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Pruned time calibrated phylogeny of Musteloidea redrawn from Law et al. (2018). The shaded blue box indicates the mustelid subclade (subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae) that exhibits higher clade carrying capacity relative to the rest of Musteloidea. The shaded yellow-green box indicates the mustelid subclade (Ictonychinae, Mustelinae, and Lutrinae) that exhibits an increase in the evolutionary rate of body length without an increase in the evolutionary rate of body mass. The shaded orange box highlights Mustelinae (weasels and polecats), the clade often considered the hallmark example of body elongation within Mustelidae. All nodes are supported by posterior probabilities > 0.95 except where noted. PLIO = Pleistocene; PLE = Pliocene.
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An elongate body with reduced or absent limbs has evolved independently in many ectothermic vertebrate lineages. While much effort has been spent examining the morphological pathways to elongation in these clades, quantitative investigations into the evolution of elongation in endothermic clades are lacking. We quantified body shape in 61 musteloid...
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... and the musteloid fossil record provide no evidence of a pulse of increased speciation during this climate transition ( ). However, these authors did recover strong support for a scenario in which a subclade of putatively elongate mustelids (consisting of the subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae; blue box in Fig. 1) exhibited decoupled diversification dynamics from the rest of the clade. In addition, analysis of rates of body length and mass evolution show that these two traits are also decoupled within this mustelid subclade (yellow-green box in Fig. 1), with the branches leading toward Ictonychinae, Mustelinae, and Lutrinae exhibiting an ...
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... of the subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae; blue box in Fig. 1) exhibited decoupled diversification dynamics from the rest of the clade. In addition, analysis of rates of body length and mass evolution show that these two traits are also decoupled within this mustelid subclade (yellow-green box in Fig. 1), with the branches leading toward Ictonychinae, Mustelinae, and Lutrinae exhibiting an increase in the rate of body length evolution without an associated increase in the rate of body mass evolution. These patterns suggest that an association between elongation and diversification rates is worthy of further ...
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... assessed the evolution of musteloid body shape and size using a phylogenetic comparative approach with a recently published musteloid phylogeny ( Fig. 1; ). This time-calibrated tree was inferred in a Bayesian framework using a supermatrix of 46 genes (four mitochondrial and 42 nuclear genes) from 75 of the 85 putative musteloid species (88.2% of musteloid species representing all 33 musteloid genera). We incorporated 74 phylogenetically constrained fossil musteloids to assist with ...
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... length and mass evolution within mustelid clades ( ), we fit two-peak OUM models under three distinct phylogenetic scenarios. The first model (OUM A) tested for a transition in head-body ER between the mustelid subclade that exhibited increased clade carrying capacity (Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae; blue box in Fig. 1) and the remaining musteloids. The second model (OUM B) tested for a transition in head-body ER between the mustelid subclade that exhibited decoupled evolutionary rates in body length and mass (Ictonychinae, Mustelinae, and Lutrinae; yellow-green box in Fig. 1) and the remaining musteloids. The third model (OUM C) tested for a ...
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... capacity (Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae; blue box in Fig. 1) and the remaining musteloids. The second model (OUM B) tested for a transition in head-body ER between the mustelid subclade that exhibited decoupled evolutionary rates in body length and mass (Ictonychinae, Mustelinae, and Lutrinae; yellow-green box in Fig. 1) and the remaining musteloids. The third model (OUM C) tested for a transition in head-body ER between a designated clade consisting of just musteline weasels and polecats (Mustela spp.; orange box in Fig. 1) and the remaining musteloids. This third model was tested because musteline weasels and polecats are considered the hallmark ...
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... subclade that exhibited decoupled evolutionary rates in body length and mass (Ictonychinae, Mustelinae, and Lutrinae; yellow-green box in Fig. 1) and the remaining musteloids. The third model (OUM C) tested for a transition in head-body ER between a designated clade consisting of just musteline weasels and polecats (Mustela spp.; orange box in Fig. 1) and the remaining musteloids. This third model was tested because musteline weasels and polecats are considered the hallmark example of body elongation within Mustelidae ( Brown et al. 1972;Gliwicz 1988;King 1989). All models were fit using the OUwie function in the R package OUwie ( Beaulieu et al. 2012). The three designated ...
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... shape within musteloids correspond with recent analyses of lineage diversification and evolutionary rates of body size. First, decoupling of diversification processes just after the Mid-Miocene Climate transition occurred along the branch leading toward the mustelid crown clades Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae ( Fig. 1) and resulted in a clade carrying capacity nearly twice as high as the remaining musteloid clade. Second, rates of body length evolution decoupled from body mass were consistent with an early-burst pattern within this mustelid subclade ( ). Together, transitions in body shape, decoupled length and mass relationships as well as increased ...
Citations
... We also recommend fitting a broader set of models than those fitted here. For instance, multiple-regime BM models that allow phylogenetic means to vary between regimes, which can be fit using mvMORPH functions (Clavel et al. 2015; smean = "FALSE"), may offer more appropriate null models than BM1, and they may complement multiple-regime OU models (e.g., Law et al., 2019;Grossnickle et al., 2020;Martinez et al., 2020;Rincon-Sandoval et al., 2020). Because these models do not model selection toward optima, support over OUM models may suggest limited or no convergence among focal lineages (e.g., Grossnickle et al., 2020). ...
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.
... Thus, performance is 38 considered the link between morphology, ecology, and species fitness [1][2][3]. Although many 39 studies have examined the form-function relationship of the skull [4][5][6][7], appendicular skeleton 40 [8][9][10][11], and axial skeleton [12][13][14][15][16], few have investigated functional trade-offs and covariation 41 among these three major skeletal systems. 42 ...
Analyses of form-function relationships are widely used to understand links between morphology, ecology, and species fitness across macroevolutionary scales. However, few have investigated functional trade-offs and covariance among functional traits within and between the skull, limbs, and vertebral column simultaneously. In this study, we investigated the adaptive landscape of skeletal form and function in carnivorans to test how functional trade-offs between these skeletal regions contribute to ecological adaptations and the topology of the landscape. We found that functional traits derived from carnivoran skeletal regions exhibit trade-offs and covariation across their performance surfaces, particularly in the appendicular and axial skeletons. These functional trade-offs and covariation corresponded as specializations to different adaptive landscapes when optimized by locomotor mode, diet, or family. Lastly, we found that the topologies of the optimized adaptive landscapes and underlying performance surfaces are largely characterized as smooth, gradual gradients between regions of low and high adaptive zones rather than as rugged, multipeak landscapes. Our results suggest that carnivorans may already occupy a broad adaptive zone as part of a larger mammalian adaptive landscape that masks the form and function relationships of skeletal traits.
... Limb loss is often associated with multiple morphological changes, with axial elongation being the most prominent feature in vertebrates (Caldwell, 2003;Collar et al., 2016;Law et al., 2019;Urošević et al., 2016). Body lengthening can be achieved by lengthening the trunk, tail, or both (Brandley et al., 2008;Ward and Brainerd, 2007). ...
Limb loss shows recurrent phenotypic evolution across squamate lineages. Here, based on three de novo-assembled genomes of limbless lizards from different lineages, we showed that divergence of conserved non-coding elements (CNEs) played an important role in limb development. These CNEs were associated with genes required for limb initiation and outgrowth, and with regulatory signals in the early stage of limb development. Importantly, we identified the extensive existence of insertions and deletions (InDels) in the CNEs, with the numbers ranging from 111 to 756. Most of these CNEs with InDels were lineage-specific in the limbless squamates. Nearby genes of these InDel CNEs were important to early limb formation, such as Tbx4, Fgf10, and Gli3. Based on functional experiments, we found that nucleotide mutations and InDels both affected the regulatory function of the CNEs. Our study provides molecular evidence underlying limb loss in squamate reptiles from a developmental perspective and sheds light on the importance of regulatory element InDels in phenotypic evolution.
... Unsurprisingly, a plethora of work has found that ecological factors affect the evolution of the shape and proportions of the skull (Janis, 1990;Olsen, 2017;Law et al., 2018;Arbour, Curtis & Santana, 2019;Grossnickle et al., 2020;Paluh, Stanley & Blackburn, 2020), limbs ( Van Valkenburgh, 1985;Higham et al., 2015;Citadini et al., 2018;Baeckens, Goeyers & Van Damme, 2020) and vertebrae (Buchholtz, 1998;Randau et al., 2016;Jones et al., 2018;Gillet, Frédérich & Parmentier, 2019;Luger et al., 2019;Adler et al., 2022). The evolution of diverse overall body shapes can also facilitate morphological, functional, and ecological innovations that can lead to increased diversification and niche specialization (Wiens, Brandley & Reeder, 2006;Collar et al., 2016;Law, 2019;Friedman, Price & Wainwright, 2021;Morinaga & Bergmann, 2020). ...
... Elongate body shapes are associated with fin and limb size reduction (Gans, 1975;Wake, 1991;Wiens & Slingluff, 2001;Skinner, Lee & Hutchinson, 2008;. In tetrapods, researchers have found that the forelimbs are generally reduced or lost prior to the hind limbs through evolutionary time (Gans, 1975;Wiens & Slingluff, 2001;Brandley, Huelsenbeck & Wiens, 2008;Law, Slater & Mehta, 2019;Morinaga & Bergmann, 2020;but see Kohlsdorf & Wagner, 2006;Bergmann & Morinaga, 2019). How locomotor ecologies affect relationships between body shape and limb lengths in mammals remains to be tested. ...
... Accordingly, we predicted that gliding squirrels would exhibit relatively longer forelimbs with increasing body elongation to increase patagium surface area for gliding. In contrast, we predicted that chipmunks and tree squirrels would exhibit relatively shorter forelimbs with increasing body elongation following similar patterns found in terrestrial carnivoran mammals (Law, Slater & Mehta, 2019). For our final objective, we examined which cranial and axial components contributed the most to overall body shape evolution across squirrels and within each ecotype. ...
Body size is often hypothesized to facilitate or constrain morphological diversity in the cranial, appendicular, and axial skeletons. However, how overall body shape scales with body size ( i.e. , body shape allometry) and whether these scaling patterns differ between ecological groups remains poorly investigated. Here, we test whether and how the relationships between body shape, body size, and limb lengths differ among species with different locomotor specializations, and describe the underlying morphological components that contribute to body shape evolution among squirrel (Sciuridae) ecotypes. We quantified the body size and shape of 87 squirrel species from osteological specimens held at museum collections. Using phylogenetic comparative methods, we first found that body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes: chipmunks and gliding squirrels exhibited more elongate bodies with increasing body sizes whereas ground squirrels exhibited more robust bodies with increasing body size. Second, we found that only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs. Third, we found that the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape evolution across squirrels. Overall, our work contributes to the growing understanding of mammalian body shape evolution and how it is influenced by body size and locomotor ecology, in this case from robust subterranean to gracile gliding squirrels.
... Functional demands on the skeleton related to behaviors such as feeding and locomotion frequently lead to predictable relationships between an organism's morphology and its ecology (Wainwright, 1991;Bock, 1994;Barr, 2018). In turn, these form-function relationships allow for the inference of behavior in species for which we have only morphological data, such as fossils (Chen and Wilson, 2015;Nations et al., 2019;Grossnickle et al., 2020;Lungmus and Angielczyk, 2021), quantification of macroevolutionary rates and modes (Kilbourne and Hutchinson, 2019;Law et al., 2019;Law, 2021;Prang et al., 2021;Slater, 2022), and the testing of hypotheses about ecological responses to competition and environmental change (Feder et al., 2010;Polly, 2010;Polly et al., 2017;Short and Lawing, 2021). A number of approaches have been used to quantify patterns of ecomorphological variation in the post-cranial skeleton, ranging from functional indices derived from linear measurements (Van Valkenburgh, 1987;Losos, 1990;Garland and Janis, 1993;Collar et al., 2013;Barr, 2014) to the description of complex patterns of 3D shape variation using the tools of geometric morphometrics (Curran, 2012;Fabre et al., 2013;Martín-Serra et al., 2014;Wang et al., 2020;Dunn and Avery, 2021). ...
A bstract
Three dimensional morphometric methods are a powerful tool for comparative analysis of shape. However, morphological shape is often represented using landmarks selected by the user to describe features of perceived importance, and this may lead to over confident prediction of form-function relationships in subsequent analyses. We used Generalized Procrustes Analysis (GPA) of 13 homologous 3D landmarks and spherical harmonics (SPHARM) analysis, a homology-free method that describes the entire shape of a closed surface, to quantify the shape of the calcaneus, a landmark poor structure that is important in hind-limb mechanics, for 111 carnivoran species spanning 12 of 13 terrestrial families. Both approaches document qualitatively similar patterns of shape variation, including a dominant continuum from short/stout to long/narrow calcanea. However, while phylogenetic generalized linear models indicate that locomotor mode best explains shape from the GPA, the same analyses find that shape described by SPHARM is best predicted by foot posture and body mass without a role for locomotor mode, though effect sizes for all are small. User choices regarding morphometric methods can dramatically impact macroevolutionary interpretations of shape change in a single structure, an outcome that is likely exacerbated when readily landmarkable features are few.
... Remarka ble morphological varia tions (i.e. the rela tive dimensions of the body, tail, and limbs), characteristic evolution and biotic interchange form the pattern of biodiversity and become one of the major goals in evolutionary biology (Carroll, 1997;Futuyma, 2005;Young et al., 2007;Ren et al., 2017;Jiang et al., 2019;Yu et al., 2021). Limb reduction in vertebrate exhibits the most intriguing trait, which repeatedly evolved in amphibians (Parra-Olea and Wake, 2001;Urosevic et al., 2016), reptiles Miralles et al., 2015;Bergmann et al., 2020), and mammals (Bejder and Hall, 2002;Law et al., 2019). Squamates, in particular, present an excellent model to study this dramatic body form transformation. ...
... Furthermore, our results demonstrated the association between body elongation Table 4 The selective pressure of 13 protein-coding genes in mitogenomes. and limb reduction in Squamata, consistent with previous studies in amphibians (Parra-Olea and Wake, 2001;Bonett and Blair, 2017), reptiles Brandley et al., 2008;Grizante et al., 2012) and mammals (Buchholtz and Schur, 2004;Buchholtz et al., 2007;Law et al., 2019), prompting that limbreduction accompanied with elongated body forms tend to be a pervasive rule in vertebrate. Previous studies had put forward three locomotive patterns for squamates with different degrees of limb loss: limbed squamates used their limbs for movement, limb-reduced squamates moved with their remaining limbs alternately with body swing and limbless squamates (including limbless lizards and snakes) relied on completely body swing (Gans, 1986;Gans and Gasc, 1990;Gans and Fusari, 1994). ...
Limb reduction in Squa ma ta present the dra ma tic cha racteristic to focus a nd usually accompa nied with pa rticula rly morphological modifica tions, impacting tremendous locomotion cha nging a nd might genera te different energy requirement. Herein, we combined both morphological a nd mitochondrial genomic da ta to explore the evolution of phenotypic tra nsforma tion a nd mitochondrial genome of limbless a nd body-elonga ted squa ma tes. We collected phenotypic measurements of 503 individuals, representing limbed or limbless taxa across all major lineages in Squa ma ta to investiga te the morphological correla tions with limb-reduction. Furthermore, we provided the mitochondrial genome of the representa tive limbless a nd elonga ted species Dibamus bourreti (Angel, 1935) to detect selective constra ints on limbless clades with published mitogenomes of other squa ma te reptiles. Our results evidenced tha t body elonga tion had certa in nega tive rela tionship with limb-reduction in Squa ma ta lineage a nd Lacertilia lineage (R = –0.495, P < 2 . 2 e -16 ; R= –0.332, P = 1.1e-13 , r e s p e c t i v e l y ) , while ta il length showed slight correla tion in both clades (R = 0 .156 , P = 4.3e-04; R= 0 .192 , P = 2.1e-05, respectively ). Besides, detection demonstra ted tha t AT P6 has experienced accelera ted evolution a mong limbless lineages, suggesting selective pressure on mitogenomes may play a n essential role in energy dispa rity for locomotion of limbed a nd limbless squamates.
... A cavity is formed between the fracture blocks, resulting in an "empty shell" phenomenon, resulting in an increase in the rate of nonunion [4][5][6]. Because of the large space between vertebral fracture blocks, the fretting of internal bone mass is also one of the physical factors of vertebral fracture nonunion [7]. Stabilizing vertebral internal fracture blocks plays a positive role in vertebral fracture healing. ...
... Relative to mammals that are flexible in their activity times, we found diurnal species decrease in body mass, but increase in head-body length with increasing urbanization. An elongated body form may represent a locomotory adaptation, allowing diurnal mammals to exploit more shelters (e.g., burrows 69 ). With increasing urbanization, nocturnal mammals demonstrate a minimal decrease in head-body length, but increase in mass similar to species that are active anytime. ...
Anthropogenically-driven climate warming is a hypothesized driver of animal body size reductions. Less understood are effects of other human-caused disturbances on body size, such as urbanization. We compiled 140,499 body size records of over 100 North American mammals to test how climate and human population density, a proxy for urbanization, and their interactions with species traits, impact body size. We tested three hypotheses of body size variation across urbanization gradients: urban heat island effects, habitat fragmentation, and resource availability. Our results demonstrate that both urbanization and temperature influence mammalian body size variation, most often leading to larger individuals, thus supporting the resource availability hypothesis. In addition, life history and other ecological factors play a critical role in mediating the effects of climate and urbanization on body size. Larger mammals and species that utilize thermal buffering are more sensitive to warmer temperatures, while flexibility in activity time appears to be advantageous in urbanized areas. This work highlights the value of using digitized, natural history data to track how human disturbance drives morphological variation.
... Arguing that this group should be recognized as a distinct genus, Hassanin et al. (2021) contended that the correct group name should be Grammogale Cabrera, 1940. Further complicating matters of nomenclature, other scientists have continued to recognize the American mink as Mustela vison (Flynn et al., 2005;2019;Burgin et al., 2020). relationships, nomenclature allows both the storage and retrieval of biological information that is shared by evolutionary descent (Mayr, 1969;Benton, 2007). ...
... Abramov (2000) subsequently elevated Neovison to generic rank and presented an unsupported tree of relationships that would justify his nomenclatural proposals: American mink appeared as sister to all species of Mustela, M. frenata and M. erminea were grouped as sisters, and M. felipei and M. africana were only distantly related. This topology for Mustela is contradicted by all subsequent phylogenetic analyses, including Koepfli and Wayne (2003), Flynn et al. (2005), Koepfli et al. (2008), Harding andSmith (2009), Sato et al. (2012), and 2019). American mink are sister to all other Mustela only in analyses that lack its closer relatives M. frenata, M. felipei, and M. africana. ...
... Evolutionary shifts to more elongate body plans have been hypothesized to serve as an innovation that facilitated the exploitation of novel grassland habitats and rodent prey during the Mid-Miocene to Pleistocene, which ultimately led to the clade's increased species richness (Law et al. 2018b;Law 2019;Law et al. 2019). Nevertheless, performance testing is still needed to show the adaptive link between elongate body plans with subterranean locomotion. ...
... Body shape is one of the most prominent features of vertebrate morphology with important influences on the physiology, performance, and ecology of organisms (Brown and Lasiewski 1972;Sharpe et al. 2015;Ward et al. 2015;Law et al. 2019;Morinaga and Bergmann 2020 morphological traits such as vertebral shape may better capture the specific structures of the vertebral column that more directly facilitate ecological functions (Boszczyk et al. 2001;Pierce et al. 2011;Galis et al. 2014;Randau et al. 2017;Jones et al. 2018;Williams et al. 2019). ...
Morphological diversity is often attributed as adaptations to distinct ecologies. Although biologists have long hypothesized that distinct ecologies drive the evolution of body shape, these relationships are rarely tested across macroevolutionary scales in mammals. Here, I tested hypotheses that locomotor, hunting, and dietary ecologies influenced body shape evolution in carnivorans, a morphologically and ecologically diverse clade of mammals. I found that adaptive models with ecological trait regimes were poor predictors of carnivoran body shape and the underlying morphological components that contribute to body shape variation. Instead, the best-supported model exhibited clade-based evolutionary shifts, indicating that the complexity and variation of body shape landscape cannot be effectively captured by a priori ecological regimes. However, ecological adaptations of body shapes cannot be ruled out, as aquatic and terrestrial carnivorans exhibited opposite allometric patterns of body shape that may be driven by different gravitational constraints associated with these different environments. Similar to body size, body shape is a prominent feature of vertebrate morphology that may transcend one-to-one mapping relationships between morphology and ecological traits, enabling species with distinct body shapes to exploit similar resources and exhibit similar ecologies. Together, these results demonstrate that the multidimensionality of both body shape morphology and ecology makes it difficult to disentangle the complex relationship among morphological evolution, ecological diversity, and phylogeny across macroevolutionary scales.
