Challenges And Advances In Measuring Phenotypic Convergence.

Tests of phenotypic convergence can provide evidence of adaptive evolution, and the popularity of such studies has grown in recent years due to the development of novel, quantitative methods for identifying and measuring convergence. These methods include the commonly applied C1-C4 measures of Stayton (2015), which measure morphological distances between lineages, and Ornstein-Uhlenbeck (OU) model-fitting analyses, which test whether lineages converged on shared adaptive peaks. We test the performance of C-measures and other convergence measures under various evolutionary scenarios and reveal a critical issue with C-measures: they often misidentify divergent lineages as convergent. We address this issue by developing novel convergence measures- Ct1-Ct4-measures -that calculate distances between lineages at specific points in time, minimizing the possibility of misidentifying divergent taxa as convergent. Ct-measures are most appropriate when focal lineages are of the same or similar geologic ages (e.g., extant taxa), meaning that the lineages' evolutionary histories include considerable overlap in time. Beyond C-measures, we find that all convergence measures are influenced by the position of focal taxa in phenotypic space, with morphological outliers often statistically more likely to be measured as strongly convergent. Further, we mimic scenarios in which researchers assess convergence using OU models with a priori regime assignments (e.g., classifying taxa by ecological traits) and find that multiple-regime OU models with phenotypically divergent lineages assigned to a shared selective regime often outperform simpler models. This highlights that model support for these multiple-regime OU models should not be assumed to always reflect convergence among focal lineages of a shared regime. Our new Ct1-Ct4-measures provide researchers with an improved comparative tool, but we emphasize that all available convergence measures are imperfect, and researchers should recognize the limitations of these methods and use multiple lines of evidence to test convergence hypotheses.

The hierarchical radiation of phyllostomid bats as revealed by adaptive molar morphology.

Adaptive radiations are bursts in biodiversity that generate new evolutionary lineages and phenotypes. However, because they typically occur over millions of years, it is unclear how their macroevolutionary dynamics vary through time and among groups of organisms. Phyllostomid bats radiated extensively for diverse diets-from insects to vertebrates, fruit, nectar, and blood-and we use their molars as a model system to examine the dynamics of adaptive radiations. Three-dimensional shape analyses of lower molars of Noctilionoidea (Phyllostomidae and close relatives) indicate that different diet groups exhibit distinct morphotypes. Comparative analyses further reveal that phyllostomids are a striking example of a hierarchical radiation; phyllostomids' initial, higher-level diversification involved an "early burst" in molar morphological disparity as lineages invaded new diet-affiliated adaptive zones, followed by subsequent lower-level diversifications within adaptive zones involving less dramatic morphological changes. We posit that strong selective pressures related to initial shifts to derived diets may have freed molars from morpho-functional constraints associated with the ancestral molar morphotype. Then, lineages with derived diets (frugivores and nectarivores) diversified within broad adaptive zones, likely reflecting finer-scale niche partitioning. Importantly, the observed early burst pattern is only evident when examining molar traits that are strongly linked to diet, highlighting the value of ecomorphological traits in comparative studies. Our results support the hypothesis that adaptive radiations are commonly hierarchical and involve different tempos and modes at different phylogenetic levels, with early bursts being more common at higher levels.

Derived faunivores are the forerunners of major synapsid radiations.

Evolutionary radiations generate most of Earth's biodiversity, but are there common ecomorphological traits among the progenitors of radiations? In Synapsida (the mammalian total group), 'small-bodied faunivore' has been hypothesized as the ancestral state of most major radiating clades, but this has not been quantitatively assessed across multiple radiations. To examine macroevolutionary patterns in a phylogenetic context, we generated a time-calibrated metaphylogeny ('metatree') comprising 1,888 synapsid species from the Carboniferous through the Eocene (305-34 Ma) based on 269 published character matrices. We used comparative methods to investigate body size and dietary evolution during successive synapsid radiations. Faunivory is the ancestral dietary regime of each major synapsid radiation, but relatively small body size is only established as the common ancestral state of radiations near the origin of Mammaliaformes in the Late Triassic. The faunivorous ancestors of synapsid radiations typically have numerous novel characters compared with their contemporaries, and these derived traits may have helped them to survive faunal turnover events and subsequently radiate.

Bursts in skull evolution weakened with time.

The skull shapes of mammals diversified more rapidly early in their history.

Multituberculate Mammals Show Evidence of a Life History Strategy Similar to That of Placentals, Not Marsupials.

AbstractThe remarkable evolutionary success of placental mammals has been partly attributed to their reproductive strategy of prolonged gestation and birthing of relatively precocial, quickly weaned neonates. Although this strategy was conventionally considered derived relative to that of marsupials with highly altricial neonates and long lactation periods, mounting evidence has challenged this view. Until now the fossil record has been relatively silent on this debate, but here we find that proportions of different bone tissue microstructures in the femoral cortices of small extant marsupials and placentals correlate with length of lactation period, allowing us to apply this histological correlate of reproductive strategies to Late Cretaceous and Paleocene members of Multituberculata, an extinct mammalian clade that is phylogenetically stemward of Theria. Multituberculate bone histology closely resembles that of placentals, suggesting that they had similar life history strategies. A stem-therian clade exhibiting evidence of placental-like life histories supports the hypothesis that intense maternal-fetal contact characteristic of placentals is ancestral for therians. Alternatively, multituberculates and placentals may have independently evolved prolonged gestation and abbreviated lactation periods. Our results challenge the hypothesis that the rise of placental mammals was driven by unique life history innovations and shed new light on early mammalian diversification.

Bat Dentitions: A Model System for Studies at The Interface of Development, Biomechanics, and Evolution.

The evolution of complex dentitions was a major innovation in mammals that facilitated the expansion into new dietary niches that imposed selection for tight form-function relationships. Teeth allow mammals to ingest and process food items by applying forces produced by a third-class lever system composed by the jaw adductors, the cranium, and the mandible. Physical laws determine changes in jaw adductor (biting) forces at different bite point locations along the mandible (outlever), thus individual teeth are expected to experience different mechanical regimes during feeding. If the mammal dentition exhibits functional adaptations to mandible feeding biomechanics, then teeth are expected to have evolved to develop mechanically-advantageous sizes, shapes, and positions. Here, we present bats as a model system to test this hypothesis and, more generally, for integrative studies of mammal dental diversity. We combine a field-collected dataset of bite forces along the tooth row with data on dental and mandible morphology across 30 bat species. We (1) describe, for the first time, bite force trends along the tooth row of bats, (2) use phylogenetic comparative methods to investigate relationships among bite force patterns, tooth and mandible morphology, and (3) hypothesize how these biting mechanics patterns may relate to the developmental processes controlling tooth formation. We find that bite force variation along the tooth row is consistent with predictions from lever mechanics models, with most species having the greatest bite force at the first lower molar. The cross-sectional shape of the mandible body is strongly associated with the position of maximum bite force along the tooth row, likely reflecting mandibular adaptations to varying stress patterns among species. Further, dental dietary adaptations seem to be related to bite force variation along molariform teeth, with insectivorous species exhibiting greater bite force more anteriorly, narrower teeth and mandibles, and frugivores/omnivores showing greater bite force more posteriorly, wider teeth and mandibles. As these craniodental traits are linked through development, dietary specialization appears to have shaped intrinsic mechanisms controlling traits relevant to feeding performance.

Functional diversity of small-mammal postcrania is linked to both substrate preference and body size.

Selective pressures favor morphologies that are adapted to distinct ecologies, resulting in trait partitioning among ecomorphotypes. However, the effects of these selective pressures vary across taxa, especially because morphology is also influenced by factors such as phylogeny, body size, and functional trade-offs. In this study, we examine how these factors impact functional diversification in mammals. It has been proposed that trait partitioning among mammalian ecomorphotypes is less pronounced at small body sizes due to biomechanical, energetic, and environmental factors that favor a "generalist" body plan, whereas larger taxa exhibit more substantial functional adaptations. We title this the Divergence Hypothesis (DH) because it predicts greater morphological divergence among ecomorphotypes at larger body sizes. We test DH by using phylogenetic comparative methods to examine the postcranial skeletons of 129 species of taxonomically diverse, small-to-medium-sized (<15 kg) mammals, which we categorize as either "tree-dwellers" or "ground-dwellers." In some analyses, the morphologies of ground-dwellers and tree-dwellers suggest greater between-group differentiation at larger sizes, providing some evidence for DH. However, this trend is neither particularly strong nor supported by all analyses. Instead, a more pronounced pattern emerges that is distinct from the predictions of DH: within-group phenotypic disparity increases with body size in both ground-dwellers and tree-dwellers, driven by morphological outliers among "medium"-sized mammals. Thus, evolutionary increases in body size are more closely linked to increases in within-locomotor-group disparity than to increases in between-group disparity. We discuss biomechanical and ecological factors that may drive these evolutionary patterns, and we emphasize the significant evolutionary influences of ecology and body size on phenotypic diversity.

Incomplete convergence of gliding mammal skeletons.

Ecology and biomechanics play central roles in the generation of phenotypic diversity. When unrelated taxa invade a similar ecological niche, biomechanical demands can drive convergent morphological transformations. Thus, examining convergence helps to elucidate the key catalysts of phenotypic change. Gliding mammals are often presented as a classic case of convergent evolution because they independently evolved in numerous clades, each possessing patagia ("wing" membranes) that generate lift during gliding. We use phylogenetic comparative methods to test whether the skeletal morphologies of the six clades of extant gliding mammals demonstrate convergence. Our results indicate that glider skeletons are convergent, with glider groups consistently evolving proportionally longer, more gracile limbs than arborealists, likely to increase patagial surface area. Nonetheless, we interpret gliders to represent incomplete convergence because (1) evolutionary model-fitting analyses do not indicate strong selective pressures for glider trait optima, (2) the three marsupial glider groups diverge rather than converge, and (3) the gliding groups remain separated in morphospace (rather than converging on a single morphotype), which is reflected by an unexpectedly high level of morphological disparity. That glider skeletons are morphologically diverse is further demonstrated by fossil gliders from the Mesozoic Era, which possess unique skeletal characteristics that are absent in extant gliders. Glider morphologies may be strongly influenced by factors such as body size and attachment location of patagia on the forelimb, which can vary among clades. Thus, convergence in gliders appears to be driven by a simple lengthening of the limbs, whereas additional skeletal traits reflect nuances of the gliding apparatus that are distinct among different evolutionary lineages. Our unexpected results add to growing evidence that incomplete convergence is prevalent in vertebrate clades, even among classic cases of convergence, and they highlight the importance of examining form-function relationships in light of phylogeny, biomechanics, and the fossil record.

Feeding ecology has a stronger evolutionary influence on functional morphology than on body mass in mammals.

Ecological specialization is a central driver of adaptive evolution. However, selective pressures may uniquely affect different ecomorphological traits (e.g., size and shape), complicating efforts to investigate the role of ecology in generating phenotypic diversity. Comparative studies can help remedy this issue by identifying specific relationships between ecologies and morphologies, thus elucidating functionally relevant traits. Jaw shape is a dietary correlate that offers considerable insight on mammalian evolution, but few studies have examined the influence of diet on jaw morphology across mammals. To this end, I apply phylogenetic comparative methods to mandibular measurements and dietary data for a diverse sample of mammals. Especially powerful predictors of diet are metrics that capture either the size of the angular process, which increases with greater herbivory, or the length of the posterior portion of the jaw, which decreases with greater herbivory. The size of the angular process likely reflects sizes of attached muscles that produce jaw movements needed to grind plant material. Further, I examine the impact of feeding ecology on body mass, an oft-used ecological surrogate in macroevolutionary studies. Although body mass commonly increases with evolutionary shifts to herbivory, it is outperformed by functional jaw morphology as a predictor of diet. Body mass is influenced by numerous factors beyond diet, and it may be evolutionarily labile relative to functional morphologies. This suggests that ecological diversification events may initially facilitate body mass diversification at smaller taxonomic and temporal scales, but sustained selective pressures will subsequently drive greater trait partitioning in functional morphologies.

Untangling the Multiple Ecological Radiations of Early Mammals.

The ecological diversification of early mammals is one of the most globally transformative events in Earth's history and the Cretaceous Terrestrial Revolution (KTR) and end-Cretaceous mass extinction are commonly hailed as catalysts. However, a confounding issue when examining this diversification is that it comprised nested radiations of mammalian subclades within the broader scope of mammalian evolution. In the past 200 million years, various independent groups experienced large-scale radiations, each involving ecological diversification from ancestral lineages of small insectivores; examples include Jurassic mammaliaforms, Late Cretaceous metatherians, and Cenozoic placentals. Here, we review these ecological radiations, highlighting the nuanced complexity of early mammal evolution, the value of ecomorphological fossil data, and the importance of phylogenetic context in macroevolutionary studies.

Publisher Correction: Late-surviving stem mammal links the lowermost Cretaceous of North America and Gondwana.

The asterisked footnote to Extended Data Table 1 should state '*Including Thomasia and Haramiyavia'. This has been corrected online.

Late-surviving stem mammal links the lowermost Cretaceous of North America and Gondwana.

Haramiyida was a successful clade of mammaliaforms, spanning the Late Triassic period to at least the Late Jurassic period, but their fossils are scant outside Eurasia and Cretaceous records are controversial1-4. Here we report, to our knowledge, the first cranium of a large haramiyidan from the basal Cretaceous of North America. This cranium possesses an amalgam of stem mammaliaform plesiomorphies and crown mammalian apomorphies. Moreover, it shows dental traits that are diagnostic of isolated teeth of supposed multituberculate affinities from the Cretaceous of Morocco, which have been assigned to the enigmatic 'Hahnodontidae'. Exceptional preservation of this specimen also provides insights into the evolution of the ancestral mammalian brain. We demonstrate the haramiyidan affinities of Gondwanan hahnodontid teeth, removing them from multituberculates, and suggest that hahnodontid mammaliaforms had a much wider, possibly Pangaean distribution during the Jurassic-Cretaceous transition.

New gliding mammaliaforms from the Jurassic.

Stem mammaliaforms are Mesozoic forerunners to mammals, and they offer critical evidence for the anatomical evolution and ecological diversification during the earliest mammalian history. Two new eleutherodonts from the Late Jurassic period have skin membranes and skeletal features that are adapted for gliding. Characteristics of their digits provide evidence of roosting behaviour, as in dermopterans and bats, and their feet have a calcaneal calcar to support the uropagatium as in bats. The new volant taxa are phylogenetically nested with arboreal eleutherodonts. Together, they show an evolutionary experimentation similar to the iterative evolutions of gliders within arboreal groups of marsupial and placental mammals. However, gliding eleutherodonts possess rigid interclavicle-clavicle structures, convergent to the avian furculum, and they retain shoulder girdle plesiomorphies of mammaliaforms and monotremes. Forelimb mobility required by gliding occurs at the acromion-clavicle and glenohumeral joints, is different from and convergent to the shoulder mobility at the pivotal clavicle-sternal joint in marsupial and placental gliders.

New evidence for mammaliaform ear evolution and feeding adaptation in a Jurassic ecosystem.

Stem mammaliaforms are forerunners to modern mammals, and they achieved considerable ecomorphological diversity in their own right. Recent discoveries suggest that eleutherodontids, a subclade of Haramiyida, were more species-rich during the Jurassic period in Asia than previously recognized. Here we report a new Jurassic eleutherodontid mammaliaform with an unusual mosaic of highly specialized characteristics, and the results of phylogenetic analyses that support the hypothesis that haramiyidans are stem mammaliaforms. The new fossil shows fossilized skin membranes that are interpreted to be for gliding and a mandibular middle ear with a unique character combination previously unknown in mammaliaforms. Incisor replacement is prolonged until well after molars are fully erupted, a timing pattern unique to most other mammaliaforms. In situ molar occlusion and a functional analysis reveal a new mode of dental occlusion: dual mortar-pestle occlusion of opposing upper and lower molars, probably for dual crushing and grinding. This suggests that eleutherodontids are herbivorous, and probably specialized for granivory or feeding on soft plant tissues. The inferred dietary adaptation of eleutherodontid gliders represents a remarkable evolutionary convergence with herbivorous gliders in Theria. These Jurassic fossils represent volant, herbivorous stem mammaliaforms associated with pre-angiosperm plants that appear long before the later, iterative associations between angiosperm plants and volant herbivores in various therian clades.

The evolutionary origin of jaw yaw in mammals.

Theria comprises all but three living mammalian genera and is one of the most ecologically pervasive clades on Earth. Yet, the origin and early history of therians and their close relatives (i.e., cladotherians) remains surprisingly enigmatic. A critical biological function that can be compared among early mammal groups is mastication. Morphometrics and modeling analyses of the jaws of Mesozoic mammals indicate that cladotherians evolved musculoskeletal anatomies that increase mechanical advantage during jaw rotation around a dorsoventrally-oriented axis (i.e., yaw) while decreasing the mechanical advantage of jaw rotation around a mediolaterally-oriented axis (i.e., pitch). These changes parallel molar transformations in early cladotherians that indicate their chewing cycles included significant transverse movement, likely produced via yaw rotation. Thus, I hypothesize that cladotherian molar morphologies and musculoskeletal jaw anatomies evolved concurrently with increased yaw rotation of the jaw during chewing cycles. The increased transverse movement resulting from yaw rotation may have been a crucial evolutionary prerequisite for the functionally versatile tribosphenic molar morphology, which underlies the molars of all therians and is retained by many extant clades.

Mammalian evolution. An arboreal docodont from the Jurassic and mammaliaform ecological diversification.

A new docodontan mammaliaform from the Middle Jurassic of China has skeletal features for climbing and dental characters indicative of an omnivorous diet that included plant sap. This fossil expands the range of known locomotor adaptations in docodontans to include climbing, in addition to digging and swimming. It further shows that some docodontans had a diet with a substantial herbivorous component, distinctive from the faunivorous diets previously reported in other members of this clade. This reveals a greater ecological diversity in an early mammaliaform clade at a more fundamental taxonomic level not only between major clades as previously thought.

Mammal disparity decreases during the Cretaceous angiosperm radiation.

Fossil discoveries over the past 30 years have radically transformed traditional views of Mesozoic mammal evolution. In addition, recent research provides a more detailed account of the Cretaceous diversification of flowering plants. Here, we examine patterns of morphological disparity and functional morphology associated with diet in early mammals. Two analyses were performed: (i) an examination of diversity based on functional dental type rather than higher-level taxonomy, and (ii) a morphometric analysis of jaws, which made use of modern analogues, to assess changes in mammalian morphological and dietary disparity. Results demonstrate a decline in diversity of molar types during the mid-Cretaceous as abundances of triconodonts, symmetrodonts, docodonts and eupantotherians diminished. Multituberculates experience a turnover in functional molar types during the mid-Cretaceous and a shift towards plant-dominated diets during the late Late Cretaceous. Although therians undergo a taxonomic expansion coinciding with the angiosperm radiation, they display small body sizes and a low level of morphological disparity, suggesting an evolutionary shift favouring small insectivores. It is concluded that during the mid-Cretaceous, the period of rapid angiosperm radiation, mammals experienced both a decrease in morphological disparity and a functional shift in dietary morphology that were probably related to changing ecosystems.