Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy.

Endothermy underpins the ecological dominance of mammals and birds in diverse environmental settings1,2. However, it is unclear when this crucial feature emerged during mammalian evolutionary history, as most of the fossil evidence is ambiguous3-17. Here we show that this key evolutionary transition can be investigated using the morphology of the endolymph-filled semicircular ducts of the inner ear, which monitor head rotations and are essential for motor coordination, navigation and spatial awareness18-22. Increased body temperatures during the ectotherm-endotherm transition of mammal ancestors would decrease endolymph viscosity, negatively affecting semicircular duct biomechanics23,24, while simultaneously increasing behavioural activity25,26 probably required improved performance27. Morphological changes to the membranous ducts and enclosing bony canals would have been necessary to maintain optimal functionality during this transition. To track these morphofunctional changes in 56 extinct synapsid species, we developed the thermo-motility index, a proxy based on bony canal morphology. The results suggest that endothermy evolved abruptly during the Late Triassic period in Mammaliamorpha, correlated with a sharp increase in body temperature (5-9 °C) and an expansion of aerobic and anaerobic capacities. Contrary to previous suggestions3-14, all stem mammaliamorphs were most probably ectotherms. Endothermy, as a crucial physiological characteristic, joins other distinctive mammalian features that arose during this period of climatic instability28.

Antiquity of forelimb ecomorphological diversity in the mammalian stem lineage (Synapsida).

Mammals and their closest fossil relatives are unique among tetrapods in expressing a high degree of pectoral girdle and forelimb functional diversity associated with fully pelagic, cursorial, subterranean, volant, and other lifestyles. However, the earliest members of the mammalian stem lineage, the "pelycosaur"-grade synapsids, present a far more limited range of morphologies and inferred functions. The more crownward nonmammaliaform therapsids display novel forelimb morphologies that have been linked to expanded functional diversity, suggesting that the roots of this quintessentially mammalian phenotype can be traced to the pelycosaur-therapsid transition in the Permian period. We quantified morphological disparity of the humerus in pelycosaur-grade synapsids and therapsids using geometric morphometrics. We found that disparity begins to increase concurrently with the emergence of Therapsida, and that it continues to rise until the Permo-Triassic mass extinction. Further, therapsid exploration of new regions of morphospace is correlated with the evolution of novel ecomorphologies, some of which are characterized by changes to overall limb morphology. This evolutionary pattern confirms that nonmammaliaform therapsid forelimbs underwent ecomorphological diversification throughout the Permian, with functional elaboration initially being more strongly expressed in the proximal end of the humerus than the distal end. The role of the forelimbs in the functional diversification of therapsids foreshadows the deployment of forelimb morphofunctional diversity in the evolutionary radiation of mammals.

Phylogeny, function and ecology in the deep evolutionary history of the mammalian forelimb.

Mammals are the only living members of the larger clade Synapsida, which has a fossil record spanning 320 Ma. Despite the fact that much of the ecological diversity of mammals has been considered in the light of limb morphology, the ecological comparability of mammals to their fossil forerunners has not been critically assessed. Because of the wide use of limb morphology in testing ecomorphological hypothesis about extinct tetrapods, we sought: (i) to estimate when in synapsid history, modern mammals become analogues for predicting fossil ecologies; (ii) to document examples of ecomorphological convergence; and (iii) to compare the functional solutions of distinct synapsid radiations. We quantitatively compared the forelimb shapes of the multiple fossil synapsid radiations to a broad sample of extant Mammalia representing a variety of divergent locomotor ecologies. Our results indicate that each synapsid radiation explored different areas of morphospace and arrived at functional solutions that reflected their distinctive ancestral morphologies. This work counters the narrative of non-mammalian synapsid forelimb evolution as a linear progression towards more mammalian morphologies. Instead, a disparate array of early-evolving shapes subsequently contracted towards more mammal-like forms.

Living fast in the Triassic: New data on life history in Lystrosaurus (Therapsida: Dicynodontia) from northeastern Pangea.

Lystrosaurus was one of the few tetrapods to survive the Permo-Triassic mass extinction, the most profound biotic crisis in Earth's history. The wide paleolatitudinal range and high abundance of Lystrosaurus during the Early Triassic provide a unique opportunity to investigate changes in growth dynamics and longevity following the mass extinction, yet most studies have focused only on species that lived in the southern hemisphere. Here, we present the long bone histology from twenty Lystrosaurus skeletal elements spanning a range of sizes that were collected in the Jiucaiyuan Formation of northwestern China. In addition, we compare the average body size of northern and southern Pangean Triassic-aged species and conduct cranial geometric morphometric analyses of southern and northern taxa to begin investigating whether specimens from China are likely to be taxonomically distinct from South African specimens. We demonstrate that Lystrosaurus from China have larger average body sizes than their southern Pangean relatives and that their cranial morphologies are distinctive. The osteohistological examination revealed sustained, rapid osteogenesis punctuated by growth marks in some, but not all, immature individuals from China. We find that the osteohistology of Chinese Lystrosaurus shares a similar growth pattern with South African species that show sustained growth until death. However, bone growth arrests more frequently in the Chinese sample. Nevertheless, none of the long bones sampled here indicate that maximum or asymptotic size was reached, suggesting that the maximum size of Lystrosaurus from the Jiucaiyuan Formation remains unknown.

Effects of taphonomic deformation on geometric morphometric analysis of fossils: a study using the dicynodont Diictodon feliceps (Therapsida, Anomodontia).

Taphonomic deformation, the distortion of fossils as a result of geological processes, poses problems for the use of geometric morphometrics in addressing paleobiological questions. Signal from biological variation, such as ontogenetic trends and sexual dimorphism, may be lost if variation from deformation is too high. Here, we investigate the effects of taphonomic deformation on geometric morphometric analyses of the abundant, well known Permian therapsid Diictodon feliceps. Distorted Diictodon crania can be categorized into seven typical styles of deformation: lateral compression, dorsoventral compression, anteroposterior compression, "saddle-shape" deformation (localized collapse at cranial mid-length), anterodorsal shear, anteroventral shear, and right/left shear. In simulated morphometric datasets incorporating known "biological" signals and subjected to uniform shear, deformation was typically the main source of variance but accurate "biological" information could be recovered in most cases. However, in empirical datasets, not only was deformation the dominant source of variance, but little structure associated with allometry and sexual dimorphism was apparent, suggesting that the more varied deformation styles suffered by actual fossils overprint biological variation. In a principal component analysis of all anomodont therapsids, deformed Diictodon specimens exhibit significant dispersion around the "true" position of this taxon in morphospace based on undistorted specimens. The overall variance associated with deformation for Anomodontia as a whole is minor, and the major axes of variation in the study sample show a strong phylogenetic signal instead. Although extremely problematic for studying variation in fossil taxa at lower taxonomic levels, the cumulative effects of deformation in this study are shown to be random, and inclusion of deformed specimens in higher-level analyses of morphological disparity are warranted. Mean morphologies of distorted specimens are found to approximate the morphology of undistorted specimens, so we recommend use of species-level means in higher-level analyses when possible.