are related to ecological adaptations, but this is under debate and has rarely been tested outside of mammals. We analyze the evolution of labyrinth morphology and its ecological drivers in living and fossil turtles, an understudied group that underwent multiple locomotory transitions during 230 million years of evolution. We show that turtles have unexpectedly large labyrinths that evolved during the origin of aquatic habits. Turtle labyrinths are relatively larger than those of mammals, and comparable to many birds, undermining the hypothesis that labyrinth size correlates directly with agility across vertebrates. We also find that labyrinth shape variation does not correlate with ecology in turtles, undermining the widespread expectation that reptilian labyrinth shapes convey behavioral signal, and demonstrating the importance of understudied groups, like turtles.

Cranial ecomorphology of turtles and neck retraction as a possible trigger of ecological diversification.

Turtles have a highly modified body plan, including a rigid shell that constrains postcranial anatomy. Skull morphology and neck mobility may therefore be key to ecological specialization in turtles. However, the ecological signal of turtle skull morphologies has not been rigorously evaluated, leaving uncertainties about the roles of ecological adaptation and convergence. We evaluate turtle cranial ecomorphology using three-dimensional geometric morphometrics and phylogenetic comparative methods. Skull shape correlates with allometry, neck retraction capability, and different aquatic feeding ecologies. We find that ecological variables influence skull shape only, whereas a key functional variable (the capacity for neck retraction) influences both shape and size. Ecology and functional predictions from three-dimensional shape are validated by high success rates for extant species, outperforming previous two-dimensional approaches. We use this to infer ecological and functional traits of extinct species. Neck retraction evolved among crownward stem-turtles by the Late Jurassic, signaling functional decoupling of the skull and neck from the shell, possibly linked to a major episode of ecomorphological diversification. We also find strong evidence for convergent ecological adaptations among marine groups. This includes parallel loss of neck retraction, evidence for active hunting, possible grazing, and suction feeding in extinct marine groups. Our large-scale assessment of dietary and functional adaptation throughout turtle evolution reveals the timing and origin of their distinct ecomorphologies, and highlights the potential for ecology and function to have distinct effects on skull form.

Tartarugas tem um plano corpóreo bastante modificado, que inclui um casco rígido que restringe sua anatomia pós-craniana. Portanto, a morfologia craniana e a mobilidade do pescoço devem ser centrais nas especializações ecológicas de tartarugas. No entanto, o sinal ecológico das diferentes morfologias de crânio de tartarugas não foi ainda rigorosamente avaliado, deixando incertezas sobre os papéis de adaptações ecológicas e convergência. Avaliamos a ecomorfologia craniana de tartarugas utilizando morfometria geométrica tridimensional e métodos filogenéticos comparativos. A forma craniana correlaciona com alometria, capacidade de retração do pescoço e diferentes ecologias alimentares aquáticas. Encontramos que variáveis ecológicas influenciam apenas a forma do crânio, enquanto uma importante variável funcional (a capacidade de retração do pescoço) influencia tanto a forma como o tamanho do crânio. Predições ecológicas e funcionais para espécies viventes a partir de formas tridimensionais são validadas com altas taxas de sucesso, superando abordagens bidimensionais. Utilizamos isso para inferir traços ecológicos e funcionais de espécies extintas. A retração do pescoço evoluiu em linhagens extintas mais próximas à origem do grupo-coronal durante o Jurássico Final, indicando uma dissociação funcional entre crânio e pescoço do casco, algo possivelmente ligado a um importante episódio de diversificação ecomorfológica. Também encontramos forte evidência para adaptações ecológicas convergentes em grupos marinhos. Isso inclui a perda paralela da retração do pescoço, evidência de caça ativa, alimentação por sucção, além de possível preferência por plantas aquáticas em grupos marinhos extintos. Nosso estudo de larga-escala sobre adaptações funcionais e relacionadas à dieta ao longo da evolução de tartarugas revela o tempo e origem de suas distintas ecomorfologias, e destaca ainda o potencial de ecologia e função terem efeitos distintos sobre a forma craniana.