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Shared extremes by ectotherms and endotherms: Body elongation in mustelids is associated with small size and reduced limbs

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Abstract

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 mammals (red panda, skunks, raccoons, and weasels) using the head‐body elongation ratio. We also examined the morphological changes that may underlie the evolution towards more extreme body plans. We found that a mustelid clade comprised of the subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae exhibited an evolutionary transition towards more elongate bodies. Furthermore, we discovered that elongation of the body is associated with the evolution of other key traits such as a reduction in body size and a reduction in forelimb length but not hindlimb length. This relationship between body elongation and forelimb length has not previously been quantitatively established for mammals but is consistent with trends exhibited by ectothermic vertebrates and suggests a common pattern of trait covariance associated with body shape evolution. This study provides the framework for documenting body shapes across a wider range of mammalian clades to better understand the morphological changes influencing shape disparity across all vertebrates. This article is protected by copyright. All rights reserved

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... Recent work on musteloid trait diversification also suggests that multiple evolutionary processes underlie the mustelid body plan. Law et al. (2019) found that the clade composed of the Helictidinae, Ictonychinae, Guloninae, Mustelinae and Lutrinae ( Fig. 1) underwent an evolutionary transition towards a more elongate body, albeit more likely due to a multi-rate BM process, and Law (2019) found that the subclade of the Ictonychinae, Mustelinae and Lutrinae experienced shifts in selective regime in cranial robustness and body size compared to other musteloids. Law et al. (2019) also found that fore-and hindlimb length likely evolved according a multi-rate BM process that distinguishes between a clade of shorter limbed mustelids (Ictonychinae, Mustelinae and Lutrinae) and other mustelids. ...
... Law et al. (2019) found that the clade composed of the Helictidinae, Ictonychinae, Guloninae, Mustelinae and Lutrinae ( Fig. 1) underwent an evolutionary transition towards a more elongate body, albeit more likely due to a multi-rate BM process, and Law (2019) found that the subclade of the Ictonychinae, Mustelinae and Lutrinae experienced shifts in selective regime in cranial robustness and body size compared to other musteloids. Law et al. (2019) also found that fore-and hindlimb length likely evolved according a multi-rate BM process that distinguishes between a clade of shorter limbed mustelids (Ictonychinae, Mustelinae and Lutrinae) and other mustelids. However, body elongation in mustelids was found to be associated with shortening of the forelimb only and not the hindlimb. ...
... However, body elongation in mustelids was found to be associated with shortening of the forelimb only and not the hindlimb. The results of Law et al. (2018Law et al. ( , 2019 and Law (2019) Looking at parameter estimates for the best fitting models reveals wide confidence limits (Supporting Information, Tables S2, S3), as was found when fitting diversification models to mustelid forelimb morphology (Kilbourne, 2017). Though the confidence limits for phenotypic optima of some best fitting models do not overlap (e.g. ...
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Background Morphological diversity of limb bone lengths, diameters, and proportions in mammals is known to vary strongly with locomotor habit. It remains less well known how different locomotor habits are correlated with cross-sectional traits of the limb skeleton, such as cross-sectional area (CSA), second moments of area (SMA), and section modulus (MOD) and whether these traits have evolved adaptively. CSA and SMA represent the bone’s resistance to axial compression and bending, respectively, whereas MOD represents bone structural strength related to shape. Sampling 28 species of mustelids, a carnivoran lineage with diverse locomotor habits, we tested for differences in humeral, radial, and ulnar cross-sectional traits among specialists for climbing, digging, and swimming, in addition to generalists. Given that the limbs of digging specialists function in the dense substance of soil, and that swimming specialists need to counteract buoyancy, we predicted that these mustelids with these specializations should have the greatest values of cross-sectional traits. Results We analyzed cross-sectional traits (calculated via μCT scanning and rendered dimensionless) in 5% increments along a bone’s length and found significant differences among locomotor habits, though differences in ulnar cross-sectional traits were fewer than those for the humerus and radius. Swimming specialists had the greatest values of cross-sectional traits, followed by digging specialists. Climbing specialists had the lowest values of cross-sectional traits. However, phylogenetic affinity underlies these results. Fitting models of trait evolution to CSA and SMA revealed that a multi-rate Brownian motion model and a multi-optima Ornstein-Uhlenbeck model are the best-fitting models of evolution for these traits. However, inspection of α-values uncovered that many of the OU models did not differ from a Brownian motion model. Conclusions Within Mustelidae, differences in limb function and locomotor habit influence cross-sectional traits in ways that produce patterns that may diverge from adaptive patterns exhibited by external traits (e.g., bone lengths) of the mammalian limb skeleton. These results suggest that not all the traits of a single organ evolve under a single evolutionary process and that models of trait evolution should be fit to a range of traits for a better understanding of the evolution of the mammalian locomotor system. Electronic supplementary material The online version of this article (10.1186/s12862-019-1349-8) contains supplementary material, which is available to authorized users.
... weasels, polecats, otters) [21][22][23]. Recent work corroborated these hypotheses, revealing evolutionary shifts towards small, elongate body plans during the Middle to Late Miocene that may have facilitated diversification by allowing mustelids to chase prey in burrows and small crevices [24]. Although these studies revealed associated transitions between body size and shape and the behaviour of entering subterranean habitats, it remains to be explored whether traits tied directly to prey capture and consumption also exhibited evolutionary shifts near the MMCT. ...
... Second, I examined the timing of evolutionary shifts in body size and body shape. Previous work used a model selection approach with a priori hypotheses to determine where evolutionary shifts in body size and shape occurred between designated clades [24]. However, these a priori hypotheses represented only a fraction of all possible shifts and may unintentionally hide additional shifts that are important in driving trait evolution [30]. ...
... I also included the other three musteloid families to provide a phylogenetic background and increase statistical robustness for model fitting [31]. Cranial shape, body size and body shape measurements of 60 extant musteloids were obtained from [27,23], and [24], respectively (see full methods in electronic supplementary material). ...
Article
Environmental changes can lead to evolutionary shifts in phenotypic traits, which in turn facilitate the exploitation of novel adaptive landscapes and lineage diversification. The global cooling, increased aridity and expansion of open grasslands during the past 50 Myr are prime examples of new adaptive landscapes that spurred lineage and ecomorphological diversity of several mammalian lineages such as rodents and large herbivorous megafauna. However, whether these environmental changes facilitated evolutionary shifts in small- to mid-sized predator morphology is unknown. Here, I used a complete cranial and body morphological dataset to examine the timing of evolutionary shifts in cranial shape, body size and body shape within extant mustelids (martens, otters, polecats and weasels) during the climatic and environmental changes of the Cenozoic. I found that evolutionary shifts in all three traits occurred within extant mustelid subclades just after the onset of the Mid-Miocene Climate Transition. These mustelid subclades first shifted towards more elongate body plans followed by concurrent shifts towards smaller body sizes and more robust crania. I hypothesize that these cranial and body morphological shifts enabled mustelids to exploit novel adaptive zones associated with the climatic and environmental changes of the Mid to Late Miocene, which facilitated significant increases in clade carrying capacity.
... In addition to these three specializations, weasels exhibit a more generalized locomotor habit. In spite of a flurry of recent studies, mustelids have been used as an ideal group to understand locomotor form-function relationships and their evolution for nearly four decades [7][8][9][10][11][12]. Though the majority of these studies have focused on long bone gross morphology [8][9][10][11][13][14][15][16][17][18], more recent studies have started to investigate cross-sectional properties and microanatomy [8,19]. ...
... It was recently emphasized that body elongation ratio was an important aspect of musteloid evolution [12]. Furthermore, forelimb length was found as reduced in correlation with body elongation (a negative relationship between forelimb length and body length). ...
... Correspondingly, Th.Sp and Conn.D values are higher for the humeral than the femoral head for most specimens (85% and 71%, respectively). However, Tb.Th values for the proximal inter-limb ratio in otters are not particularly low (neither Tb.Sp nor Conn.D values are particularly high), which could have been expected given the stronger reduction of their forelimb when compared to other mustelids [12]. ...
Article
Full-text available
Mustelidae, a carnivoran clade that includes for instance weasels, badgers, otters and martens, has undergone several evolutionary transitions of lifestyle, resulting in specializations for fossorial, natatorial and scansorial locomotion, in addition to more generalized species. The family is therefore regarded as offering an adequate framework for morpho-functional analyses. However, the architecture of the epiphyseal trabecular bone, which is argued to be particularly responsive to the biomechanical environment, has never been studied. Here, we quantify trabecular bone parameters of the proximal and distal epiphyses of the humerus and femur in 29 species of mustelids and assess the differences of these parameters among groups defined a priori based on the aforementioned locomotor types. The parameters are assessed in a phylogenetic framework, taking into account the potential effect on an individual's body mass. The range of variation described by the acquired parameters is relatively restricted when compared to that of other clades. Generalists, however, are featuring a wider range of variation than the other types. While clear discrimination of locomotor types is difficult, some differences were highlighted by our analysis, such as a greater bone fraction associated with the natatorial taxa, which we discuss in a functional context.
... Recent work on musteloid trait diversification also suggests that multiple evolutionary processes underlie the mustelid body plan. Law et al. (2019) found that the clade composed of the Helictidinae, Ictonychinae, Guloninae, Mustelinae and Lutrinae ( Fig. 1) underwent an evolutionary transition towards a more elongate body, albeit more likely due to a multi-rate BM process, and Law (2019) found that the subclade of the Ictonychinae, Mustelinae and Lutrinae experienced shifts in selective regime in cranial robustness and body size compared to other musteloids. Law et al. (2019) also found that fore-and hindlimb length likely evolved according a multi-rate BM process that distinguishes between a clade of shorter limbed mustelids (Ictonychinae, Mustelinae and Lutrinae) and other mustelids. ...
... Law et al. (2019) found that the clade composed of the Helictidinae, Ictonychinae, Guloninae, Mustelinae and Lutrinae ( Fig. 1) underwent an evolutionary transition towards a more elongate body, albeit more likely due to a multi-rate BM process, and Law (2019) found that the subclade of the Ictonychinae, Mustelinae and Lutrinae experienced shifts in selective regime in cranial robustness and body size compared to other musteloids. Law et al. (2019) also found that fore-and hindlimb length likely evolved according a multi-rate BM process that distinguishes between a clade of shorter limbed mustelids (Ictonychinae, Mustelinae and Lutrinae) and other mustelids. However, body elongation in mustelids was found to be associated with shortening of the forelimb only and not the hindlimb. ...
... However, body elongation in mustelids was found to be associated with shortening of the forelimb only and not the hindlimb. The results of Law et al. (2018Law et al. ( , 2019 and Law (2019) Looking at parameter estimates for the best fitting models reveals wide confidence limits (Supporting Information, Tables S2, S3), as was found when fitting diversification models to mustelid forelimb morphology (Kilbourne, 2017). Though the confidence limits for phenotypic optima of some best fitting models do not overlap (e.g. ...
Article
Though form-function relationships of the mammalian locomotor system have been investigated for over a century, recent models of trait evolution have hitherto been seldom used to identify likely evolutionary processes underlying the locomotor system’s morphological diversity. Using mustelids, an ecologically diverse carnivoran lineage, I investigated whether variation in hindlimb skeletal morphology functionally coincides with climbing, digging, swimming and generalized locomotor habits by using 15 linear traits of the femur, tibia, fibula, calcaneum and metatarsal III across 44 species in a principal component analysis. I subsequently fit different models of Brownian motion and adaptive trait diversification individually to each trait. Climbing, digging and swimming mustelids occupy distinct regions of phenotypic space characterized by differences in bone robustness. Models of adaptive and neutral evolution are, respectively, the best fits for long bone lengths and muscle in-levers, suggesting that different kinds of traits may be associated with different evolutionary processes. However, simulations based upon models of best fit reveal low statistical power to rank the models. Though differences in mustelid hindlimb skeletal morphology appear to coincide with locomotor habits, further study, with sampling expanded beyond the Mustelidae, is necessary to better understand to what degree adaptive evolution shapes morphological diversity of the locomotor system.
... 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). ...
Article
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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.
... 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). ...
Article
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.
... 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. ...
Article
Full-text available
A brief review of the phylogeny and nomenclature of the weasels, genus Mustela Linnaeus, 1758 in the broad sense, indicates continuing confusion over the appropriate name for the well-supported American clade included within it. A case is made that the American mink (Neovison vison) and three allied species (Mustela frenata, M. felipei, and M. africana) should now be recognized in the genus Neogale Gray, 1865. The ages and morphological disparities of both Neogale and Mustela sensu stricto indicate that both are in need of comprehensive revisions.
... Law et al. (2018) also found that the decoupled diversification of these two traits in mustelids is linked to body elongation and increased clade carrying capacity. Additionally, Law et al. (2019) found that differing regions of the mustelid axial skeleton diversify under disparate models of trait evolution, with head elongation likely undergoing adaptive evolution and the other regions of the axial skeleton likely undergoing a multi-peak BM model. Furthermore, Law et al. (2019) also found that body elongation is associated with a reduced length of the forelimb but not of the hindlimb. ...
... Additionally, Law et al. (2019) found that differing regions of the mustelid axial skeleton diversify under disparate models of trait evolution, with head elongation likely undergoing adaptive evolution and the other regions of the axial skeleton likely undergoing a multi-peak BM model. Furthermore, Law et al. (2019) also found that body elongation is associated with a reduced length of the forelimb but not of the hindlimb. Together these results strongly suggest that the mustelid body plan can be considered the sum of a suite of several traits diversifying under different models of trait evolution. ...
Article
Full-text available
Synopsis Locomotor habits in mammals are strongly tied to limb bones’ lengths, diameters, and proportions. By comparison, fewer studies have examined how limb bone cross-sectional traits relate to locomotor habit. Here, we tested whether climbing, digging, and swimming locomotor habits reflect biomechanically meaningful differences in three cross-sectional traits rendered dimensionless— cross-sectional area (CSA), second moments of area (SMA), and section modulus (MOD)—using femora, tibiae, and fibulae of 28 species of mustelid. CSA and SMA represent resistance to axial compression and bending, respectively, whereas MOD represents structural strength. Given the need to counteract buoyancy in aquatic environments and soil’s high density, we predicted that natatorial and fossorial mustelids have higher values of cross-sectional traits. For all three traits, we found that natatorial mustelids have the highest values, followed by fossorial mustelids, with both of these groups significantly differing from scansorial mustelids. However, phylogenetic relatedness strongly influences diversity in cross-sectional morphology, as locomotor habit strongly correlates with phylogeny. Testing whether hind limb bone cross-sectional traits have evolved adaptively, we fit Ornstein–Uhlenbeck (OU) and Brownian motion (BM) models of trait diversification to cross-sectional traits. The cross-sectional traits of the femur, tibia, and fibula appear to have, respectively, diversified under a multi-rate BM model, a single rate BM model, and a multi-optima OU model. In light of recent studies on mustelid body size and elongation, our findings suggest that the mustelid body plan—and perhaps that of other mammals—is likely the sum of a suite of traits evolving under different models of trait diversification.
... Elongate forms have evolved many times in most major lineages of vertebrates (Lande 1978;Greer 1991;Caldwell 2003;Wiens et al. 2006;Brandley et al. 2008;Ward and Mehta 2014;Law et al. 2019). Therefore, their convergent evolution is a major theme in vertebrate evolution. ...
... In contrast, body elongation in squamates (lizards and snakes) occurs through the addition of vertebrae and the lengthening of the body or both the body and tail (Bergmann and Irschick 2012;Wiens et al. 2006;Brandley et al. 2008;Bergmann and Morinaga 2019). Finally, in mustelids and whales, the regional lengthening of trunk vertebrae is responsible for elongation of the body rather than increasing the number of vertebrae (Buchholtz 2001;Law et al. 2019). ...
Article
Elongate, snake- or eel-like, body forms have evolved convergently many times in most major lineages of vertebrates. Despite studies of various clades with elongate species, we still lack an understanding of their evolutionary dynamics and distribution on the vertebrate tree of life. We also do not know whether this convergence in body form coincides with convergence at other biological levels. Here, we present the first craniate-wide analysis of how many times elongate body forms have evolved, as well as rates of its evolution and reversion to a non-elongate form. We then focus on five convergently elongate squamate species and test if they converged in vertebral number and shape, as well as their locomotor performance and kinematics. We compared each elongate species to closely related quadrupedal species and determined whether the direction of vertebral or locomotor change matched in each case. The five lineages examined are obscure species from remote locations, providing a valuable glimpse into their biology. They are the skink lizards Brachymeles lukbani, Lerista praepedita, and Isopachys anguinoides, the basal squamate Dibamus novaeguineae, and the basal snake Malayotyphlops cf. ruficaudus. Our results support convergence among these species in the number of trunk and caudal vertebrae, but not vertebral shape. We also find that the elongate species are relatively slower than their limbed counterparts and move with lower frequency and higher amplitude body undulations, with the exception of Isopachys. This is among the first evidence of locomotor convergence across distantly related, elongate species.
... Its evolution and reversion to a quadrupedal form is an excellent opportunity for understanding functional mechanisms of evolutionary reversal. Snake-like body forms have evolved in most major vertebrate clades, including at least 25 times in squamates (lizards and snakes) [17][18][19][20][21][22][23][24]. The prevalent hypothesis is that snake-like forms evolved as an adaptation for fossoriality [25][26][27]. ...
Article
Evolutionary reversals, including re-evolution of lost structures, are commonly found in phylogenetic studies. However, we lack an understanding of how these reversals happen mechanistically. A snake-like body form has evolved many times in vertebrates, and occasionally a quadrupedal form has re-evolved, including in Brachymeles lizards. We use body form and locomotion data for species ranging from snake-like to quadrupedal to address how a quadrupedal form could re-evolve. We show that large, quadrupedal species are faster at burying and surface locomotion than snake-like species, indicating a lack of expected performance trade-off between these modes of locomotion. Species with limbs use them while burying, suggesting that limbs are useful for burying in wet, packed substrates. Palaeoclimatological data suggest that Brachymeles originally evolved a snake-like form under a drier climate probably with looser soil in which it was easier to dig. The quadrupedal clade evolved as the climate became humid, where limbs and large size facilitated fossorial locomotion in packed soils.
... Previous researchers support this hypothesis, positing that small female conspecifics are selected to reduce the high energetic demands associated with reproduction and rearing of young 51,63,70,71 . Most mustelids exhibit elongate body plans 72 and therefore increased energy requirements imposed by an increased surface-to-volume ratio [73][74][75] . Rearing of young further increases these energetic demands; for example, lactating southern sea otters (Enhydra lutris neresis) exhibit daily energy demands 85-110% higher than non-reproductive females 76,77 . ...
Article
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Although sexual size dimorphism (SSD) is widespread across the animal tree of life, the underlying evolutionary processes that influence this phenomenon remains elusive and difficult to tease apart. In this study, I examined how social system (as a proxy for sexual selection) and diet (as a proxy for natural selection) influenced the evolution of SSD in terrestrial carnivorans (Carnivora; Mammalia). Using phylogenetic comparative methods, I found that are territorial solitary and carnivorous carnivorans exhibited selection towards increased degree of male-biased SSD compared to other carnivorans with alternative social systems and diets. I also found the absence of Rensch’s rule across most carnivoran clades, suggestion a relaxation of the influences of sexual selection on SSD. These results together suggest that sexual selection and niche divergence together are important processes influencing the evolution of male-biased SSD in extant terrestrial carnivorans.
... A snake-like form has evolved dozens of times across most major vertebrate lineages, and this transition involves the elongation of the body and the reduction of the limbs [9,19,20]. The prevailing hypotheses for the evolution of this body form are that it is an adaptation for fossoriality and/or inhabiting cluttered habitats because such bodies experience less drag and can fit through narrower gaps than limbed forms [10,[21][22][23]. ...
Article
Dramatic evolutionary transitions in morphology are often assumed to be adaptive in a new habitat. However, these assumptions are rarely tested because such tests require intermediate forms, which are often extinct. In vertebrates, the evolution of an elongate, limbless body is generally hypothesized to facilitate locomotion in fossorial and/or cluttered habitats. However, these hypotheses remain untested because few studies examine the locomotion of species ranging in body form from tetrapod to snake-like. Here, we address these functional hypotheses by testing whether trade-offs exist between locomotion in surface, fossorial and cluttered habitats in Australian Lerista lizards, which include multiple intermediate forms. We found that snake-like species penetrated sand substrates faster than more lizard-like species, representing the first direct support of the adaptation to fossoriality hypothesis. By contrast, body form did not affect surface locomotion or locomotion through cluttered leaf litter. Furthermore, all species with hindlimbs used them during both fossorial and surface locomotion. We found no evidence of a trade-off between fossorial and surface locomotion. This may be either because Lerista employed kinematic strategies that took advantage of both axial- and limb-based propulsion. This may have led to the differential occupation of their habitat, facilitating diversification of intermediate forms.
... 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. ...
... The observed increase in interspecific disparity with body size is a relatively novel result. Countless studies have demonstrated that body size plays an important role in structuring vertebrate phenotypic diversity (e.g., Collar et al. 2011;Dosik and Stayton 2016;Reynolds et al. 2016;Zelditch et al. 2017;Law et al. 2019), but few (if any) have shown that phenotypic diversity is greater among larger taxa. In fact, some studies support the opposite pattern, that phenotypic diversity is greater among smaller species (e.g., Reynolds et al. 2016). ...
Article
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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.
... 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. ...
... The spectrum of shapes is also very broad, ranging from nearly spherical in the marsupial mole Notoryctes typhlops to nearly tubular in species like the fossil vombatiform Silvabestius johnnilandi (compare on Fig. 1). This resembles other instances where an axis of global change related to elongation determines morphological diversification, for example, in the whole body of fishes, lizards, and mustelids (Bergmann and Irschick 2010;Ward and Mehta 2010;Law et al. 2019). Shape diversification partially associated with elongation has also been postulated for the therian cranium (e.g., Cardini et al. 2015), although this so-called "Cranial Rule of Evolutionary Allometry" is also associated with size variation, which has no strong influence in our dataset. ...
Article
Little is known about how the large brains of mammals are accommodated into the dazzling diversity of their skulls. It has been suggested that brain shape is influenced by relative brain size, that it evolves or develops according to extrinsic or intrinsic mechanical constraints, and that its shape can provide insights into its proportions and function. Here, we characterise the shape variation among 84 marsupial cranial endocasts of 57 species including fossils, using 3D geometric morphometrics and virtual dissections. Statistical shape analysis revealed four main patterns: over half of endocast shape variation ranges between elongate and straight to globular and inclined; little allometric variation with respect to centroid size, and none for relative volume; no association between locomotion and endocast shape; limited association between endocast shape and previously published histological cortex volumes. Fossil species tend to have smaller cerebral hemispheres. We find divergent endocast shapes in closely related species and within species, and diverse morphologies superimposed over the main variation. An evolutionarily and individually malleable brain with a fundamental tendency to arrange into a spectrum of elongate‐to‐globular shapes – possibly mostly independent of brain function ‐ may explain the accommodation of brains within the enormous diversity of mammalian skull form. This article is protected by copyright. All rights reserved
... 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. ...
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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.
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The sacrum is a key piece of the vertebrate skeleton, since it connects the caudal region with the presacral region of the vertebral column and the hind limbs through the pelvis. Therefore, understanding its form and function is of great relevance in vertebrate ecomorphology. However, it is striking that morphometric studies that quantify its morphological evolution in relation to function are scarce. The main goal of this study is to investigate the morphological evolution of the sacrum in relation to its function in the mammalian order Carnivora, using three‐dimensional (3D) geometric morphometrics. Principal component analysis under a phylogenetic background indicated that changes in sacrum morphology are mainly focused on the joint areas where it articulates with other parts of the skeleton allowing resistance to stress at these joints caused by increasing muscle loadings. In addition, we demonstrated that sacrum morphology is related to both the length of the tail relativised to the length of the body, and the length of the body relativised to body mass. We conclude that the sacrum in carnivores has evolved in response to the locomotor requirements of the species analysed, but in locomotion, each family has followed alternative morphological solutions to address the same functional demands. The sacrum in carnivores has evolved in response to the locomotor requirements of the species analysed, but in locomotion, each family has followed alternative morphological solutions to address the same functional demands.
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Although convergence is often recognized as a ubiquitous feature across the Tree of Life, whether the underlying traits also exhibit similar evolutionary pathways towards convergent forms puzzles biologists. In carnivoran mammals, “elongate,” “slender,” and “long” are often used to describe and even to categorize mustelids (martens, polecats, and weasels), herpestids (mongooses), viverrids (civets and genets), and other carnivorans together. But just how similar these carnivorans are and whether there is convergence in the morphological component that contribute to elongation has never been assessed. Here, I found that these qualitatively-described elongate carnivorans exhibited incomplete convergence towards elongate bodies compared to other terrestrial carnivorans. In contrast, the morphological components underlying body shape variation do not exhibit convergence despite evidence that these components are more elongate in elongate carnivorans compared to non-elongate carnivorans. Furthermore, these components also exhibited shorter but different phylogenetic half-lives towards more elongate adaptive peaks, indicating that different selective pressures can create multiple pathways to elongation. Incorporating the fossil record will facilitate further investigation of whether body elongation evolved adaptively or if it is simply a retained ancestral trait.
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The diversity of body shapes is one of the most prominent features of phenotypic variation in vertebrates. Biologists, however, still lack a full understanding of the underlying morphological components that contribute to its diversity, particularly in endothermic vertebrates such as mammals. In this study, I tested hypotheses pertaining to the evolution of the cranial and axial components that contribute to the diversity of carnivoran body shapes. I found three trends in the evolution of carnivoran body shapes: 1) carnivorans exhibit diverse body shapes with intrafamilial variation predicted best by family clade age, 2) body shape is driven by strong allometric effects of body size where species become more elongate with decreasing size, and 3) the thoracic and lumbar regions and rib length contribute the most to body shape variation, albeit pathways differ between different families. These results reveal the morphological patterns that led to increased diversity in carnivoran body shapes and provide elucidate the similarities and dissimilarities that govern body shape diversity across vertebrates. This article is protected by copyright. All rights reserved
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Extreme body elongation has occurred repeatedly in the evolutionary history of ray-finned fishes. Lengthening of the anterior-posterior body axis relative to depth and width can involve changes in the cranial skeleton and vertebral column, but to what extent is anatomical evolution determined by selective factors and intrinsic constraints that are shared broadly among closely related lineages? In this study, we fit adaptive (Ornstein-Uhlenbeck) evolutionary models to body shape and its anatomical determinants and identified two instances of extreme elongation by divergent anatomical peak shifts in the Blenniiformes, a radiation of small-bodied substrate-associated marine teleost fishes. Species in the genus Xiphasia (hairtail blennies) evolved toward a peak defined by a highly elongated caudal vertebral region but ancestral cranial and precaudal vertebral morphology. In contrast, a clade that includes the genera Chaenopsis and Lucayablennius (pike and arrow blennies) evolved toward a peak with a long slender skull but ancestral axial skeletal anatomy. Neither set of anatomical peak shifts aligns closely with the major axis of anatomical diversification in other blenniiform fishes. These results provide little evidence that ancestral constraints have affected body shape transformation, and instead suggest that extreme elongation arose with distinct shifts in selective factors and development. This article is protected by copyright. All rights reserved.
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Convergent evolution is often attributed to adaptation of form to function, but it can also result from ecological filtering, exaptation, or nonaptation. Testing among these possibilities is critical to understanding how and why morphological similarities emerge independently in multiple lineages. To address this challenge, we combined multiple preexisting phylogenetic methods to jointly estimate the habitats and morphologies of lineages within a phylogeny. We applied this approach to the invasions of snakes into the marine realm. We utilized a data set for 1,243 extant snake species consisting of newly compiled biome occupancy information and preexisting data on reproductive strategy, body mass, and environmental temperature and elevation. We find evidence for marine clades arising from a variety of aquatic and terrestrial habitats. Furthermore, there is strong evidence of ecological filtering for nonmarine ancestors that were already viviparous, had slightly larger-than-average body sizes, and lived in environments with higher-than-average temperatures and lower-than-average elevations. In aggregate, similarities among independent lineages of marine snakes result from a combination of exaptation and strong ecological filtering. Strong barriers to entry of new habitats appear to be more important than common adaptations following invasions for producing similarities among independent lineages invading a shared, novel habitat.
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Little is known about how the large brains of mammals are accommodated into the dazzling diversity of their skulls. It has been suggested that brain shape is influenced by relative brain size, that it evolves or develops according to extrinsic or intrinsic mechanical constraints, and that its shape can provide insights into its proportions and function. Here, we characterise the shape variation among 84 marsupial cranial endocasts of 57 species including fossils, using 3D geometric morphometrics and virtual dissections. Statistical shape analysis revealed four main patterns: over half of endocast shape variation ranges between elongate and straight to globular and inclined; little allometric variation with respect to centroid size, and none for relative volume; no association between locomotion and endocast shape; limited association between endocast shape and previously published histological cortex volumes. Fossil species tend to have smaller cerebral hemispheres. We find divergent endocast shapes in closely related species and within species, and diverse morphologies superimposed over the main variation. An evolutionarily and individually malleable brain with a fundamental tendency to arrange into a spectrum of elongate-to-globular shapes – possibly mostly independent of brain function - may explain the accommodation of brains within the enormous diversity of mammalian skull form.
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Comparative studies tend to differ from optimality and functionality studies in how they treat adaptation. While the comparative approach focuses on the origin and change of traits, optimality studies assume that adaptations are maintained at an optimum by stabilizing selection. This paper presents a model of adaptive evolution on a macroevolutionary time scale that includes the maintenance of traits at adaptive optima by stabilizing selection as the dominant evolutionary force. Interspecific variation is treated as variation in the position of adaptive optima. The model illustrates how phylogenetic constraints not only lead to correlations between phylogenetically related species, but also to imperfect adaptations. From this model, a statistical comparative method is derived that can be used to estimate the effect of a selective factor on adaptive optima in a way that would be consistent with an optimality study of adaptation to this factor. The method is illustrated with an analysis of dental evolution in fossil horses. The use of comparative methods to study evolutionary trends is also discussed.
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Adaptive radiation is hypothesized to be a primary mechanism that drives the remarkable species diversity and morphological disparity across the Tree of Life. Tests for adaptive radiation in extant taxa are traditionally estimated from calibrated molecular phylogenies with little input from extinct taxa. With 85 putative species in 33 genera and over 400 described extinct species, the carnivoran superfamily Musteloidea is a prime candidate to investigate patterns of adaptive radiation using both extant- and fossil-based macroevolutionary methods. The species diversity and equally impressive ecological and phenotypic diversity found across Musteloidea is often attributed to 2 adaptive radiations coinciding with 2 major climate events, the Eocene-Oligocene transition and the Mid-Miocene Climate Transition. Here, we compiled a novel time-scaled phylogeny for 88% of extant musteloids and used it as a framework for testing the predictions of adaptive radiation hypotheses with respect to rates of lineage diversification and phenotypic evolution. Contrary to expectations, we found no evidence for rapid bursts of lineage diversification at the origin of Musteloidea, and further analyses of lineage diversification rates using molecular and fossil-based methods did not find associations between rates of lineage diversification and the Eocene-Oligocene transition or Mid-Miocene Climate Transition as previously hypothesized. Rather, we found support for decoupled diversification dynamics driven by increased clade carrying capacity in the branches leading to a subclade of elongate mustelids. Supporting decoupled diversification dynamics between the subclade of elongate mustelids and the ancestral musteloid regime is our finding of increased rates of body length evolution, but not body mass evolution, within the decoupled mustelid subclade. The lack of correspondence in rates of body mass and length evolution suggest that phenotypic evolutionary rates under a single morphological metric, even one as influential as mass, may not capture the evolution of diversity in clades that exhibit elongate body shapes. The discordance in evolutionary rates between body length and body mass along with evidence of decoupled diversification dynamics suggests that body elongation might be an innovation for the exploitation of novel Mid-Miocene resources, resulting in the radiation of some musteloids.
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Almost all mammals have seven vertebrae in their cervical spines. This consistency represents one of the most prominent examples of morphological stasis in vertebrae evolution. Hence, the requirements associated with evolutionary modifications of neck length have to be met with a fixed number of vertebrae. It has not been clear whether body size influences the overall length of the cervical spine and its inner organization (i.e., if the mammalian neck is subject to allometry). Here, we provide the first large scale analysis of the scaling patterns of the cervical spine and its constituting cervical vertebrae. Our findings reveal that the opposite allometric scaling of C1 and C2-C7 accommodate the increase of neck bending moment with body size. The internal organization of the neck skeleton exhibits surprisingly uniformity in the vast majority of mammals. Deviations from this general pattern only occur under extreme loading regimes associated with particular functional and allometric demands. Our results indicate that the main source of variation in the mammalian neck stems from the disparity of overall cervical spine length. The mammalian neck reveals how evolutionary disparity manifests itself in a structure that is otherwise highly restricted by meristic constraints. This article is protected by copyright. All rights reserved
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At least 17 carnivoran taxa occur in the Pliocene Glenns Ferry Formation at Hagerman Fossil Beds National Monument (HAFO), Idaho. This assemblage was examined for stratigraphic changes in species distribution, specimen abundance, and species diversity. Three relatively common mustelids, Trigonictis cookii, Trigonictis macrodon, and Mustela rexroadensis, occur at most stratigraphic levels, but are absent during an interval coinciding with the coolest time segment at HAFO. It is within this gap that two less-common mustelids, Ferinestrix vorax and Buisnictis breviramus, first appear at HAFO; they persist up-section with the more common mustelids listed above. Specimens of Borophagus hilli are restricted to the warm intervals at HAFO, irrespective of the relative abundance of surface water. The other canid at HAFO, Canis lepophagus, is more abundant during the dry intervals at HAFO, regardless of the estimated paleotemperature. Most remarkable is the recovery of many taxa impacted by abrupt climate change, although a notable change is the much higher relative abundance of carnivoran species following a return to warm temperatures.
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The weasels (Mustela spp.) are a group of small mustelid carnivores that originated in the late Pliocene and are now distributed throughout the Holarctic region. Mustela erminea, the stoat or ermine, is circumboreal north of about 40°N. M. nivalis is sympatric with erminea over most of the same area. It includes two distinct subspecies, the common weasel of western Europe and Britain (M. n. vulgaris Erxleben 1777), and the least weasel of northern Scandinavia, USSR, and North America (M. n. nivalis Linnaeus 1766), which are different in appearance and range (Stolt 1979) but interbreed in captivity (F. Frank, pers. comm.). A third species, M. frenata, the long-tailed weasel, is confined to America, from about 50°N to about 15°S.
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Comparative studies tend to differ from optimality and functionality studies in how they treat adaptation. While the comparative approach focuses on the origin and change of traits, optimality studies assume that adaptations are maintained at an optimum by stabilizing selection. This paper presents a model of adaptive evolution on a macroevolutionary time scale that includes the maintenance of traits at adaptive optima by stabilizing selection as the dominant evolutionary force. Interspecific variation is treated as variation in the position of adaptive optima. The model illustrates how phylogenetic constraints nor only lead to correlations between phylogenetically related species, but also to imperfect adaptations. From this model, a statistical comparative method is derived that can be used to estimate the effect of a selective factor on adaptive optima in a way that would be consistent with an optimality study of adaptation to this factor. The method is illustrated with an analysis of dental evolution in fossil horses. The use of comparative methods to study evolutionary trends is also discussed.
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Tropical reef fishes are widely regarded as being perhaps the most morphologically diverse vertebrate assemblage on earth, yet much remains to be discovered about the scope and patterns of this diversity. We created a morphospace of 2,939 species spanning 56 families of tropical Indo-Pacific reef fishes and established the primary axes of body shape variation, the phylogenetic consistency of these patterns, and whether dominant patterns of shape change can be accomplished by diverse underlying changes. Principal component analysis showed a major axis of shape variation that contrasts deep-bodied species with slender, elongate forms. Furthermore, using custom methods to compare the elongation vector (axis that maximizes elongation deformation) and the main vector of shape variation (first principal component) for each family in the morphospace, we showed that two thirds of the families diversify along an axis of body elongation. Finally, a comparative analysis using a principal coordinate analysis based on the angles among first principal component vectors of each family shape showed that families accomplish changes in elongation with a wide range of underlying modifications. Some groups such as Pomacentridae and Lethrinidae undergo decreases in body depth with proportional increases in all body regions, while other families show disproportionate changes in the length of the head (e.g., Labridae), the trunk or caudal region in all combinations (e.g., Pempheridae and Pinguipedidae). In conclusion, we found that evolutionary changes in body shape along an axis of elongation dominates diversification in reef fishes. Changes in shape on this axis are thought to have immediate implications for swimming performance, defense from gape limited predators, suction feeding performance and access to some highly specialized habitats. The morphological modifications that underlie changes in elongation are highly diverse, suggesting a role for a range of developmental processes and functional consequences.
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Phylogenetic analyses which include fossils or molecular sequences that are sampled through time require models that allow one sample to be a direct ancestor of another sample. As previously available phylogenetic inference tools assume that all samples are tips, they do not allow for this possibility. We have developed and implemented a Bayesian Markov Chain Monte Carlo (MCMC) algorithm to infer what we call sampled ancestor trees, that is, trees in which sampled individuals can be direct ancestors of other sampled individuals. We use a family of birth-death models where individuals may remain in the tree process after the sampling, in particular we extend the birth-death skyline model [Stadler et al, 2013] to sampled ancestor trees. This method allows the detection of sampled ancestors as well as estimation of the probability that an individual will be removed from the process when it is sampled. We show that sampled ancestor birth-death models where all samples come from different time points are non-identifiable and thus require one parameter to be known in order to infer other parameters. We apply this method to epidemiological data, where the possibility of sampled ancestors enables us to identify individuals that infected other individuals after being sampled and to infer fundamental epidemiological parameters. We also apply the method to infer divergence times and diversification rates when fossils are included among the species samples, so that fossilisation events are modelled as a part of the tree branching process. Such modelling has many advantages as argued in literature. The sampler is available as an open-source BEAST2 package (https://code.google.com/p/sampled ancestors/).
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Sea otters (Enhydra lutris) have the highest mass-specific metabolic rate of any marine mammal, which is superimposed on the inherently high costs of reproduction and lactation in adult females. These combined energetic demands have been implicated in the poor body condition and increased mortality of female sea otters nearing the end of lactation along the central California coast. However, the cost of lactation is unknown and currently cannot be directly measured for this marine species in the wild. Here, we quantified the energetic demands of immature sea otters across five developmental stages as a means of assessing the underlying energetic challenges associated with pup rearing that may contribute to poor maternal condition. Activity-specific metabolic rates, daily activity budgets and field metabolic rates (FMR) were determined for each developmental stage. Mean FMR of pre-molt pups was 2.29±0.81 MJ day(-1) and increased to 6.16±2.46 and 7.41±3.17 MJ day(-1) in post-molt pups and dependent immature animals, respectively. Consequently, daily energy demands of adult females increase 17% by 3 weeks postpartum and continue increasing to 96% above pre-pregnancy levels by the average age of weaning. Our results suggest that the energetics of pup rearing superimposed on small body size, marine living and limited on-board energetic reserves conspire to make female sea otters exceptionally vulnerable to energetic shortfalls. By controlling individual fitness, maternal behavior and pup provisioning strategies, this underlying metabolic challenge appears to be a major factor influencing current population trends in southern sea otters (Enhydra lutris nereis).
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The evolution of grasses using C₄ photosynthesis and their sudden rise to ecological dominance 3 to 8 million years ago is among the most dramatic examples of biome assembly in the geological record. A growing body of work suggests that the patterns and drivers of C₄ grassland expansion were considerably more complex than originally assumed. Previous research has benefited substantially from dialog between geologists and ecologists, but current research must now integrate fully with phylogenetics. A synthesis of grass evolutionary biology with grassland ecosystem science will further our knowledge of the evolution of traits that promote dominance in grassland systems and will provide a new context in which to evaluate the relative importance of C₄ photosynthesis in transforming ecosystems across large regions of Earth.
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Biologists employ phylogenetic comparative methods to study adaptive evolution. However, none of the popular methods model selection directly. We explain and develop a method based on the Ornstein-Uhlenbeck (OU) process, first proposed by Hansen. Ornstein-Uhlenbeck models incorporate both selection and drift and are thus qualitatively different from, and more general than, pure drift models based on Brownian motion. Most importantly, OU models possess selective optima that formalize the notion of adaptive zone. In this article, we develop the method for one quantitative character, discuss interpretations of its parameters, and provide code implementing the method. Our approach allows us to translate hypotheses regarding adaptation in different selective regimes into explicit models, to test the models against data using maximum-likelihood-based model selection techniques, and to infer details of the evolutionary process. We illustrate the method using two worked examples. Relative to existing approaches, the direct modeling approach we demonstrate allows one to explore more detailed hypotheses and to utilize more of the information content of comparative data sets than existing methods. Moreover, the use of a model selection framework to simultaneously compare a variety of hypotheses advances our ability to assess alternative evolutionary explanations.
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We developed a linear-time algorithm applicable to a large class of trait evolution models, for efficient likelihood calculations and parameter inference on very large trees. Our algorithm solves the traditional computational burden associated with two key terms, namely the determinant of the phylogenetic covariance matrix V and quadratic products involving the inverse of V. Applications include Gaussian models such as Brownian motion (BM) derived models like Pagel's lambda, kappa, delta and the early-burst model; Ornstein-Uhlenbeck models to account for natural selection with possibly varying selection parameters along the tree; as well as non-Gaussian models such as phylogenetic logistic regression, phylogenetic Poisson regression and phylogenetic generalized linear mixed models. Outside of phylogenetic regression, our algorithm also applies to phylogenetic principal component analysis, phylogenetic discriminant analysis or phylogenetic prediction. The computational gain opens up new avenues for complex models or extensive resampling procedures on very large trees. We identify the class of models that our algorithm can handle as all models whose covariance matrix has a 3-point structure. We further show that this structure uniquely identifies a rooted tree whose branch lengths parametrize the trait covariance matrix, which acts as a similarity matrix. The new algorithm is implemented in the R package phylolm, including functions for phylogenetic linear regression and phylogenetic logistic regression.
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SYNOPSIS. The evolution of fully aquatic mammals from quadrupedal, terrestrial mammals was associated with changes in morphology and swimming mode. Drag is minimized by streamlining body shape and appendages. Improvement in speed, thrust production and efficiency is accomplished by a change of swimming mode. Terrestrial and semiaquatic mammals employ drag-based propulsion with paddling appendages, whereas fully aquatic mammals use lift-based propulsion with oscillating hydrofoils. Aerobic efficiencies are low for drag-based swimming, but reach a maximum of 30% for lift-based propulsion. Propulsive efficiency is over 80% for lift-based swimming while only 33% for paddling. In addition to swimming mode, the transition to high performance propul- sion was associated with a shift from surface to submerged swimming providing a reduction in transport costs. The evolution of aquatic mam- mals from terrestrial ancestors required increased swimming performance with minimal compromise to terrestrial movement. Examination of mod- ern analogs to transitional swimming stages suggests that only slight mod- ification to the neuromotor pattern used for terrestrial locomotion is re- quired to allow for a change to lift-based propulsion.
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One can predict fasting endurance in mammals by dividing energy reserves by their rate of use. The result, the scaling of fasting endurance, favors large body size. This relationship is of primary significance in seasonal environments where organisms must endure occasional periods of fasting.-from Authors
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Convergent evolution can occur through similar or different evolutionary pathways, which are the sequences of trait changes that led to convergent phenotypic endpoints. These evolutionary pathways may differ, owing to historically contingent events during the evolution of each lineage, or can arise deterministically due to similar histories of selection or evolutionary constraints. Thus, the relative contribution of determinism and contingency to the evolutionary history of convergent clades affects the evolutionary pathway that each has taken. We tested for morphological convergence in body elongation and limb reduction and the evolutionary pathways that gave rise to them in two major clades of Lerista, a species-rich genus of semi-fossorial lizards endemic to Australia. Our analyses showed strong evidence that the two clades evolved deterministically: both clades shared multiple convergent trait optima and similar patterns of integration of the hind limbs. However, the analyses also showed evidence of historical contingency because not all trait optima were realized by both clades, front limbs were not similarly integrated, and the body parts related by linear or threshold relationships differed between clades. Our findings suggest convergence occurs through deterministic pathways that are nevertheless contingent on historical events, and may have functional and ecological implications for convergent organisms.
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Moray eels comprise a large radiation of elongate marine predators that are thought to swallow large prey whole but also circumvent gape constraints by manipulating prey into more manageable pieces. Prey manipulation behaviors include shaking, rotation, knotting, and ramming prey against another object to assist in swallowing. Most morays feed on a wide variety of prey that vary in mechanical properties such as stiffness and toughness, which could potentially affect feeding behaviors. There is little diet data informing us of the maximum prey size morays can swallow whole and whether maximum prey size differs between prey types. Our study examines feeding behaviors for the California moray (Gymnothorax mordax) in the laboratory. We recorded morays feeding on freshly thawed fish and cephalopods of varying size. We found that prey size had a strong effect on total feeding time and manipulation duration for both fish and cephalopods. While morays were observed using a diversity of prey manipulation behaviors and the durations for each of these behaviors increased with prey size, prey type had no effect on manipulation behaviors employed. Total manipulation duration, however, comprised a greater proportion of total feeding time for fish compared to cephalopods. As relative prey mass (RPM) increased for cephalopods, morays spent a greater proportion of their total feeding time transporting prey. Transport rate was higher for cephalopod prey but the relationship between RPM and transport rate was negative for both prey types. Despite this decrease in transport rate, we attribute the lower total feeding times for larger cephalopod prey compared to fish to behavioral tactics of morays. Morays used the corners of the aquaria to aid in the transport of larger cephalopod prey. We hypothesize that the deformable tissues of cephalopods and the presumably low coefficient of friction of their thawed mantles and tentacles may be difficult for the recurved teeth on the pharyngeal jaws to pierce and grip during transport.
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This paper questions the common explanation of surplus killing by small mustelids as an incidental response to superabundance of prey. Alternatively, we propose that surplus hunting in weasels is a regular seasonal (winter) strategy, a mean of: (1) balancing the cold-inducted increase of energy need, (2) compensating the concurrent restriction in hunting activity, (3) constantly supplying a "buffer" cache against unpredictable winter conditions. We tested this prediction in seminatural conditions in nineteen experiments performed over three years with 8 nonreproductive weasels Mustela nivalis Linnaeus, 1766 and very high densities of rodents, mainly the bank voles Clethrionomys glareolus (Schreber, 1780). Each experiment lasted from 6 to 25 days.
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Through the Cenozoic, paleoclimate records show general trends of global cooling and increased aridity, and environments in North America shifted from predominantly forests to more open habitats. Paleobotanical records indicate grasses were present on the continent in the Eocene; however, paleosol and phytolith studies indicate that open habitats did not arise until the late Eocene or even later in the Oligocene. Studies of large mammalian herbivores have documented changes in ecomorphology and community structure through time, revealing that shifts in mammalian morphology occurred millions of years after the environmental changes thought to have triggered them. Smaller mammals, like rodents and lagomorphs, should more closely track climate and habitat changes due to their shorter generation times and smaller ranges, but these animals have received much less study. To examine changes in smaller mammals through time, we have assembled and analyzed an ecomorphological database of all North American rodent and lagomorph species.
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Animals that are specialized for a particular habitat or mode of locomotion often demonstrate locomotor efficiency in a focal environment when compared to a generalist species. However, measurements of these focal habitats or behaviors are often difficult or impossible to do in the field. In this study, the energetics and kinematics of simulated tunnel locomotion by two unrelated semi-fossorial mammals, the ferret and degu, were analyzed using open-flow respirometry and digital video. Animals were trained to move inside of normal (unconstrained, overground locomotion) and height-decreased (simulated tunnel, adjusted to tolerance limits for each species) Plexiglas chambers that were mounted flush onto a treadmill. Both absolute and relative tunnel performance differed between the species; ferrets tolerated a tunnel height that forced them to crouch at nearly 25% lower hip height than in an unconstrained condition, while degus would not perform on the treadmill past a ∼9% reduction in hip height. Both ferrets and degus exhibited significantly higher metabolic rates and cost of transport (CoT) values when moving in the tunnel condition relative to overgound locomotion. When comparing CoT values across small (<10kg) mammals, ferrets demonstrated a lower than predicted metabolic cost during both tunnel and terrestrial locomotion, whereas degus were very close to line of best fit. Although tunnel locomotion requires a more striking change in posture for ferrets, ferrets are more efficient locomotors in both conditions than mammals of similar mass.
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Lifetime reproductive success of males is often dependent upon the ability to physically compete for mates. However, species variation in social structure leads to differences in the relative importance of intraspecific aggression. Here we present a large comparative data set on sexual dimorphism in skeletal shape in Carnivora to test the hypotheses that carnivorans exhibit sexual dimorphism in skeletal anatomy that is reflective of greater specialization for physical aggression in males relative to females and that this dimorphism is associated with the intensity of sexual selection. We tested these hypotheses using a set of functional indices predicted to improve aggressive performance. Our results indicate that skeletal shape dimorphism is widespread within our sample. Functional traits thought to enhance aggressive performance are more pronounced in males. Phylogenetic model selection suggests that the evolution of this dimorphism is driven by sexual selection, with the best-fitting model indicating greater dimorphism in polygynous versus non-polygynous species. Skeletal shape dimorphism is correlated with body size dimorphism, a common indicator of the intensity of male-male competition, but not with mean body size. These results represent the first evidence of sexual dimorphism in the primary locomotor system of a large sample of mammals. This article is protected by copyright. All rights reserved.
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Major morphological transformations, such as the evolution of elongate body shape in vertebrates, punctuate evolutionary history. A fundamental step in understanding the processes that give rise to such transformations is identification of the underlying anatomical changes. But as we demonstrate in this study, important insights can also be gained by comparing these changes to those that occur in ancestral and closely related lineages. In labyrinth fishes (Anabantoidei), rapid evolution of a highly derived torpedo-shaped body in the common ancestor of the pikehead (Luciocephalus aura and L. pulcher) occurred primarily through exceptional elongation of the head, with secondary contributions involving reduction in body depth and lengthening of the precaudal vertebral region. This combination of changes aligns closely with the primary axis of anatomical diversification in other anabantoids, revealing that pikehead evolution involved extraordinarily rapid change in structures that were ancestrally labile. Finer-scale examination of the anatomical components that determine head elongation also shows alignment between the pikehead evolutionary trajectory and the primary axis of cranial diversification in anabantoids, with much higher evolutionary rates leading to the pikehead. Altogether, our results show major morphological transformation stemming from extreme change along a shared morphological axis in labyrinth fishes. This article is protected by copyright. All rights reserved
Chapter
Body elongation and limblessness have evolved significantly within Tetrapoda, typically associated with aquatic, fossorial, crevice dwelling, or grass-swimming lifestyles. Some lineages of secondarily elongate vertebrates (for example, limbless skinks) have solved the concomitant problem of reduction in size of the feeding apparatus by eating many tiny items, whereas others (for example, some caecilians) shear ingestible chunks out of large prey. Many advanced snakes achieved a third solution by radically restructuring their heads and feeding infrequently on large items; perhaps not coincidentally. Among limbless squamate reptiles, only Serpentes has achieved substantial adaptive radiation and high species richness. More than 2,500 species of living snakes inhabit most temperate and tropical land masses, and they often are prominent predators in terrestrial, arboreal, fossorial, aquatic, and even marine faunas. Snakes eat prey as different as onycophorans, fish eggs, centipedes, cormorants, and porcupines; many species commonly consume individual items weighing 20% of their own mass, and some venomous species occasionally subdue and eat prey that exceed their own mass by as much as 50%. This chapter first briefly surveys snake diversity and then examines in detail the functional and morphological aspects of capturing, swallowing, and processing prey that generally characterize relatively derived subgroups. It only touches on sensory aspects of feeding.
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The feeding behavior of three species of muraenid eels was divided into two parts: detection-orientation-assessment-capture, and manipulation-feed. Home, search, strike, orient, "M," rotate, knot, shake, release, probe, and feed were mutually exclusive behaviors observed in feeding sequences. Feeding episodes, analyzed by lag sequential analysis, revealed that the feeding sequence is non-random and that feeding episodes involving small prey are less complex than those involving large prey. Direct observation revealed that the behavioral repertoire of Echidna nebulosa and Enchelycore pardalis includes rotation and knotting, while that of Gymnomuraena zebra includes rotation but not knotting. Knotting is utilized when feeding on "large" prey or when resistance is met when pulling on prey.
Article
Discusses surplus hunting as a strategy to utilise unpredictable or indefensible resources. Even with the assumption that surplus hunting is an activity with substantial immediate and future costs, a model predicts that a tendency to participate in surplus hunting under periods of high prey density is evolutionarily plausible for the smallest members of predator guilds (and for generalists) in cool or dry environments.-P.J.Jarvis
Article
Field data on the diet of stoats in relation to different prey density were used to examine food preference and selective feeding and to test predictions from optimal foraging theory. The relationship between diet and reproductive output was also examined in three food environments. Stoats concentrated on voles (their basic food) when vole density was high or moderately high. Male stoats showed a high preference for the larger water voles. Selective hunting for them increased with their relative abundance but the males specialized less on water voles at overall high density of rodents. This was probably due to high relative density of the prey second in preference (field vole). The data are in agreement with the theory predicting relative density of prey to be important in determining optimal diet. Females did not show any clear preference for water vole relative to field vole and no long term change occurred in selective hunting relative to changes in vole density. The difference between males and females was ascribed to different fitness set functions, implying a combination of large and small voles to be the optimal diet for females and large prey as water vole as optimal diet for males. No consistent difference in reproductive success was found in the different food environments, but the highest reproductive output occurred in areas with relatively high water vole density. /// Данные полевых исследований состава пищи у горностая в зависимости от различий плотности жертв использовали для анализа пищевого преферендума и пищевий избирательности, а таюже для проверки оптимальной фуражирочной теории. Изучали таюже зависимость между составом пищи и эффективностью размножения в трех местообитаниях с разным составом пищи. Горностаи в основном питались полевками (их основная пища), если плотность полевок была высокой или умеренно высокой. Самцы предпочитали крупных водных полевок. Селективность охоты за ними повышалась при увеличении их относительной плотности, но самцы меньше специализировались на водных полевках при общей высокой численности грызунов. Это оченидно определялось высокой относительной плотностью жертв, занимающих второе место в рядах предпочитаемости (пашенные полевки). Результаты согласуются с теорией, предсказывающей, что относительная плотность жертв имеет важное значение при определении оптимальной диеты. У самок нет четкого предпочтения водных полевок в сравнении с пашенными и не отмечены долговременные изменения в избирательности охоты в зависимости от плотности полевок. Различия между самцами и самками были описаны разными уравнениями функциональных зависимостей, в которых комбинируются крупные и мелкие полевки для оптимальной диеты самок и отмечены крупные жертвы в виде водных полевок как оптимальная пища самцов. Не было отмечено существенных различий в плодовитости в разных местообитаниях, но наибольшая скорость размножения установлена в участках с относительно высокой плотностью водных полевок.
Article
Maximum body curvature during the initial phase of escape swimming (stage 1 of C-start) was measured in four species of tropical marine fishes. A linear correlation between maximum curvature and number of functional intervertebral joints was found (range for number of joints, 17-25). A biomechanical model of vertebral column bending predicts that, if intervertebral joint angles are held constant, increasing the number of joints should produce a linear decrease in the measured curvature coefficient (curvature coefficient is inversely related to curvature). The measured curvature coefficients fit this model closely, indicating that, within the range of 17-25 joints, vertebral number is an important determinant of vertebral column flexibility. The study species with the lowest vertebral number, a filefish, Monacanthus hispidus, is a member of the Tetraodontiformes, a group characterized by the lowest vertebral numbers found among fishes. Elaborate antipredator defenses, such as a carapace and the ability to inflate the body, have evolved six times within the Tetraodontiformes, and some form of mechanical defense is present in all families of this group. We propose an evolutionary scenario in which low vertebral number reduced the escape swimming performance of ancestral tetraodontiforms, thus increasing their vulnerability to predators and driving the repeated evolution of mechanical defenses in this group. Our finding that lower vertebral numbers are correlated with lower C-start curvature suggests that low vertebral number may impair escape performance; thus, one necessary condition for the proposed scenario is met.
Article
A hypothesis is proposed to explain extreme sexual dimorphism in small mustelids. It is suggested that the dimorphism could be a result of selective pressure on the body diameter of weasels: the maximum diameter should not exceed the diameter of burrows of their basic prey. Pregnancy, which changes substantially female body diameter, causes females (when non-pregnant) to be thinner than males, and in consequence shorter and much smaller.
Article
Squamates classified as "subarenaceous" possess the ability to move long distances within dry sand; body elongation among sand and soil burrowers has been hypothesized to enhance subsurface performance. Using x-ray imaging, we performed the first kinematic investigation of the subsurface locomotion of the long, slender shovel-nosed snake (Chionactis occipitalis) and compared its biomechanics to those of the shorter, limbed sandfish lizard (Scincus scincus). The sandfish was previously shown to maximize swimming speed and minimize mechanical cost of transport during burial. Our measurements revealed that the snake also swims through sand by propagating traveling waves down the body, head to tail. Unlike the sandfish, the snake nearly followed its own tracks, thus swimming in an approximate tube of self-fluidized granular media. We measured deviations from tube movement by introducing a parameter, the local slip angle, βs, which measures the angle between direction of movement of each segment and body orientation. The average slip angle (β(-) s) was smaller for the snake than the sandfish; granular resistive force theory (RFT) revealed that the curvature utilized by each animal optimized its performance. The snake benefits from its slender body shape (and increased vertebral number) which allows propagation of a higher number of optimal curvature body undulations. The snake's low skin friction also increases performance. The agreement between experiment and RFT combined with the relatively simple properties of the granular "frictional fluid" make subarenaceous swimming an attractive system to study functional morphology and bauplan evolution.
Article
Time-calibrated species phylogenies are critical for addressing a wide range of questions in evolutionary biology, such as those that elucidate historical biogeography or uncover patterns of coevolution and diversification. Because molecular sequence data are not informative on absolute time, external data-most commonly, fossil age estimates-are required to calibrate estimates of species divergence dates. For Bayesian divergence time methods, the common practice for calibration using fossil information involves placing arbitrarily chosen parametric distributions on internal nodes, often disregarding most of the information in the fossil record. We introduce the "fossilized birth-death" (FBD) process-a model for calibrating divergence time estimates in a Bayesian framework, explicitly acknowledging that extant species and fossils are part of the same macroevolutionary process. Under this model, absolute node age estimates are calibrated by a single diversification model and arbitrary calibration densities are not necessary. Moreover, the FBD model allows for inclusion of all available fossils. We performed analyses of simulated data and show that node age estimation under the FBD model results in robust and accurate estimates of species divergence times with realistic measures of statistical uncertainty, overcoming major limitations of standard divergence time estimation methods. We used this model to estimate the speciation times for a dataset composed of all living bears, indicating that the genus Ursus diversified in the Late Miocene to Middle Pliocene.
Article
1. Here, I present a new, multifunctional phylogenetics package, phytools, for the R statistical computing environment. 2. The focus of the package is on methods for phylogenetic comparative biology; however, it also includes tools for tree inference, phylogeny input/output, plotting, manipulation and several other tasks. 3. I describe and tabulate the major methods implemented in phytools, and in addition provide some demonstration of its use in the form of two illustrative examples. 4. Finally, I conclude by briefly describing an active web-log that I use to document present and future developments for phytools. I also note other web resources for phylogenetics in the R computational environment.
Article
Serially homologous systems with high internal differentiation frequently exhibit meristic constraints, although the developmental basis for constraint is unknown. Constraints in the counts of the cervical and lumbosacral vertebral series are unique to mammals, and appeared in the Triassic, early in their history. Concurrent adaptive modifications of the mammalian respiratory and locomotor systems involved a novel source of cells for muscularization of the diaphragm from cervical somites, and the loss of ribs from lumbar vertebrae. Each of these innovations increased the modularity of the somitic mesoderm, and altered somitic and lateral plate mesodermal interactions across the lateral somitic frontier. These developmental innovations are hypothesized here to constrain the anteroposterior transposition of the limbs along the column, and thus also cervical and thoracolumbar count. Meristic constraints are therefore regarded here as the nonadaptive, secondary consequences of adaptive respiratory and locomotor traits.
Article
Size-related shape changes in animals are studied within a general framework of size variables and shape vectors. Isometry, or independence of shape and size, is defined as the independence of some (all) shape vector(s) from a particular size variable. With mild restrictions it is shown that isometry is possible with respect to at most one size variable, or in other words that shape will always be related to a variety of size variables. The choice of a size variable is a hitherto neglected, but important, part of an allometric study.The use of functional relationships in allometry is contrasted with the approach developed here. Also, size and shape variables are used in characterizations of the lognormal, gamma and generalized gamma distributions. The results, given in a biological context, are of interest in size and shape studies generally.
Article
The least weasel (Mustela nivalis) is a remarkably well adapted predator of mice and other small animals. Each kill is rather stereotyped, in that the weasel grabs the prey by the napeof the neck and bites through the base of the skull and/or throat, using its lithe body to "wrap up" and hold the prey. The least weasel will kill mice successively until it is too exhausted physically to kill more. Mice are always eaten from the head posteriorly until completely consumed. The least weasel (Mustelamnivalis L.), the smallest living carnivore, is an extremely well adapted and efficient predator. Its chief food item is mouse-sizemammals; small invertebrates andbirds also are eaten (Allen, 1940; Day, 1966,1968;Hurrell, 1966). The weaselis long and slender (140-210 mm); males weighbetween60 and 90 g and females between40 and 70 g. The short legs, tail, and ears allow it to travel freely along surfacerunways and burrows constructed by small mice. It is veryagile and quick, with great variation in body movements and positions. The observationsand conclusions contained herein are the result of numerous observations of killing and feeding by members of a colony of least weasels maintained in the MichiganState University Live Animal Colony between 1966 and 1970(see Heidt, 1970, for details of the colony). Llewellyn (1942)described killingand feeding;however, his observations werelimited to onlyone weasel over a period of several days. Severaladditions and differences were found by the writer. Short (1961), Allen (1940), East and Lockie (1964), and Polderboer et al. (1941) described various aspects concerning the amounts of food consumedby least weasels. The killingbehaviorof the weaselis rather stereotyped.The weaselgenerallyseizes the prey at the nape of the neck and bites through the base of the skull and/or throat area. The weaselmay first grasp a prey item almost any place on the prey's body in order to gain leverage for the neck bite, using its feet to manipulate the prey and commonlywrappingits long, slender body around the victim for more leverage.Llewellyn (1942)never observed his weasel to release its grip until the mouse was dead. However, in our colonythe weaselscommonly woulddrop a mouse after immobilizing it. At times they would )laywith the mouse much as a house cat might. If a second mouse was placed in the cage the weasel usually would mmobilize the first and then catch and kill the second, returningto kill the first if it had not already died. The entire tillingprocedure is generally veryrapid, ranging from 10to 60 sec. The attack stimulus seems to be movement by the mouse, a:- weaselshave been observed to pass within inches of a completely still mouse withoutseeming to see it. The weaselis a voraciouskiller in that it willkill one mouse after another until tooexhausted physicallyto kill more. At one time whenseven mice were placed in a cage with one weasel, the weasel immediatelyand systematically killed all seven and began a search pattern of the cage for more mice.
Article
Multiple lines of tetrapods show reduced limbs or their loss. Such patterns are in diverse lines associated with multiple other characteristics. Only bodily elongation represents a common denominator. Analysis suggests that elongation for traverse of crevices in a sheltering environment and for the utilization of undulatory locomotion may have provided the initial selective advantage to the system. Limb reduction would then have been secondary. This hypothesis leads to several interesting implications about the process of diversification in tetrapods.
Article
Metabolism of cold stressed weasels is 50-100 per cent greater than that of normally shaped mammals of the same weight. This can be attributed to their greater surface area, shorter fur, and inability to attain a spherical resting posture. In evolving an elongate shape which enables them to enter confined spaces in search of prey, weasels have sacrificed energetic efficiency. Increased ability to obtain prey, made possible by elongate shape and sexual dimorphism in body size, apparently more than compensates for the energetic cost of being long and thin. The information on weasels indicates that body surface area is an important determinant of heat loss in small homeotherms and suggests that energetic efficiency has played a significant role in the evolution of body shape and size.