The influence of the land-to-sea macroevolutionary transition on vertebral column disparification in Pinnipedia.

The repeated returns of vertebrates to the marine ecosystems since the Triassic serve as an evolutionary model to understand macroevolutionary change. Here we investigate the effects of the land-to-sea transition on disparity and constraint of the vertebral column in aquatic carnivorans (Carnivora; Pinnipedia) to assess how their functional diversity and evolutionary innovations influenced major radiations of crown pinnipeds. We use three-dimensional geometric morphometrics and multivariate analysis for high-dimensional data under a phylogenetic framework to quantify vertebral size and shape in living and extinct pinnipeds. Our analysis demonstrates an important shift in vertebral column evolution by 10-12 million years ago, from an unconstrained to a constrained evolutionary scenario, a point of time that coincides with the major radiation of crown pinnipeds. Moreover, we also demonstrate that the axial skeleton of phocids and otariids followed a different path of morphological evolution that was probably driven by their specialized locomotor strategies. Despite this, we found a significant effect of habitat preference (coastal versus pelagic) on vertebral morphology of crown taxa regardless of the family they belong. In summary, our analysis provides insights into how the land-to-sea transition influenced the complex evolutionary history of pinniped vertebral morphology.

Evolutionary ecomorphology for the twenty-first century: examples from mammalian carnivores.

Carnivores (cats, dogs and kin) are a diverse group of mammals that inhabit a remarkable range of ecological niches. While the relationship between ecology and morphology has long been of interest in carnivorans, the application of quantitative techniques has resulted in a recent explosion of work in the field. Therefore, they provide a case study of how quantitative techniques, such as geometric morphometrics (GMM), have impacted our ability to tease apart complex ecological signals from skeletal anatomy, and the implications for our understanding of the relationships between form, function and ecological specialization. This review provides a synthesis of current research on carnivoran ecomorphology, with the goal of illustrating the complex interaction between ecology and morphology in the skeleton. We explore the ecomorphological diversity across major carnivoran lineages and anatomical systems. We examine cranial elements (skull, sensory systems) and postcranial elements (limbs, vertebral column) to reveal mosaic patterns of adaptation related to feeding and hunting strategies, locomotion and habitat preference. We highlight the crucial role that new approaches have played in advancing our understanding of carnivoran ecomorphology, while addressing challenges that remain in the field, such as ecological classifications, form-function relationships and multi-element analysis, offering new avenues for future research.

The impact of the land-to-sea transition on evolutionary integration and modularity of the pinniped backbone.

In this study, we investigate how the terrestrial-aquatic transition influenced patterns of axial integration and modularity in response to the secondary adaptation to a marine lifestyle. We use 3D geometric morphometrics to quantify shape covariation among presacral vertebrae in pinnipeds (Carnivora; Pinnipedia) and to compare with patterns of axial integration and modularity in their close terrestrial relatives. Our results indicate that the vertebral column of pinnipeds has experienced a decrease in the strength of integration among all presacral vertebrae when compared to terrestrial carnivores (=fissipeds). However, separate integration analyses among the speciose Otariidae (i.e., sea lions and fur seals) and Phocidae (i.e., true seals) also suggests the presence of different axial organizations in these two groups of crown pinnipeds. While phocids present a set of integrated "thoracic" vertebrae, the presacral vertebrae of otariids are characterized by the absence of any set of vertebrae with high integration. We hypothesize that these differences could be linked to their specific modes of aquatic locomotion -i.e., pelvic vs pectoral oscillation. Our results provide evidence that the vertebral column of pinnipeds has been reorganized from the pattern observed in fissipeds but is more complex than a simple "homogenization" of the modular pattern of their close terrestrial relatives.

Function of revolute zygapophyses in the lumbar vertebrae of early placental mammals.

The unique morphology of mammalian lumbar vertebrae allows the spine to flex and extend in the sagittal plane during locomotion. This movement increases stride length and allows mammals to efficiently breathe while running with an asymmetric gait. In extant mammals, the amount of flexion that occurs varies across different locomotor styles, with dorsostable runners relying more on movement of long limbs to run and dorsomobile runners incorporating more flexion of the back. Although long limbs and a stabilized lumbar region are commonly associated with each other in extant mammals, many "archaic" placental mammals with short limbs had lumbar vertebrae with revolute zygapophyses. These articulations with an interlocking S-shape are found only in artiodactyls among extant mammals and have been hypothesized to stabilize against flexion of the back. This would suggest that archaic placental mammals may not have incorporated dorsoventral flexion into locomotion to the same extent as extant mammals with similar proportions. We tested the relative mobility of fossil lumbar vertebrae from two early placental mammals, the creodonts Patriofelis and Limnocyon, to see how these vertebrae may have functioned. We compared range of motion (ROM) between the original vertebrae, with revolute morphology and digitally altered vertebrae with a flat morphology. We found that the revolute morphology had relatively little effect on dorsoventral flexion and instead that it likely prevented disarticulation due to shear forces on the spine. These results show that flexion of the spine has been an important part of mammalian locomotion for at least 50 million years.

Increase in infected corneal ulcerations in dogs during the northern Colorado's 2020 wildfire season.

OBJECTIVE: In the fall of 2020, Colorado experienced the two largest wildfires in state history. The smoke blanketed the college town of Fort Collins, Colorado, the location of the Veterinary Teaching Hospital at Colorado State University (CSU-VTH). The objective for this cross-sectional observational study was to evaluate how these wildfires and the corresponding elevated air quality index (AQI)) was associated with infected corneal ulcerations in dogs when compared to the two previous years. ANIMALS: Seventeen dogs were included in this study. PROCEDURES: Medical records from dogs presented to the CSU-VTH ophthalmology service with infected corneal ulcerations in August, September, and October of 2020, 2019, and 2018 were evaluated. Only corneal ulcerations with growth on their microbial cultures were included in this study. RESULTS: The study revealed a significant increase in prevalence of infected corneal ulcerations in dogs presented to the CSU-VTH during the three wildfire months of 2020 that is, 3.5% (9/255) when compared with the two previous years, 2019: 1.0% (4/383, p = 0.04), and 2018: 0.9% (4/457) (p = .01). The AQI (mean ± standard error) was also significantly elevated for dogs that presented with infected corneal ulcerations in 2020 (70.2 ± 5.8) compared with 2019 (19.7 ± 8.7) and 2018 (45.6 ± 8.7) (p < .01). CONCLUSIONS AND CLINICAL RELEVANCE: Elevation of AQI from wildfires seems to be correlated with an increased prevalence of infected corneal ulceration in dogs. As the duration and frequency of wildfires continues to rise globally, the effects of these wildfires on animal health should be investigated further.

Size and shape regional differentiation during the development of the spine in the nine-banded armadillo (Dasypus novemcinctus).

Xenarthrans (armadillos, anteaters, sloths, and their extinct relatives) are unique among mammals in displaying a distinctive specialization of the posterior trunk vertebrae-supernumerary vertebral xenarthrous articulations. This study seeks to understand how xenarthry develops through ontogeny and if it may be constrained to appear within pre-existing vertebral regions. Using three-dimensional geometric morphometrics on the neural arches of vertebrae, we explore phenotypic, allometric, and disparity patterns of the different axial morphotypes during the ontogeny of nine-banded armadillos. Shape-based regionalization analyses showed that the adult thoracolumbar column is divided into three regions according to the presence or absence of ribs and the presence or absence of xenarthrous articulations. A three-region division was retrieved in almost all specimens through development, although younger stages (e.g., fetuses, neonates) have more region boundary variability. In size-based regionalization analyses, thoracolumbar vertebrae are separated into two regions: a prediaphragmatic, prexenarthrous region, and a postdiaphragmatic xenarthrous region. We show that posterior thoracic vertebrae grow at a slower rate, while anterior thoracics and lumbars grow at a faster rate relatively, with rates decreasing anteroposteriorly in the former and increasing anteroposteriorly in the latter. We propose that different proportions between vertebrae and vertebral regions might result from differences in growth pattern and timing of ossification.

Adaptive landscapes challenge the "lateral-to-sagittal" paradigm for mammalian vertebral evolution.

The evolution of mammals from their extinct forerunners, the non-mammalian synapsids, is one of the most iconic locomotor transitions in the vertebrate fossil record. In the limb skeleton, the synapsid-mammal transition is traditionally characterized by a shift from a sprawling limb posture, resembling that of extant reptiles and amphibians, to more adducted limbs, as seen in modern-day mammals. Based on proposed postural similarities between early synapsids and extant reptiles, this change is thought to be accompanied by a shift from ancestral reptile-like lateral bending to mammal-like sagittal bending of the vertebral column. To test this "lateral-to-sagittal" evolutionary paradigm, we used combinatorial optimization to produce functionally informed adaptive landscapes and determined the functional trade-offs associated with evolutionary changes in vertebral morphology. We show that the synapsid adaptive landscape is different from both extant reptiles and mammals, casting doubt on the reptilian model for early synapsid axial function, or indeed for the ancestral condition of amniotes more broadly. Further, the synapsid-mammal transition is characterized by not only increasing sagittal bending in the posterior column but also high stiffness and increasing axial twisting in the anterior column. Therefore, we refute the simplistic lateral-to-sagittal hypothesis and instead suggest the synapsid-mammal locomotor transition involved a more complex suite of functional changes linked to increasing regionalization of the backbone. These results highlight the importance of fossil taxa for understanding major evolutionary transitions.

Regionalization of the axial skeleton predates functional adaptation in the forerunners of mammals.

The evolution of semi-independent modules is hypothesized to underlie the functional diversification of serially repeating (metameric) structures. The mammal vertebral column is a classic example of a metameric structure that is both modular, with well-defined morphological regions, and functionally differentiated. How the evolution of regions is related to their functional differentiation in the forerunners of mammals remains unclear. Here we gathered morphometric and biomechanical data on the presacral vertebrae of two extant species that bracket the synapsid-mammal transition and use the relationship between form and function to predict functional differentiation in extinct non-mammalian synapsids. The origin of vertebral functional diversity does not correlate with the evolution of new regions but appears late in synapsid evolution. This decoupling of regions from functional diversity implies that an adaptive trigger is needed to exploit existing modularity. We propose that the release of axial respiratory constraints, combined with selection for novel mammalian behaviours in Late Triassic cynodonts, drove the functional divergence of pre-existing morphological regions.

Author Correction: Regionalization of the axial skeleton predates functional adaptation in the forerunners of mammals.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Stepwise shifts underlie evolutionary trends in morphological complexity of the mammalian vertebral column.

A fundamental concept in evolutionary biology is that life tends to become more complex through geologic time, but empirical examples of this phenomenon are controversial. One debate is whether increasing complexity is the result of random variations, or if there are evolutionary processes which actively drive its acquisition, and if these processes act uniformly across clades. The mammalian vertebral column provides an opportunity to test these hypotheses because it is composed of serially-repeating vertebrae for which complexity can be readily measured. Here we test seven competing hypotheses for the evolution of vertebral complexity by incorporating fossil data from the mammal stem lineage into evolutionary models. Based on these data, we reject Brownian motion (a random walk) and uniform increasing trends in favor of stepwise shifts for explaining increasing complexity. We hypothesize that increased aerobic capacity in non-mammalian cynodonts may have provided impetus for increasing vertebral complexity in mammals.

Adaptation and constraint in the evolution of the mammalian backbone.

BACKGROUND: The axial skeleton consists of repeating units (vertebrae) that are integrated through their development and evolution. Unlike most tetrapods, vertebrae in the mammalian trunk are subdivided into distinct thoracic and lumbar modules, resulting in a system that is constrained in terms of count but highly variable in morphology. This study asks how thoracolumbar regionalization has impacted adaptation and evolvability across mammals. Using geometric morphometrics, we examine evolutionary patterns in five vertebral positions from diverse mammal species encompassing a broad range of locomotor ecologies. We quantitatively compare the effects of phylogenetic and allometric constraints, and ecological adaptation between regions, and examine their impact on evolvability (disparity and evolutionary rate) of serially-homologous vertebrae. RESULTS: Although phylogenetic signal and allometry are evident throughout the trunk, the effect of locomotor ecology is partitioned between vertebral positions. Lumbar vertebral shape correlates most strongly with ecology, differentiating taxa based on their use of asymmetric gaits. Similarly, disparity and evolutionary rates are also elevated posteriorly, indicating a link between the lumbar region, locomotor adaptation, and evolvability. CONCLUSION: Vertebral regionalization in mammals has facilitated rapid evolution of the posterior trunk in response to selection for locomotion and static body support.

Vertebral bending mechanics and xenarthrous morphology in the nine-banded armadillo (Dasypus novemcinctus).

The vertebral column has evolved to accommodate the broad range of locomotor pressures found across vertebrate lineages. Xenarthran (armadillos, sloths and anteaters) vertebral columns are characterized by xenarthrous articulations, novel intervertebral articulations located in the posterior trunk that are hypothesized to stiffen the vertebral column to facilitate digging. To determine the degree to which xenarthrous articulations impact vertebral movement, we passively measured compliance and range of motion during ventroflexion, dorsiflexion and lateral bending across the thoracolumbar region of the nine-banded armadillo, Dasypus novemcinctus Patterns of bending were compared with changes in vertebral morphology along the column to determine which morphological features best predict intervertebral joint mechanics. We found that compliance was lower in post-diaphragmatic, xenarthrous vertebrae relative to pre-xenarthrous vertebrae in both sagittal and lateral planes of bending. However, we also found that range of motion was higher in this region. These changes in mechanics are correlated with the transition from pre-xenarthrous to xenarthrous vertebrae, as well as with the transition from thoracic to lumbar vertebrae. Our results thus substantiate the hypothesis that xenarthrous articulations stiffen the vertebral column. Additionally, our data suggest that xenarthrous articulations, and their associated enlarged metapophyses, also act to increase the range of motion of the post-diaphragmatic region. We propose that xenarthrous articulations perform the dual role of stiffening the vertebral column and increasing mobility, resulting in passively stable vertebrae that are capable of substantial bending under appropriate loads.

New insights on equid locomotor evolution from the lumbar region of fossil horses.

The specialization of equid limbs for cursoriality is a classic case of adaptive evolution, but the role of the axial skeleton in this famous transition is not well understood. Extant horses are extremely fast and efficient runners, which use a stiff-backed gallop with reduced bending of the lumbar region relative to other mammals. This study tests the hypothesis that stiff-backed running in horses evolved in response to evolutionary increases in body size by examining lumbar joint shape from a broad sample of fossil equids in a phylogenetic context. Lumbar joint shape scaling suggests that stability of the lumbar region does correlate with size through equid evolution. However, scaling effects were dampened in the posterior lumbar region, near the sacrum, which suggests strong selection for sagittal mobility in association with locomotor-respiratory coupling near the lumbosacral joint. I hypothesize that small-bodied fossil horses may have used a speed-dependent running gait, switching between stiff-backed and flex-backed galloping as speed increased.

Evolutionary allometry of the thoracolumbar centra in felids and bovids.

Mammals have evolved a remarkable range of body sizes, yet their overall body plan remains unaltered. One challenge of evolutionary biology is to understand the mechanisms by which this size diversity is achieved, and how the mechanical challenges associated with changing body size are overcome. Despite the importance of the axial skeleton in body support and locomotion, and much interest in the allometry of the appendicular skeleton, little is known about vertebral allometry outside primates. This study compares evolutionary allometry of the thoracolumbar centra in two families of quadrupedal running mammals: Felidae and Bovidae. I test the hypothesis that, as size increases, the thoracolumbar region will resist increasing loads by becoming a) craniocaudally shorter, and b) larger in cross-sectional area, particularly in the sagittal plane. Length, width, and height of the thoracolumbar centra of 23 felid and 34 bovid species were taken. Thoracic, prediaphragmatic, lumbar, and postdiaphragmatic lengths were calculated, and diameters were compared at three equivalent positions: the midthoracic, the diaphragmatic and the midlumbar vertebra. Allometric slopes were calculated using a reduced major axis regression, on both raw and independent contrasts data. Slopes and elevations were compared using an ANCOVA. As size increases the thoracolumbar centra become more robust, showing preferential reinforcement in the sagittal plane. There was less allometric shortening of the thoracic than the lumbar region, perhaps reflecting constraints due to its connection with the respiratory apparatus. The thoracic region was more robust in bovids than felids, whereas the lumbar region was longer and more robust in felids than bovids. Elongation of lumbar centra increases the outlever of sagittal bending at intervertebral joints, increasing the total pelvic displacement during dorsomobile running. Both locomotor specializations and functional regionalization of the axial skeleton appear to have influenced its response to increasing size.

Impact of the terrestrial-aquatic transition on disparity and rates of evolution in the carnivoran skull.

BACKGROUND: Which factors influence the distribution patterns of morphological diversity among clades? The adaptive radiation model predicts that a clade entering new ecological niche will experience high rates of evolution early in its history, followed by a gradual slowing. Here we measure disparity and rates of evolution in Carnivora, specifically focusing on the terrestrial-aquatic transition in Pinnipedia. We analyze fissiped (mostly terrestrial, arboreal, and semi-arboreal, but also including the semi-aquatic otter) and pinniped (secondarily aquatic) carnivorans as a case study of an extreme ecological transition. We used 3D geometric morphometrics to quantify cranial shape in 151 carnivoran specimens (64 fissiped, 87 pinniped) and five exceptionally-preserved fossil pinnipeds, including the stem-pinniped Enaliarctos emlongi. Range-based and variance-based disparity measures were compared between pinnipeds and fissipeds. To distinguish between evolutionary modes, a Brownian motion model was compared to selective regime shifts associated with the terrestrial-aquatic transition and at the base of Pinnipedia. Further, evolutionary patterns were estimated on individual branches using both Ornstein-Uhlenbeck and Independent Evolution models, to examine the origin of pinniped diversity. RESULTS: Pinnipeds exhibit greater cranial disparity than fissipeds, even though they are less taxonomically diverse and, as a clade nested within fissipeds, phylogenetically younger. Despite this, there is no increase in the rate of morphological evolution at the base of Pinnipedia, as would be predicted by an adaptive radiation model, and a Brownian motion model of evolution is supported. Instead basal pinnipeds populated new areas of morphospace via low to moderate rates of evolution in new directions, followed by later bursts within the crown-group, potentially associated with ecological diversification within the marine realm. CONCLUSION: The transition to an aquatic habitat in carnivorans resulted in a shift in cranial morphology without an increase in rate in the stem lineage, contra to the adaptive radiation model. Instead these data suggest a release from evolutionary constraint model, followed by aquatic diversifications within crown families.

Early Eocene fossils suggest that the mammalian order Perissodactyla originated in India.

Cambaytheres (Cambaytherium, Nakusia and Kalitherium) are recently discovered early Eocene placental mammals from the Indo-Pakistan region. They have been assigned to either Perissodactyla (the clade including horses, tapirs and rhinos, which is a member of the superorder Laurasiatheria) or Anthracobunidae, an obscure family that has been variously considered artiodactyls or perissodactyls, but most recently placed at the base of Proboscidea or of Tethytheria (Proboscidea+Sirenia, superorder Afrotheria). Here we report new dental, cranial and postcranial fossils of Cambaytherium, from the Cambay Shale Formation, Gujarat, India (~54.5 Myr). These fossils demonstrate that cambaytheres occupy a pivotal position as the sister taxon of Perissodactyla, thereby providing insight on the phylogenetic and biogeographic origin of Perissodactyla. The presence of the sister group of perissodactyls in western India near or before the time of collision suggests that Perissodactyla may have originated on the Indian Plate during its final drift toward Asia.

Ontogenetic allometry in the thoracolumbar spine of mammal species with differing gait use.

Vertebrae are serially homologous structures with tight integration through their evolution and development. However, in mammals, the thoracic and lumbar regions are morphologically and functionally differentiated. We test the hypothesis that locomotor specialization is associated with altered post-natal growth patterns in vertebrae from different vertebral regions. We use longitudinal data to examine thoracolumbar growth in two specialized half-bounding (Oryctolagus cuniculus and Chinchilla lanigera) and two non-specialized (Cavia porcellus and Monodelphis domestica) species with similar body sizes. Lateral X-rays of 38 individuals were the source of centrum length, centrum height and intervertebral space length measures for 19-20 thoracolumbar vertebrae. The repeated measurements design included the same individuals soon after birth and again at adult size. Data from columns with different vertebral counts were compared by either summing (length) or averaging (height) within regions, and individual vertebrae were directly compared at the first and last five vertebral positions. Specialized half-bounders had longer lumbar regions than generalists, which was attributable to positively allometric growth of the lumbar centra. Lumbar centrum length was more variable both ontogenetically and interspecifically than the other variables, suggesting heterochrony may be generating lumbar variation. Craniocaudal patterns of centrum growth correlate with expression of regionalizing genes (i.e., Hox).

Body size and premolar evolution in the early-middle eocene euprimates of Wyoming.

The earliest euprimates to arrive in North America were larger-bodied notharctids and smaller-bodied omomyids. Through the Eocene, notharctids generally continued to increase in body size, whereas omomyids generally radiated within small- and increasingly mid-sized niches in the middle Eocene. This study examines the influence of changing body size and diet on the evolution of the lower fourth premolar in Eocene euprimates. The P4 displays considerable morphological variability in these taxa. Despite the fact that most studies of primate dental morphology have focused on the molars, P4 can also provide important paleoecological insights. We analyzed the P4 from 177 euprimate specimens, representing 35 species (11 notharctids and 24 omomyids), in three time bins of approximately equal duration: early Wasatchian, late Wasatchian, and Bridgerian. Two-dimensional surface landmarks were collected from lingual photographs, capturing important variation in cusp position and tooth shape. Disparity metrics were calculated and compared for the three time bins. In the early Eocene, notharctids have a more molarized P4 than omomyids. During the Bridgerian, expanding body size range of omomyids was accompanied by a significant increase in P4 disparity and convergent evolution of the semimolariform condition in the largest omomyines. P4 morphology relates to diet in early euprimates, although patterns vary between families.

Morphology and biomechanics of the pinniped jaw: mandibular evolution without mastication.

Pinnipeds (seals, sea lions, and walruses) underwent a shift in jaw function away from typical carnivoran mastication to more novel marine behaviors during the terrestrial-aquatic transition. Here we test the effect of aquatic prey capture and male-male combat on the morphological evolution of a mammal jaw that does not masticate. Nine three-dimensional landmarks were taken along the mandible for 25 species (N = 83), and corpus and symphysis external and cortical breadths for a subset of five species (N = 33). Principal components analysis was performed on size-corrected landmark data to assess variation in overall jaw morphology across pinnipeds. Corpus breadths were input to a beam model to calculate strength properties and estimated bite force of specific species with contrasting behaviors (filter feeding, suction feeding, grip-and-tear feeding, and male-male combat). Results indicate that, although phylogenetic signal in jaw shape is strong, function is also important in determining morphology. Filter feeders display an elongate symphysis and a long toothrow that may play a role in filtering krill. Grip-and-tear feeders have a long jaw and large estimated bite force relative to non-biting species. However, the largest estimated bite forces were observed in males of male-male combative species, likely due to the high selection pressure associated with male success in highly polygynous species. The suction feeding jaw is weak in biting but has a different morphology in the two suction feeding taxa. In conclusion, familial patterns of pinniped jaw shape due to phylogenetic relatedness have been modified by adaptations to specialized behavior of individual taxa.