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. * This article corresponds to Quinn, B. L. 2020. Digest: Incomplete convergence drives formfunction relationship in gliders. Evolution.
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 tradeoffs. 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 (less than 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 not 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.
The Hell Creek region of northeastern Montana is an excellent study system to explore the rise to dominance of mammalian faunas after the Cretaceous–Paleogene (K–Pg) mass extinction. The Tullock Member of the Fort Union Formation exposed in that region was deposited during the first 1.2 Ma after the Chicxulub bolide impact. Some aspects of post-K–Pg mammalian succession remain obscure, however, due to a lack of finer stratigraphic resolution between vertebrate fossil localities. Here, we present a new stratigraphic model for the lower and middle Tullock and identify a stratigraphic succession of five mammal-bearing sedimentary units that span the first ∼ 900 ka of the Paleocene. Most notably, we find that middle Tullock fossil localities, which were previously thought to be deposited by a single, large fluvial channel complex, are derived from two temporally and lithologically distinct sedimentary units: the Biscuit Springs unit (BS) and the Garbani channel (GC). The top of the GC is stratigraphically above the top of the BS, but in some places cuts through the entirety of the BS, a relationship that previously complicated interpretations of their relative age. This cross-cutting relationship reveals that the BS is older than the GC. Thus, the BS local fauna represents a potential intermediate between the older local faunas from the post-K–Pg ‘disaster' interval and the younger, more taxonomically/ecologically diverse GC local fauna. This new stratigraphic framework sets the stage for future studies focused on the pattern and timing of biotic recovery in the aftermath of the K–Pg mass extinction.
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/or measuring convergence. Two commonly used methods include (i) distance-based methods that measure morphological distances between lineages in phylomorphospace and (ii) fitting evolutionary models to morphological datasets to test whether lineages have evolved toward adaptive peaks. Here, we demonstrate that both types of convergence measures are influenced by the position of putatively convergent taxa in morphospace such that morphological outliers are statistically more likely to exhibit convergence by chance. A more substantial issue is that some methods will often misidentify divergent lineages as being convergent. These issues likely influence the results of many studies, especially those that focus on morphological outliers. To help address these problems, we developed a new distance-based method for measuring convergence that incorporates distances between lineages through time and minimizes the possibility of divergent taxa being misidentified as convergent. We advocate the use of this method when the phylogenetic tips of putatively convergent lineages are of the same or similar geologic ages (e.g., extant taxa), meaning that convergence among the lineages is expected to be synchronous. We conclude by emphasizing that all available convergence measures are imperfect, and researchers should recognize the limitations of these methods and use multiple lines of evidence when inferring and measuring convergence.
In non-mammalian synapsids and early mammals, evolutionary transformations in the feeding and hearing apparatuses are posited to have been prerequisites for the radiation of extant mammals. Unlike most vertebrates, including many early synapsids, mammals have precise dental occlusion, a lower jaw composed of one bone, and middle ear ossicles derived from ancestral jaw bones. We illuminate a related functional transition: therian mammals (eutherians and metatherians) evolved anteriorly directed chewing strokes, which are absent in other synapsid lineages. Anteriorly directed jaw movement during occlusion necessitates anteriorly directed muscle force vectors, and we posit that a shift in muscle orientation is reflected in the fossil record by the evolutionary appearance of a posteriorly positioned angular process in cladotherians (therians and their close kin). Anteriorly directed occlusion might have been absent in earlier synapsids because of the presence of attached middle ear elements in the posterior region of the jaw that prohibited the posterior insertion of jaw musculature. These changes to the masticatory apparatus in cladotherians are likely to have permitted the evolution of novel masticatory movements, including grinding in both the anterior and medial directions (e.g. rodents and ungulates, respectively). Thus, this evolutionary transition might have been a crucial prerequisite for the dietary diversification of therians.
Cimolodontan multituberculates were a diverse and long-lived group of mammals characterized by large, blade-like lower fourth premolars (p4). Blade-like (plagiaulacoid) dentitions have evolved numerous times in distantly related mammalian lineages. Here we investigate how p4-shape disparity changed through time in the Cimolodonta. We address two hypotheses: (H1) blade-like dentitions constrain the ability of plagiaulacoid mammals to evolve novel dental morphologies, (H2) cimolodontan dental evolution proceeded gradually along a morphocline during the Late Cretaceous. We quantify functionally important aspects of p4 shape, including ratios reflecting height (H:L), symmetry (L1:L), and mesial-face height (H1:H), in a large sample of cimolodontans spanning the mid-Cretaceous through early Paleogene of North America (ca. 100–35 Mya). Our results do not support the morphocline hypothesis (H2) and, instead, show that cimolodontans evolved a wide range of p4 shapes by the mid-Cretaceous, and that p4-shape disparity remained stable through the Late Cretaceous. We hypothesize that the two-stage cimolodontan chewing cycle (slicing-crushing then grinding) imposed functional constraints on p4 morphology. After the Cretaceous-Paleogene boundary, p4-shape disparity increased sharply, driven by the appearance of the Taeniolabidoidea, Microcosmodontidae, and Eucosmodontidae, in the early Paleocene. We contend that the slicing-crushing functions of the p4 became less important in those taxa, relaxing functional constraints on p4 morphology. Cimolodontans that retained both the slicing-crushing and grinding function of the p4 had a more limited range of p4 morphologies, and probably were largely restricted to animal-dominated omnivory. Taxa that shifted the initial slicing-crushing function from the p4 to the incisors had fewer functional constraints on p4 morphology, and were able to increase their molar grinding capacity to exploit plant-dominated omnivory and herbivory. That the p4 was reduced in herbivorous taxa rather than modified into a broader, multi-cusped tooth lends support to the morphological constraint hypothesis (H1), and this relationship between p4 morphology and function suggests that retaining a large, blade-like p4 might have limited the range of herbivorous diets cimolodontans could exploit. These findings highlight the ecological and evolutionary limitations that specialized dentitions can impose on mammals by restricting their morphological and, in turn, functional diversification.
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