Finite element analysis of kangaroo astragali: A new angle on the ankle.

Using finite element analysis on the astragali of five macropodine kangaroos (extant and extinct hoppers) and three sthenurine kangaroos (extinct proposed bipedal striders) we investigate how the stresses experienced by the ankle in similarly sized kangaroos of different hypothesized/known locomotor strategy compare under different simulation scenarios, intended to represent the moment of midstance at different gaits. These tests showed a clear difference between the performance of sthenurines and macropodines with the former group experiencing lower stress in simulated bipedal strides in all species compared with hopping simulations, supporting the hypothesis that sthenurines may have utilized this gait. The Pleistocene macropodine Protemnodon also performed differently from all other species studied, showing high stresses in all simulations except for bounding. This may support the hypothesis of Protemnodon being a quadrupedal bounder.

Who was the real sabertooth predator: Thylacosmilus or Thylacoleo?

Sabertoothed mammalian predators, all now extinct, were almost exclusively feloid carnivorans (Eutheria, Placentalia): here a couple of extinct metatherian predators are considered in comparison with the placental sabertooths. Thylacosmilus (the "marsupial sabertooth") and Thylacoleo (the "marsupial lion") were both relatively large (puma-sized) carnivores of the Plio-Pleistocene in the Southern Hemisphere (Argentina and Australia, respectively). Both carnivores have captured the public imagination, especially as predators that were somehow analogous to northern placental forms. But a more detailed consideration of their morphology shows that neither can be simply analogized with its supposed placental counterpart. While Thylacosmilus did indeed have saber-like canines, many aspects of its anatomy show that it could not have killed prey in the manner proposed for the sabertoothed felids such as Smilodon. Rather than being an active predator, it may have been a specialized scavenger, using the hypertrophied canines to open carcasses, and perhaps deployed a large tongue to extract the innards. Thylacoleo lacked canines, and its supposedly "caniniform" incisors could not have acted like a felid's canines. Nevertheless, while its mode of dispatching its prey remains a subject for debate, it was clearly a powerful predator, likely to be capable of bringing down prey bigger than itself while hunting alone. In that regard, it may have filled the ecomorphological role proposed for placental sabertooths, and so despite the lack of canines can be nominated as the true "marsupial sabertooth" out of the two extinct taxa.

A timescale for placental mammal diversification based on Bayesian modeling of the fossil record.

The timing of the placental mammal radiation has been the focus of debate over the efficacy of competing methods for establishing evolutionary timescales. Molecular clock analyses estimate that placental mammals originated before the Cretaceous-Paleogene (K-Pg) mass extinction, anywhere from the Late Cretaceous to the Jurassic. However, the absence of definitive fossils of placentals before the K-Pg boundary is compatible with a post-Cretaceous origin. Nevertheless, lineage divergence must occur before it can be manifest phenotypically in descendent lineages. This, combined with the non-uniformity of the rock and fossil records, requires the fossil record to be interpreted rather than read literally. To achieve this, we introduce an extended Bayesian Brownian bridge model that estimates the age of origination and, where applicable, extinction through a probabilistic interpretation of the fossil record. The model estimates the origination of placentals in the Late Cretaceous, with ordinal crown groups originating at or after the K-Pg boundary. The results reduce the plausible interval for placental mammal origination to the younger range of molecular clock estimates. Our findings support both the Long Fuse and Soft Explosive models of placental mammal diversification, indicating that the placentals originated shortly prior to the K-Pg mass extinction. The origination of many modern mammal lineages overlapped with and followed the K-Pg mass extinction.

Hipparion tracks and horses' toes: the evolution of the equid single hoof.

The traditional story of the evolution of the horse (family Equidae) has been in large part about the evolution of their feet. How did modern horses come to have a single toe (digit III), with the hoof bearing a characteristic V-shaped keratinous frog on the sole, and what happened to the other digits? While it has long been known that the proximal portions of digits II and IV are retained as the splint bones, a recent hypothesis suggested that the distal portion of these digits have also been retained as part of the frog, drawing upon the famous Laetoli footprints of the tridactyl (three-toed) equid Hipparion as part of the evidence. We show here that, while there is good anatomical and embryological evidence for the proximal portions of all the accessory digits (i.e. I and V, as well as II and IV) being retained in the feet of modern horses, evidence is lacking for the retention of any distal portions of these digits. There is also good ichnological evidence that many tridactyl equids possessed a frog, and that the frog has been part of the equid foot for much of equid evolutionary history.

Divergent locomotor evolution in "giant" kangaroos: Evidence from foot bone bending resistances and microanatomy.

The extinct sthenurine (giant, short-faced) kangaroos have been proposed to have a different type of locomotor behavior to extant (macropodine) kangaroos, based both on physical limitations (the size of many exceeds the proposed limit for hopping) and anatomical features (features of the hind limb anatomy suggestive of weight-bearing on one leg at a time). Here, we use micro computerised tomography (micro-CT) scans of the pedal bones of six kangaroos, three sthenurine, and three macropodine, ranging from ~50 to 150 kg, to investigate possible differences in bone resistances to bending and cortical bone distribution that might relate to differences in locomotion. Using second moment of area analysis, we show differences in resistance to bending between the two subfamilies. Distribution of cortical bone shows that sthenurines had less resistant calcaneal tubers, implying a different foot posture during locomotion, and the long foot bones were more resistant to the medial bending stresses. These differences were the most pronounced between Pleistocene monodactyl sthenurines (Sthenurus stirlingi and Procoptodon browneorum) and the two species of Macropus (the extant M. giganteus and the extinct M. cf. M. titan) and support the hypothesis that these derived sthenurines employed bipedal striding. The Miocene sthenurine Hadronomas retains some more macropodine-like features of bone resistance to bending, perhaps reflecting its retention of the fifth pedal digit. The Pleistocene macropodine Protemnodon has a number of unique features, possibly indicative of a type of locomotion unlike the other kangaroos.

Jaw shape and mechanical advantage are indicative of diet in Mesozoic mammals.

Jaw morphology is closely linked to both diet and biomechanical performance, and jaws are one of the most common Mesozoic mammal fossil elements. Knowledge of the dietary and functional diversity of early mammals informs on the ecological structure of palaeocommunities throughout the longest era of mammalian evolution: the Mesozoic. Here, we analyse how jaw shape and mechanical advantage of the masseter (MAM) and temporalis (MAT) muscles relate to diet in 70 extant and 45 extinct mammals spanning the Late Triassic-Late Cretaceous. In extant mammals, jaw shape discriminates well between dietary groups: insectivores have long jaws, carnivores intermediate to short jaws, and herbivores have short jaws. Insectivores have low MAM and MAT, carnivores have low MAM and high MAT, and herbivores have high MAM and MAT. These traits are also informative of diet among Mesozoic mammals (based on previous independent determinations of diet) and set the basis for future ecomorphological studies.

Postcranial elements of small mammals as indicators of locomotion and habitat.

Many studies have shown a correlation between postcranial anatomy and locomotor behavior in mammals, but the postcrania of small mammals (<5 kg) is often considered to be uninformative of their mode of locomotion due to their more generalized overall anatomy. Such small body size was true of all mammals during the Mesozoic. Anatomical correlates of locomotor behavior are easier to determine in larger mammals, but useful information can be obtained from the smaller ones. Limb bone proportions (e.g., brachial index) can be useful locomotor indicators; but complete skeletons, or even complete long bones, are rare for Mesozoic mammals, although isolated articular surfaces are often preserved. Here we examine the correlation of the morphology of long bone joint anatomy (specifically articular surfaces) and locomotor behavior in extant small mammals and demonstrate that such anatomy may be useful for determining the locomotor mode of Mesozoic mammals, at least for the therian mammals.

Perissodactyl diversities and responses to climate changes as reflected by dental homogeneity during the Cenozoic in Asia.

Cenozoic mammal evolution and faunal turnover are considered to have been influenced and triggered by global climate change. Teeth of large terrestrial ungulates are reliable proxies to trace long-term climatic changes due to their morphological and physicochemical properties; however, the role of premolar molarization in ungulate evolution and related climatic change has rarely been investigated. Recently, three patterns of premolar molarization among perissodactyls have been recognized: endoprotocrista-derived hypocone (type I); paraconule-protocone separation (type II); and metaconule-derived pseudohypocone (type III). These three patterns of premolar molarization play an important role in perissodactyl diversity coupled with global climate change during the Cenozoic in Asia. Those groups with a relatively higher degree of premolar molarization, initiated by the formation of the hypocone, survived into Neogene, whereas those with a lesser degree of molarization, initiated by the deformation of existing ridges and cusps, went extinct by the end of the Oligocene. In addition, the hypothesis of the "Ulan Gochu Decline" is proposed here to designate the most conspicuous decrease of perissodactyl diversity that occurred in the latest middle Eocene rather than at the Eocene-Oligocene transition in Asia, as conventionally thought; this event was likely comparable to the contemporaneous post-Uintan decline of the North American land fauna.

An eye for a tooth: Thylacosmilus was not a marsupial "saber-tooth predator".

BACKGROUND: Saber-toothed mammals, now all extinct, were cats or "cat-like" forms with enlarged, blade-like upper canines, proposed as specialists in taking large prey. During the last 66 Ma, the saber-tooth ecomorph has evolved convergently at least in five different mammalian lineages across both marsupials and placentals. Indeed, Thylacosmilus atrox, the so-called "marsupial saber-tooth," is often considered as a classic example of convergence with placental saber-tooth cats such as Smilodon fatalis. However, despite its superficial similarity to saber-toothed placentals, T. atrox lacks many of the critical anatomical features related to their inferred predatory behavior-that of employing their enlarged canines in a killing head strike. METHODS: Here we follow a multi-proxy approach using canonical correspondence analysis of discrete traits, biomechanical models of skull function using Finite Element Analysis, and 3D dental microwear texture analysis of upper and lower postcanine teeth, to investigate the degree of evolutionary convergence between T. atrox and placental saber-tooths, including S. fatalis. RESULTS: Correspondence analysis shows that the craniodental features of T. atrox are divergent from those of placental saber-tooths. Biomechanical analyses indicate a superior ability of T. atrox to placental saber-tooths in pulling back with the canines, with the unique lateral ridge of the canines adding strength to this function. The dental microwear of T. atrox indicates a soft diet, resembling that of the meat-specializing cheetah, but its blunted gross dental wear is not indicative of shearing meat. CONCLUSIONS: Our results indicate that despite its impressive canines, the "marsupial saber-tooth" was not the ecological analogue of placental saber-tooths, and likely did not use its canines to dispatch its prey. This oft-cited example of convergence requires reconsideration, and T. atrox may have had a unique type of ecology among mammals.

Palaeophysiology of pH regulation in tetrapods.

The involvement of mineralized tissues in acid-base homeostasis was likely important in the evolution of terrestrial vertebrates. Extant reptiles encounter hypercapnia when submerged in water, but early tetrapods may have experienced hypercapnia on land due to their inefficient mode of lung ventilation (likely buccal pumping, as in extant amphibians). Extant amphibians rely on cutaneous carbon dioxide elimination on land, but early tetrapods were considerably larger forms, with an unfavourable surface area to volume ratio for such activity, and evidence of a thick integument. Consequently, they would have been at risk of acidosis on land, while many of them retained internal gills and would not have had a problem eliminating carbon dioxide in water. In extant tetrapods, dermal bone can function to buffer the blood during acidosis by releasing calcium and magnesium carbonates. This review explores the possible mechanisms of acid-base regulation in tetrapod evolution, focusing on heavily armoured, basal tetrapods of the Permo-Carboniferous, especially the physiological challenges associated with the transition to air-breathing, body size and the adoption of active lifestyles. We also consider the possible functions of dermal armour in later tetrapods, such as Triassic archosaurs, inferring palaeophysiology from both fossil record evidence and phylogenetic patterns, and propose a new hypothesis relating the archosaurian origins of the four-chambered heart and high systemic blood pressures to the perfusion of the osteoderms. This article is part of the theme issue 'Vertebrate palaeophysiology'.

Sixty-six million years along the road of mammalian ecomorphological specialization.

The fossil record of the large terrestrial mammals of the North American Cenozoic has previously been quantitatively summarized in six sequential episodes of faunal associations-"evolutionary faunas"-that correspond well with previously proposed qualitative "Chronofaunas." Here, we investigate the ecological spectrum of these faunas by classifying their major taxonomic components into discrete ecomorphological categories of diet, locomotion, and body size. To specifically address the potential influence of long-term climatic shifts on the ecomorphological composition of these faunas, we analyze via contingency tables and detrended correspondence analyses the frequency distribution of ecomorph types within faunas. We show that each evolutionary fauna has a unique, nonrandom association of ecomorphs, and we identify a long-term trend toward greater ecomorphological specialization over successive faunas during the past 66 My. Major vegetation shifts induced by climatic changes appear to underlie the ecomorphological dynamics of these six temporal associations that summarize Cenozoic North American mammalian evolutionary history.

The phylogenetic signal in tooth wear: What does it mean?

A new study by Fraser et al (2018) urges the use of phylogenetic comparative methods, whenever possible, in analyses of mammalian tooth wear. We are concerned about this for two reasons. First, this recommendation may mislead the research community into thinking that phylogenetic signal is an artifact of some sort rather than a fundamental outcome of the evolutionary process. Secondly, this recommendation may set a precedent for editors and reviewers to enforce phylogenetic adjustment where it may unnecessarily weaken or even directionally alter the results, shifting the emphasis of analysis from common patterns manifested by large clades to rare cases.

Correlates between calcaneal morphology and locomotion in extant and extinct carnivorous mammals.

Locomotor mode is an important component of an animal's ecology, relating to both habitat and substrate choice (e.g., arboreal versus terrestrial) and in the case of carnivores, to mode of predation (e.g., ambush versus pursuit). Here, we examine how the morphology of the calcaneum, the 'heel bone' in the tarsus, correlates with locomotion in extant carnivores. Other studies have confirmed the correlation of calcaneal morphology with locomotion behaviour and habitat. The robust nature of the calcaneum means that it is frequently preserved in the fossil record. Here, we employ linear measurements and 2D-geometric morphometrics on a sample of calcanea from eighty-seven extant carnivorans and demonstrate a signal of correlation between calcaneal morphology and locomotor mode that overrides phylogeny. We used this correlation to determine the locomotor mode, and hence aspects of the palaeobiology of, 47 extinct carnivorous mammal taxa, including both Carnivora and Creodonta. We found ursids (bears), clustered together, separate from the other carnivorans. Our results support greater locomotor diversity for nimravids (the extinct 'false sabertooths', usually considered to be more arboreal), than previously expected. However, there are limitations to interpretation of extinct taxa because their robust morphology is not fully captured in the range of modern carnivoran morphology.

Mammal body size evolution in North America and Europe over 20 Myr: similar trends generated by different processes.

Because body size interacts with many fundamental biological properties of a species, body size evolution can be an essential component of the generation and maintenance of biodiversity. Here we investigate how body size evolution can be linked to the clade-specific diversification dynamics in different geographical regions. We analyse an extensive body size dataset of Neogene large herbivores (covering approx. 50% of the 970 species in the orders Artiodactyla and Perissodactyla) in Europe and North America in a Bayesian framework. We reconstruct the temporal patterns of body size in each order on each continent independently, and find significant increases of minimum size in three of the continental assemblages (except European perissodactyls), suggesting an active selection for larger bodies. Assessment of trait-correlated birth-death models indicates that the common trend of body size increase is generated by different processes in different clades and regions. Larger-bodied artiodactyl species on both continents tend to have higher origination rates, and both clades in North America show strong links between large bodies and low extinction rate. Collectively, our results suggest a strong role of species selection and perhaps of higher-taxon sorting in driving body size evolution, and highlight the value of investigating evolutionary processes in a biogeographic context.

Twenty-million-year relationship between mammalian diversity and primary productivity.

At global and regional scales, primary productivity strongly correlates with richness patterns of extant animals across space, suggesting that resource availability and climatic conditions drive patterns of diversity. However, the existence and consistency of such diversity-productivity relationships through geological history is unclear. Here we provide a comprehensive quantitative test of the diversity-productivity relationship for terrestrial large mammals through time across broad temporal and spatial scales. We combine >14,000 occurrences for 690 fossil genera through the Neogene (23-1.8 Mya) with regional estimates of primary productivity from fossil plant communities in North America and Europe. We show a significant positive diversity-productivity relationship through the 20-million-year record, providing evidence on unprecedented spatial and temporal scales that this relationship is a general pattern in the ecology and paleo-ecology of our planet. Further, we discover that genus richness today does not match the fossil relationship, suggesting that a combination of human impacts and Pleistocene climate variability has modified the 20-million-year ecological relationship by strongly reducing primary productivity and driving many mammalian species into decline or to extinction.

Mountain uplift explains differences in Palaeogene patterns of mammalian evolution and extinction between North America and Europe.

Patterns of late Palaeogene mammalian evolution appear to be very different between Eurasia and North America. Around the Eocene-Oligocene (EO) transition global temperatures in the Northern Hemisphere plummet: following this, European mammal faunas undergo a profound extinction event (the Grande Coupure), while in North America they appear to pass through this temperature event unscathed. Here, we investigate the role of surface uplift to environmental change and mammalian evolution through the Palaeogene (66-23 Ma). Palaeogene regional surface uplift in North America caused large-scale reorganization of precipitation patterns, particularly in the continental interior, in accord with our combined stable isotope and ecometric data. Changes in mammalian faunas reflect that these were dry and high-elevation palaeoenvironments. The scenario of Middle to Late Eocene (50-37 Ma) surface uplift, together with decreasing precipitation in higher-altitude regions of western North America, explains the enigma of the apparent lack of the large-scale mammal faunal change around the EO transition that characterized western Europe. We suggest that North American mammalian faunas were already pre-adapted to cooler and drier conditions preceding the EO boundary, resulting from the effects of a protracted history of surface uplift.

Continuously growing rodent molars result from a predictable quantitative evolutionary change over 50 million years.

The fossil record is widely informative about evolution, but fossils are not systematically used to study the evolution of stem-cell-driven renewal. Here, we examined evolution of the continuous growth (hypselodonty) of rodent molar teeth, which is fuelled by the presence of dental stem cells. We studied occurrences of 3,500 North American rodent fossils, ranging from 50 million years ago (mya) to 2 mya. We examined changes in molar height to determine whether evolution of hypselodonty shows distinct patterns in the fossil record, and we found that hypselodont taxa emerged through intermediate forms of increasing crown height. Next, we designed a Markov simulation model, which replicated molar height increases throughout the Cenozoic and, moreover, evolution of hypselodonty. Thus, by extension, the retention of the adult stem cell niche appears to be a predictable quantitative rather than a stochastic qualitative process. Our analyses predict that hypselodonty will eventually become the dominant phenotype.

Locomotion in extinct giant kangaroos: were sthenurines hop-less monsters?

Sthenurine kangaroos (Marsupialia, Diprotodontia, Macropodoidea) were an extinct subfamily within the family Macropodidae (kangaroos and rat-kangaroos). These "short-faced browsers" first appeared in the middle Miocene, and radiated in the Plio-Pleistocene into a diversity of mostly large-bodied forms, more robust than extant forms in their build. The largest (Procoptodon goliah) had an estimated body mass of 240 kg, almost three times the size of the largest living kangaroos, and there is speculation whether a kangaroo of this size would be biomechanically capable of hopping locomotion. Previously described aspects of sthenurine anatomy (specialized forelimbs, rigid lumbar spine) would limit their ability to perform the characteristic kangaroo pentapedal walking (using the tail as a fifth limb), an essential gait at slower speeds as slow hopping is energetically unfeasible. Analysis of limb bone measurements of sthenurines in comparison with extant macropodoids shows a number of anatomical differences, especially in the large species. The scaling of long bone robusticity indicates that sthenurines are following the "normal" allometric trend for macropodoids, while the large extant kangaroos are relatively gracile. Other morphological differences are indicative of adaptations for a novel type of locomotor behavior in sthenurines: they lacked many specialized features for rapid hopping, and they also had anatomy indicative of supporting their body with an upright trunk (e.g., dorsally tipped ischiae), and of supporting their weight on one leg at a time (e.g., larger hips and knees, stabilized ankle joint). We propose that sthenurines adopted a bipedal striding gait (a gait occasionally observed in extant tree-kangaroos): in the smaller and earlier forms, this gait may have been employed as an alternative to pentapedal locomotion at slower speeds, while in the larger Pleistocene forms this gait may have enabled them to evolve to body sizes where hopping was no longer a feasible form of more rapid locomotion.

Forelimb anatomy and the discrimination of the predatory behavior of carnivorous mammals: the thylacine as a case study.

Carnivorous mammals use their forelimbs in different ways to capture their prey. Most terrestrial carnivores have some cursorial (running) adaptations, but ambush predators retain considerable flexibility in their forelimb movement, important for grappling with their prey. In contrast, predators that rely on pursuit to run down their prey have sacrificed some of this flexibility for locomotor efficiency, in the greater restriction of the forelimb motion to the parasagittal plane. In this article, we measured aspects of the forelimb anatomy (44 linear measurements) in 36 species of carnivorous mammals of known predatory behavior, and used multivariate analyses to investigate how well the forelimb anatomy reflects the predatory mode (ambush, pursuit, or pounce-pursuit). A prime intention of this study was to establish morphological correlates of behavior that could then be applied to fossil mammals: for this purpose, five individuals of the recently extinct thylacine (Thylacinus cynocephalus) were also included as unknowns. We show that the three different types of predators can be distinguished by their morphology, both in analyses where all the forelimb bones are included together, and in the separate analyses of each bone individually. Of particular interest is the ability to distinguish between the two types of more cursorial predators, pursuit and pounce-pursuit, which have previously been considered as primarily size-based categories. Despite a prior consideration of the thylacine as a "pounce-pursuit" or an "ambush" type of predator, the thylacines did not consistently cluster with any type of predatory carnivores in our analyses. Rather, the thylacines appeared to be more generalized in their morphology than any of the extant carnivores. The absence of a large diversity of large carnivorous mammals in Australia, past and present, may explain the thylacine's generalized morphology.

Dermal bone in early tetrapods: a palaeophysiological hypothesis of adaptation for terrestrial acidosis.

The dermal bone sculpture of early, basal tetrapods of the Permo-Carboniferous is unlike the bone surface of any living vertebrate, and its function has long been obscure. Drawing from physiological studies of extant tetrapods, where dermal bone or other calcified tissues aid in regulating acid-base balance relating to hypercapnia (excess blood carbon dioxide) and/or lactate acidosis, we propose a similar function for these sculptured dermal bones in early tetrapods. Unlike the condition in modern reptiles, which experience hypercapnia when submerged in water, these animals would have experienced hypercapnia on land, owing to likely inefficient means of eliminating carbon dioxide. The different patterns of dermal bone sculpture in these tetrapods largely correlates with levels of terrestriality: sculpture is reduced or lost in stem amniotes that likely had the more efficient lung ventilation mode of costal aspiration, and in small-sized stem amphibians that would have been able to use the skin for gas exchange.