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Evolutionary and morphological patterns underlying carnivoran body shape diversity
Abstract
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.
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... Given the universal potential for natural selection to act upon body shape, it is not surprising that many studies have sought to investigate associations between body proportions and ecological niche occupation [8][9][10][11][12][13][14] . While these studies have regularly identified important trends in the evolution of body proportions 8-14 , they have tended to focus on individual taxonomic or ecological groups, or on an individual aspect of body shape. ...
... Body shape also plays a determinant role at multiple physiological levels; for example, in describing the space available for accommodating major organ systems 4,5 , and body surface area for heat exchange 6,7 . Because different environments and behaviours place different demands on the functional mechanics and physiologies of organisms, it is expected that body proportions should vary across animals occupying different ecological niches [8][9][10][11][12][13][14] . However, modification of body size and shape by ecological pressures may also be constrained by other factors, notably phylogenetic history and the ecological trajectory of evolutionary change 3,15,16 . ...
... Given the universal potential for natural selection to act upon body shape, it is not surprising that many studies have sought to investigate associations between body proportions and ecological niche occupation [8][9][10][11][12][13][14] . While these studies have regularly identified important trends in the evolution of body proportions [8][9][10][11][12][13][14] , they have tended to focus on individual taxonomic or ecological groups, or on an individual aspect of body shape. ...
Body size and shape play fundamental roles in organismal function and it is expected that animals may possess body proportions that are well-suited to their ecological niche. Tetrapods exhibit a diverse array of body shapes, but to date this diversity in body proportions and its relationship to ecology have not been systematically quantified. Using whole-body skeletal models of 410 extinct and extant tetrapods, we show that allometric relationships vary across individual body segments thereby yielding changes in overall body shape as size increases. However, we also find statistical support for quadratic relationships indicative of differential scaling in small-medium versus large animals. Comparisons of locomotor and dietary groups highlight key differences in body proportions that may mechanistically underlie occupation of major ecological niches. Our results emphasise the pivotal role of body proportions in the broad-scale ecological diversity of tetrapods.
... Although these pathways have been found in fishes, amphibians, and squamate reptiles (Parra-Olea and Wake 2001;Mehta et al. 2010;Morinaga and Bergmann 2017;Bergmann and Morinaga 2019), investigations of convergence towards similar elongate body plans in mammals are rare. Law (2021a) found that evolutionary pathways to body shape variation in carnivoran mammals are clade specific, but whether body elongation and its underlying morphological components exhibit patterns of convergence remain to be tested. ...
... Because multiple morphological pathways contribute to carnivoran body shape variation (Law 2021a), I also tested the same predictions on whether elongate carnivorans exhibit similar morphological components including elongation/shortening of the head, elongation/shortening of the vertebral regions, and reduction/increase of body depth. Examining the degree of convergence in these components will clarify whether convergence in body elongation evolved through similar pathways. ...
... I obtained data on body shape and its underlying morphological components from 176 terrestrial carnivorans (∼71% of diversity) from Law (2021a). The components consist of head elongation ratio (head ER), the axial elongation index (AEI V ) of each vertebral region (i.e., cervical, thoracic, lumbar, and sacral), and size-corrected rib length as a proxy for relative body depth (see Appendix 1 of the Supplementary material available on Dryad at https://doi.org/10.5061/dryad.bg79cnpc4. ...
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.
... In addition, carnivorans range in body sizes and shapes from large robust bears to small elongate weasels. Although recent work revealed that smaller carnivorans exhibited more elongate bodies, body size explained only 42% of body shape variation (Law 2021a). This suggests additional independent factors may influence body size and body shape separately across carnivoran evolution. ...
... This suggests additional independent factors may influence body size and body shape separately across carnivoran evolution. Furthermore, multiple morphological components contribute to carnivoran body shape variation (Law 2021a); therefore, I also test whether locomotor, hunting, and dietary ecologies influenced the evolution of these underlying morphological components. Because of the different mechanical demands of moving through diverse environments (Kardong 2014), I predict that locomotion and hunting behavior will have the greatest influence on the evolution of carnivoran body size and shape as well as on the thoracolumbar region underlying body shape variation. ...
... Relative support for each of the six models was assessed through computation of small sample corrected Akaike weights (AICcW) as described above. Because body shape is driven by strong allometric effects of body size (Law 2021a), I also performed OUwie and bayou analyses on size-corrected hbER. I sizecorrected hbER by obtaining residuals from a PGLS regression of ln hbER against ln body size (geometric mean) using the R function phyl.resid ...
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.
Divergence in body shape is one of the most widespread and repeated patterns of morphological variation in fishes and is associated with habitat specification and swimming mechanics. Such ecological diversification is the first stage of the explosive adaptive radiation of cichlid fishes in the East African Rift Lakes. We use two hybrid crosses of cichlids (Metriaclima sp. × Aulonocara sp. and Labidochromis sp. × Labeotropheus sp., >975 animals total) to determine the genetic basis of body shape diversification that is similar to benthic-pelagic divergence across fishes. Using a series of both linear and geometric shape measurements, we identified 34 quantitative trait loci (QTL) that underlie various aspects of body shape variation. These QTL are spread throughout the genome, each explaining 3.2-8.6% of phenotypic variation, and are largely modular. Further, QTL are distinct both between these two crosses of Lake Malawi cichlids and compared to previously identified QTL for body shape in fishes such as sticklebacks. We find that body shape is controlled by many genes of small effect. In all, we find that convergent body shape phenotypes commonly observed across fish clades are most likely due to distinct genetic and molecular mechanisms.
Body size is often hypothesized to facilitate or constrain morphological diversity in the cranial, appendicular, and axial skeletons. However, how overall body shape scales with body size ( i.e. , body shape allometry) and whether these scaling patterns differ between ecological groups remains poorly investigated. Here, we test whether and how the relationships between body shape, body size, and limb lengths differ among species with different locomotor specializations, and describe the underlying morphological components that contribute to body shape evolution among squirrel (Sciuridae) ecotypes. We quantified the body size and shape of 87 squirrel species from osteological specimens held at museum collections. Using phylogenetic comparative methods, we first found that body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes: chipmunks and gliding squirrels exhibited more elongate bodies with increasing body sizes whereas ground squirrels exhibited more robust bodies with increasing body size. Second, we found that only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs. Third, we found that the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape evolution across squirrels. Overall, our work contributes to the growing understanding of mammalian body shape evolution and how it is influenced by body size and locomotor ecology, in this case from robust subterranean to gracile gliding squirrels.
Body size influences nearly every aspect of an organism’s biology and ecology. When studying body size, researchers often focus on a single dimension, such as length, despite the fact that size can evolve by altering multiple body dimensions. The distinct ways organisms change their size can have profound consequences on evolutionary and ecological processes. Here, we investigate the evolution of size as a complex trait by exploring the interaction between body length, depth, and width across 42 orders of teleost fishes. Using Ornstein-Uhlenbeck models, we compare shifts in the adaptive landscapes of each of the three size components, and in the scaling relationships between them. We find that fishes change their size in a myriad of ways: changes in length, depth and width rarely co-occur on the phylogeny or in accordance with composite measures of size (body mass or the geometric mean). Body size diversity tends to accumulate along trajectories close to isometry but there is also some variation in the allometric regimes. Finally, orders with scaling shifts are more species rich than those without shifts, suggesting that body size diversity trajectories have the potential to be associated with distinct diversification scenarios in teleosts. Based on the evolutionary relationships we found between size components, we recommend that researchers treat body size as a complex trait to properly evaluate the patterns and processes of size variation in nature.
Divergence along the benthic-pelagic axis is one of the most widespread and repeated patterns of morphological variation in fishes, producing body shape diversity associated with ecology and swimming mechanics. This ecological shift is also the first stage of the explosive adaptive radiation of cichlid fishes in the East African Rift Lakes. We use two hybrid crosses of cichlids (Metriaclima sp. x Aulonocara sp. and Labidochromis sp. x Labeotropheus sp., >975 animals total) along the benthic-pelagic ecomorphological axis to determine the genetic basis of body shape diversification. Using a series of both linear and geometric shape measurements, we identify 55 quantitative trait loci (QTL) that underlie various aspects of body shape variation associated with benthic-pelagic divergence. These QTL are spread throughout the genome, each explain 3.0-7.2% of phenotypic variation, and are largely modular. Further, QTL are distinct both between these two crosses of Lake Malawi cichlids and compared to previously identified QTL for body shape in fishes such as sticklebacks. We find that body shape is controlled by many genes of small effects. In all, we find that convergent benthic and pelagic body phenotypes commonly observed across fish clades are most likely due to distinct genetic and molecular mechanisms.
Carnivorans represent extreme ecomorphological diversity, encompassing remarkable variation in form, habitat, and diet. The relationship between the masticatory musculature and dietary ecology has been explored in a number of carnivoran lineages, including felids and the superfamily Musteloidea. In this study, we present novel architectural data on two additional carnivoran families – Ursidae and Canidae – and supplement these previous studies with additional felid, musteloid, herpestid, hyaenid, and viverrid taxa (a total of 53 species across 10 families). Gross dissection data were collected following a standardized protocol ‐ sharp dissection followed by chemical digestion. Summed jaw adductor forces were also transformed into bite force estimates (BF) using osteologically‐calculated leverages. All data were linearized, log‐transformed, and size‐adjusted using two proxies for each taxon – body mass and cranial geometric mean – to assess relative scaling trends. These architectural data were then analyzed in the context of dietary ecology to examine the impact of dietary size and dietary mechanical properties. Muscle mass, physiological cross‐sectional area and BF scaled with isometry or positive allometry in all cases, whereas fascicle lengths scaled with isometry or negative allometry. With respect to diet, body mass adjusted fascicle lengths were strongly correlated with dietary size in musteloids, but not in any other lineage. The relationship between size‐adjusted BF and dietary mechanical properties was also significant within musteloids, and across the sample as a whole, but not within other individual lineages. This interfamilial trend may reflect the increased morphological and dietary diversity of musteloids relative to other carnivoran groups. This article is protected by copyright. All rights reserved.
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.
Big, time-scaled phylogenies are fundamental to connecting evolutionary processes to modern biodiversity patterns. Yet inferring reliable phylogenetic trees for thousands of species involves numerous trade-offs that have limited their utility to comparative biologists. To establish a robust evolutionary timescale for all approximately 6,000 living species of mammals, we developed credible sets of trees that capture root-to-tip uncertainty in topology and divergence times. Our “backbone-and-patch” approach to tree building applies a newly assembled 31-gene supermatrix to two levels of Bayesian inference: (1) backbone relationships and ages among major lineages, using fossil node or tip dating, and (2) species-level “patch” phylogenies with nonoverlapping in-groups that each correspond to one representative lineage in the backbone. Species unsampled for DNA are either excluded (“DNA-only” trees) or imputed within taxonomic constraints using branch lengths drawn from local birth–death models (“completed” trees). Joining time-scaled patches to backbones results in species-level trees of extant Mammalia with all branches estimated under the same modeling framework, thereby facilitating rate comparisons among lineages as disparate as marsupials and placentals. We compare our phylogenetic trees to previous estimates of mammal-wide phylogeny and divergence times, finding that (1) node ages are broadly concordant among studies, and (2) recent (tip-level) rates of speciation are estimated more accurately in our study than in previous “supertree” approaches, in which unresolved nodes led to branch-length artifacts. Credible sets of mammalian phylogenetic history are now available for download at http://vertlife.org/phylosubsets, enabling investigations of long-standing questions in comparative biology.
A fundamental concept in evolutionary biology is that life tends to become more complex through geologic time, but empirical examples of this phenomenon are controversial. One debate is whether increasing complexity is the result of random variations, or if there are evolutionary processes which actively drive its acquisition, and if these processes act uniformly across clades. The mammalian vertebral column provides an opportunity to test these hypotheses because it is composed of serially-repeating vertebrae for which complexity can be readily measured. Here we test seven competing hypotheses for the evolution of vertebral complexity by incorporating fossil data from the mammal stem lineage into evolutionary models. Based on these data, we reject Brownian motion (a random walk) and uniform increasing trends in favor of stepwise shifts for explaining increasing complexity. We hypothesize that increased aerobic capacity in non-mammalian cynodonts may have provided impetus for increasing vertebral complexity in mammals.
Rapid adaptive radiation poses two distinct questions apart from speciation and adaptation: What happens after one speciation event and how do some lineages continue speciating through a rapid burst? We review major features of rapid radiations and their mismatch with theoretical models and speciation mechanisms. The paradox is that the hallmark rapid burst pattern of adaptive radiation is contradicted by most speciation models, which predict continuously decelerating diversification and niche subdivision. Furthermore, it is unclear if and how speciation-promoting mechanisms such as magic traits, phenotype matching, and physical linkage of coadapted alleles promote rapid bursts of speciation. We review additional mechanisms beyond ecological opportunity to explain rapid radiations: ( a) ancient adaptive alleles and the transporter hypothesis, ( b) sexual signal complexity, ( c) fitness landscape connectivity, ( d) diversity begets diversity, and ( e) plasticity first. We propose new questions and predictions connecting microevolutionary processes to macroevolutionary patterns through the study of rapid radiations.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 50 is November 4, 2019. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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.
Restricted variation in numbers of presacral vertebrae in mammals is a classic example of evolutionary stasis. Cervical number is nearly invariable in most mammals, and numbers of thoracolumbar vertebrae are also highly conserved. A recent hypothesis posits that stasis in mammalian presacral count is due to stabilizing selection against the production of incomplete homeotic transformations at the lumbo-sacral border in fast-running mammals, while slower, ambulatory mammals more readily tolerate intermediate lumbar/sacral vertebrae. We test hypotheses of variation in presacral numbers of vertebrae based on running speed, positional behaviour and vertebral contribution to locomotion. We find support for the hypothesis that selection against changes in presacral vertebral number led to stasis in mammals that rely on dorsomobility of the spine during running and leaping, but our results are independent of running speed per se. Instead, we find that mammals adapted to dorsostability of the spine, such as those that engage in suspensory behaviour, demonstrate elevated variation in numbers of presacral vertebrae compared to dorsomobile mammals. We suggest that the evolution of dorsostability and reduced reliance on flexion and extension of the spine allowed for increased variation in numbers of presacral vertebrae, leading to departures from an otherwise stable evolutionary pattern.
Sleep is an essential human function but its regulation is poorly understood. Using accelerometer data from 85,670 UK Biobank participants, we perform a genome-wide association study of 8 derived sleep traits representing sleep quality, quantity and timing, and validate our findings in 5,819 individuals. We identify 47 genetic associations at P < 5 × 10⁻⁸, of which 20 reach a stricter threshold of P < 8 × 10⁻¹⁰. These include 26 novel associations with measures of sleep quality and 10 with nocturnal sleep duration. The majority of identified variants associate with a single sleep trait, except for variants previously associated with restless legs syndrome. For sleep duration we identify a missense variant (p.Tyr727Cys) in PDE11A as the likely causal variant. As a group, sleep quality loci are enriched for serotonin processing genes. Although accelerometer-derived measures of sleep are imperfect and may be affected by restless legs syndrome, these findings provide new biological insights into sleep compared to previous efforts based on self-report sleep measures.
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.
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Background
The axial skeleton consists of repeating units (vertebrae) that are integrated through their development and evolution. Unlike most tetrapods, vertebrae in the mammalian trunk are subdivided into distinct thoracic and lumbar modules, resulting in a system that is constrained in terms of count but highly variable in morphology. This study asks how thoracolumbar regionalization has impacted adaptation and evolvability across mammals. Using geometric morphometrics, we examine evolutionary patterns in five vertebral positions from diverse mammal species encompassing a broad range of locomotor ecologies. We quantitatively compare the effects of phylogenetic and allometric constraints, and ecological adaptation between regions, and examine their impact on evolvability (disparity and evolutionary rate) of serially-homologous vertebrae.
Results
Although phylogenetic signal and allometry are evident throughout the trunk, the effect of locomotor ecology is partitioned between vertebral positions. Lumbar vertebral shape correlates most strongly with ecology, differentiating taxa based on their use of asymmetric gaits. Similarly, disparity and evolutionary rates are also elevated posteriorly, indicating a link between the lumbar region, locomotor adaptation, and evolvability.
Conclusion
Vertebral regionalization in mammals has facilitated rapid evolution of the posterior trunk in response to selection for locomotion and static body support.
Electronic supplementary material
The online version of this article (10.1186/s12862-018-1282-2) contains supplementary material, which is available to authorized users.
Size and shape are often considered important variables that lead to variation in performance. In studies of feeding, size‐corrected metrics of the skull are often used as proxies of biting performance; however, few studies have examined the relationship between cranial shape in it's entirety and estimated bite force across species and how dietary ecologies may affect these variables differently. Here, we used geometric morphometric and phylogenetic comparative approaches to examine relationships between cranial morphology and estimated bite force in the carnivoran clade Musteloidea. We found a strong relationship between cranial size and estimated bite force but did not find a significant relationship between cranial shape and size‐corrected estimated bite force. Many‐to‐one mapping of form to function may explain this pattern because a variety of evolutionary shape changes rather than a single shape change may have contributed to an increase in relative biting ability. We also found that dietary ecologies influenced cranial shape evolution but did not influence cranial size nor size‐corrected bite force evolution. While musteloids with different diets exhibit variation in cranial shapes, they have similar estimated bite forces suggesting that other feeding performance metrics and potentially non‐feeding traits are also important contributors to cranial evolution. We postulate that axial and appendicular adaptations and the interesting feeding behaviors reported for species within this group also facilitate different dietary ecologies between species. Future work integrating cranial, axial, and appendicular form and function with behavioral observations will reveal further insights in the evolution of dietary ecologies and other ecological variables.
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Early shifts lead to big changes
Mammals represent one of the most morphologically diverse taxonomic groups. One of the unique features underlying this diversity is variability of the spine, which facilitates everything from flexibility for speedy running and support for upright walking. Jones et al. studied a group ancestral to modern mammals—nonmammalian synapsids, or mammal-like reptiles. As forelimb function diversified, the spine developed distinct regions. These regions then differentiated further, leading to the highly varied mammalian forms we see today.
Science , this issue p. 1249
The musteloids are the most speciose of the carnivorans and have a global distribution. They display a wide diversity of morphological and physiological form and function, which have been shaped by their adaptation to a wide variety of ecological niches, ranging from the Arctic to the tropics and deserts to the seas. This chapter explores how several morphological and physiological adaptations are key to their successful diversification, including an elongated body, a highly insulating pelage, powerful teeth and jaws, anal sacs for olfactory communication or chemical defence, and reproductive physiologies that allow females to optimise their reproductive output. While many of these adaptations are shared by other carnivorans, it is their combination in musteloids that has allowed them to diversify so successfully globally.
Residual randomization in permutation procedures (RRPP) is an appropriate means of generating empirical sampling distributions for ANOVA statistics and linear model coefficients, using ordinary or generalized least‐squares estimation. This is an especially useful approach for high‐dimensional (multivariate) data.
Here, we present an r package that provides a comprehensive suite of tools for applying RRPP to linear models. Important available features include choices for OLS or GLS coefficient estimation, data or dissimilarity matrix analysis capability, choice among types I, II, or III sums of squares and cross‐products, various effect size estimation methods, and an ability to perform mixed‐model ANOVA.
The lm.rrpp function is similar to the lm function in many regards, but provides coefficient and ANOVA statistics estimates over many random permutations. The S3 generic functions commonly used with lm also work with lm.rrpp . Additionally, a pairwise function provides statistical tests for comparisons of least‐squares means or slopes, among designated groups. Users have many options for varying random permutations. Compared to similar available packages and functions, RRPP is extremely fast and yields comprehensive results for downstream analyses and graphics, following model fits with lm.rrpp .
The RRPP package facilitates analysis of both univariate and multivariate response data, even when the number of variables exceeds the number of observations.
Phylogenetic regression is frequently utilized in macroevolutionary studies, and its statistical properties have been thoroughly investigated. By contrast, phylogenetic ANOVA has received relatively less attention, and the conditions leading to incorrect statistical and biological inferences when comparing multivariate phenotypes among groups remains under‐explored. Here we propose a refined method of randomizing residuals in a permutation procedure (RRPP) for evaluating phenotypic differences among groups while conditioning the data on the phylogeny. We show that RRPP displays appropriate statistical properties for both phylogenetic ANOVA and regression models, and for univariate and multivariate datasets. For ANOVA, we find that RRPP exhibits higher statistical power than methods utilizing phylogenetic simulation. Additionally, we investigate how group dispersion across the phylogeny affects inferences, and reveal that highly aggregated groups generate strong and significant correlations with the phylogeny, which reduce statistical power and subsequently affect biological interpretations. We discuss the broader implications of this phylogenetic group aggregation, and its relation to challenges encountered with other comparative methods where one or a few transitions in discrete traits are observed on the phylogeny. Finally, we recommend that phylogenetic comparative studies of continuous trait data utilize RRPP for assessing the significance of indicator variables as sources of trait variation.
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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.
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
Recent advances in geometric morphometrics provide improved techniques for extraction of biological information from shape and have greatly contributed to the study of ecomorphology and morphological evolution. However, the vertebral column remains an under-studied structure due in part to a concentration on skull and limb research, but most importantly because of the difficulties in analysing the shape of a structure composed of multiple articulating discrete units (i.e. vertebrae). Here, we have applied a variety of geometric morphometric analyses to three-dimensional landmarks collected on 19 presacral vertebrae to investigate the influence of potential ecological and functional drivers, such as size, locomotion and prey size specialisation, on regional morphology of the vertebral column in the mammalian family Felidae. In particular, we have here provided a novel application of a method—phenotypic trajectory analysis (PTA)—that allows for shape analysis of a contiguous sequence of vertebrae as functionally linked osteological structures. Our results showed that ecological factors influence the shape of the vertebral column heterogeneously and that distinct vertebral sections may be under different selection pressures. While anterior presacral vertebrae may either have evolved under stronger phylogenetic constraints or are ecologically conservative, posterior presacral vertebrae, specifically in the post-T10 region, show significant differentiation among ecomorphs. Additionally, our PTA results demonstrated that functional vertebral regions differ among felid ecomorphs mainly in the relative covariation of vertebral shape variables (i.e. direction of trajectories, rather than in trajectory size) and, therefore, that ecological divergence among felid species is reflected by morphological changes in vertebral column shape.
Evolutionary morphologists frequently wish to understand the extent to which organisms are integrated, and whether the strength of morphological integration among subsets of phenotypic variables differ among taxa or other groups. However, comparisons of the strength of integration across datasets are difficult, in part because the summary measures that characterize these patterns (RV and rPLS) are dependent both on sample size and on the number of variables. As a solution to this issue we propose a standardized test statistic (a z-score) for measuring the degree of morphological integration between sets of variables. The approach is based on a partial least squares analysis of trait covariation, and its permutation-based sampling distribution. Under the null hypothesis of a random association of variables, the method displays a constant expected value and confidence intervals for datasets of differing sample sizes and variable number, thereby providing a consistent measure of integration suitable for comparisons across datasets. A two-sample test is also proposed to statistically determine whether levels of integration differ between datasets, and an empirical example examining cranial shape integration in Mediterranean wall lizards illustrates its use. Some extensions of the procedure are also discussed. This article is protected by copyright. All rights reserved
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 propulsion was associated with a shift from surface to submerged swimming providing a reduction in transport costs. The evolution of aquatic mammals from terrestrial ancestors required increased swimming performance with minimal compromise to terrestrial movement. Examination of modern analogs to transitional swimming stages suggests that only slight modification to the neuromotor pattern used for terrestrial locomotion is required to allow for a change to lift-based propulsion.
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.
Significance
Our study explains one of the riddles of mammal evolution: the strong conservation of the number of trunk vertebrae. The vertebral column and its high evolvability are considered to be of central importance for the evolution of vertebrates, which is why the constancy is both puzzling and important. We hypothesize, on biomechanical and developmental grounds, that evolutionary change is virtually impossible in fast running and agile mammals. The rationale is that several mutations are necessary to change trunk vertebral counts, with single mutations usually leading to irregular lumbosacral joints that severely hamper running and jumping capability. Our observations indeed show that selection against these initial changes is strong in fast and agile mammals and weak in slower and sturdier ones.
Phylogenetic comparative methods are essential for addressing evolutionary hypotheses with interspecific data. The scale and scope of such data has increased dramatically in the last few years. Many existing approaches are either computationally infeasible or inappropriate for data of this size. To address both of these problems, we present geiger v2.0, a complete overhaul of the popular R package geiger (Harmon et al., 2008). We have re-implemented existing methods with more efficient algorithms and have developed several new approaches for accomodating heterogeneous models and data types.
This R package is available on the CRAN repository http://cran.r-project.org/web/packages/geiger/. All source code is also available on github http://github.com/mwpennell/geiger-v2. geiger v2.0 depends on the ape package (Paradis et al., 2004).
mwpennell@gmail.com.
Species are generally regarded as a fundamental unit of biodiversity. By contrast, higher taxa such as genera and families, while widely used as biodiversity metrics and for classification and communication, are generally not believed to be shaped by shared evolutionary processes in the same way as species. We use simulations to show that processes which are important for emergence of evolutionarily significant units (ESUs) at the species level, namely geographical isolation and ecological divergence, can generate evolutionary independence above the species level and thereby lead to emergence of discrete phylogenetic clusters (higher ESUs). Extending phylogenetic approaches for delimiting evolutionarily significant species to broader phylogenetic scales, we find evidence for the existence of higher ESUs in mammals. In carnivores, euungulates and lagomorphs the hierarchical level of units detected correspond, on average, to the level of family or genus in traditional taxonomy. The units in euungulates are associated with divergent patterns of body mass, consistent with occupation of distinct ecological zones. Our findings demonstrate a new framework for studying biodiversity that unifies approaches at species and higher levels, thus potentially restoring higher taxa to their historical status as natural entities.
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.
Static, ontogenetic, and evolutionary allometry in all five larval instars of nine species of the water strider genera Gerris and Aquarius were compared using a multivariate approach. Common principal component analysis (CPCA), a generalization extending principal component analysis (PCA) to multigroup situations, was carried out on covariance matrices of log-transformed measurements of eight characters of antennae and legs. For all three types of allometry, a good fit of the model of simple multivariate allometry was found, and PCA results were similar in all instars and species, which justifies the use of CPCA to estimate a common pattern of allometric variation for each of the three types of allometry. We found a fairly close association between static and ontogenetic allometry. which indicates at least in part a developmental origin of individual variation. Evolutionary allometry differed markedly from static and ontogenetic allometry, with leg segments displaying strongly positive allometry. We discuss the possible importance of differences in habitat use for the evolution of the characters considered. Static, ontogenetic, and evolutionary variation are reciprocally interrelated phenomena that need to be considered in studies of the evolution of morphological traits.
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.
Optimisation of energy by aquatic mammals requires adaptations that reduce drag, and improve thrust production and efficiency. Drag is minimised by streamlining the body and appendages. Highly derived aquatic mammals have body shapes close to the optimal hydrodynamic design for drag reduction. There is no conclusive evidence for specialised drag reduction mechanisms, although decreasing hair density is associated with reduced drag. Improvement in thrust production and efficiency is accomplished by changes in propulsive mode and appendage design. Semiaquatic mammals employ drag-based propulsion using paddles, whereas fully aquatic mammals use lift-based propulsion with hydrofoils. Because paddling generates thrust through half the stroke cycle, propulsive efficiency is low and energetic cost is high compared with that for mammals using hydrofoils. Lift-based swimming is a rapid and high-powered propulsive mode. Oscillations of the hydrofoil generate thrust throughout the stroke cycle. For cetaceans and pinnipeds, propulsive efficiency is approximately 80%, and transport cost is below that of semiaquatic mammals. Behavioural adaptations help minimise energy expenditure by swimming mammals. Submerged swimming avoids increased drag from energy lost in formation of surface waves. Porpoising and wave riding, characteristic of dolphins, can reduce the transport costs, allowing for longer-duration swimming at high speeds.
Mammals flex, extend, and rotate their spines as they perform behaviors critical for survival, such as foraging, consuming prey, locomoting, and interacting with conspecifics or predators. The atlas‐axis complex is a mammalian innovation that allows precise head movements during these behaviors. While morphological variation in other vertebral regions has been linked to ecological differences in mammals, less is known about morphological specialization in the cervical vertebrae, which are developmentally constrained in number but highly variable in size and shape. Here, we present the first phylogenetic comparative study of the atlas‐axis complex across mammals. We used spherical harmonics to quantify 3D shape variation of the atlas and axis across a diverse sample of species, and performed phylogenetic analyses to investigate if vertebral shape is associated with body size, locomotion, and diet. We found that differences in atlas and axis shape are partly explained by phylogeny, and that mammalian subclades differ in morphological disparity. Atlas and axis shape diversity is associated with differences in body size and locomotion; large terrestrial mammals have craniocaudally elongated vertebrae, while smaller mammals and aquatic mammals have more compressed vertebrae. These results provide a foundation for investigating functional hypotheses underlying the evolution of neck morphologies across mammals. This article is protected by copyright. All rights reserved
We present a dataset that quantifies body shape in three dimensions across the teleost phylogeny. Built by a team of researchers measuring easy-to-identify, functionally relevant traits on specimens at the Smithsonian National Museum of Natural History it contains data on 16,609 specimens from 6144 species across 394 families. Using phylogenetic comparative methods to analyze the dataset we describe the teleostean body shape morphospace and identify families with extraordinary rates of morphological evolution. Using log shape ratios, our preferred method of body-size correction, revealed that fish width is the primary axis of morphological evolution across teleosts, describing a continuum from narrow-bodied laterally compressed flatfishes to wide-bodied dorsoventrally flattened anglerfishes. Elongation is the secondary axis of morphological variation and occurs within the more narrow-bodied forms. This result highlights the importance of collecting shape on three dimensions when working across teleosts. Our analyses also uncovered the fastest rates of shape evolution within a clade formed by notothenioids and scorpaeniforms, which primarily thrive in cold waters and/or have benthic habits, along with freshwater elephantfishes, which as their name suggests, have a novel head and body shape. This unprecedented dataset of teleostean body shapes will enable the investigation of the factors that regulate shape diversification. Biomechanical principles, which relate body shape to performance and ecology, are one promising avenue for future research.
Understanding the causes of body shape variability across the tree of life is one of the central issues surrounding the origins of biodiversity. One potential mechanism driving observed patterns of shape disparity is a strongly conserved relationship between size and shape. Conserved allometry has been shown to account for as much as 80% of shape variation in some vertebrate groups. Here, we quantify the amount of body shape disparity attributable to changes in body size across nearly 800 species of Indo‐Pacific shore fishes using a phylogenetic framework to analyze 17 geometric landmarks positioned to capture general body shape and functionally‐significant features. In marked contrast to other vertebrate lineages, we find that changes in body size only explain 2.9% of the body shape variation across fishes, ranging from 3–50% within our 11 sampled families. We also find a slight but significant trend of decreasing rates of shape evolution with increasing size. Our results suggest that the influence of size on fish shape has largely been overwhelmed by lineage‐specific patterns of diversification that have produced the modern landscape of highly diverse forms that we currently observe in nature.
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Morphological variation among the true sea snakes (Hydrophiinae), a clade of fully aquatic elapid snakes, includes an extreme 'microcephalic' ecomorph that has a very small head atop a narrow forebody, while the hind body is much thicker (up to 3 times the forebody girth). Previous research has demonstrated that this morphology has evolved at least nine times as a consequence of dietary specialization on burrowing eels, and has also examined morphological changes to the vertebral column underlying this body shape. The question addressed in this study is what happens to the skull during this extreme evolutionary change? Here we use X-ray micro-computed tomography and geometric morphometric methods to characterize cranial shape variation in 30 species of sea snakes. We investigate ontogenetic and evolutionary patterns of cranial shape diversity to understand whether cranial shape is predicted by dietary specialization, and examine whether cranial shape of microcephalic species may be a result of heterochronic processes. We show that the diminutive cranial size of microcephalic species has a convergent shape that is correlated with trophic specialization to burrowing prey. Furthermore, their cranial shape is predictable for their size and very similar to that of juvenile individuals of closely related but non-microcephalic sea snakes. Our findings suggest that heterochronic changes (resulting in paedomorphosis) have driven cranial shape convergence in response to dietary specializations in sea snakes.
Simpson's “early burst” model of adaptive radiation was intended to explain the early proliferation of morphological and functional variation in diversifying clades. Yet, despite much empirical testing, questions remain regarding its frequency across the tree of life. Here, we evaluate the support for an early burst model of adaptive radiation in 14 ecomorphological traits plus body mass for the extant mammalian order Carnivora and its constituent families. We find strong support for early bursts of dental evolution, suggesting a classic Simpsonian adaptive radiation along dietary resource axes. However, the signal of this early burst is not consistently recovered in analyses at the family level, where support for a variety of different models emerges. Furthermore, we find no evidence for early burst–like dynamics in size–related traits, and Bayesian analyses of evolutionary correlations corroborate a decoupling of size and dental evolution, driven in part by dietary specialization. Our results are consistent with the perspective that trait diversification unfolds hierarchically, with early bursts restricted to traits associated with higher level niches, such as macrohabitat use and dietary strategy, and thus with the origins of higher taxa. The lack of support for early burst adaptive radiation in previous phylogenetic studies may be a consequence of focusing on low‐level niche traits (i.e., those associated with microhabitat use) in clades at shallow phylogenetic levels. A richer understanding of early burst adaptive radiation will require a renewed focus on functional traits and their evolution over higher‐level clades.
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Convergence is widely regarded as compelling evidence for adaptation, often being portrayed as evidence that phenotypic outcomes are predictable from ecology, overriding contingencies of history. However, repeated outcomes may be very rare unless adaptive landscapes are simple, structured by strong ecological and functional constraints. One such constraint may be a limitation on body size because performance often scales with size, allowing species to adapt to challenging functions by modifying only size. When size is constrained, species might adapt by changing shape; convergent shapes may therefore be common when size is limiting and functions are challenging. We examine the roles of size and diet as determinants of jaw shape in Sciuridae. As expected, size and diet have significant interdependent effects on jaw shape and ecomorphological convergence is rare, typically involving demanding diets and limiting sizes. More surprising is morphological without ecological convergence, which is equally common between and within dietary classes. Those cases, like rare ecomorphological convergence, may be consequences of evolving on an adaptive landscape shaped by many-to-many relationships between ecology and function, many-to-one relationships between form and performance, and one-to-many relationships between functionally versatile morphologies and ecology. On complex adaptive landscapes, ecological selection can yield different outcomes. This article is protected by copyright. All rights reserved.
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.
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
Barstovian (medial Miocene) mammalian faunas from the Texas Gulf Coastal Plain contained four apparently sympatric species of rhinoceroses: the common forms Aphelops megalodus and Teleoceras medicornutus , a dwarf Teleoceras , and a dwarf Peraceras. Previous work has suggested positive allometry in tooth area with respect to body size in several groups of mammals, i.e., larger mammals have relatively more tooth area. However, dwarfing lineages were shown to have relatively more tooth area for their body size. Our data show no significant allometry in post-canine tooth area of either artiodactyls or ceratomorphs. Similarly, dwarf rhinoceroses and hippopotami show no more tooth area than would be predicted for their size. Limbs are proportionately longer and more robust in larger living ceratomorphs (rhinos and tapirs) than predicted by previous authors. Limb proportions of both dwarf rhinoceroses and dwarf hippopotami are even more robust than in their living relatives.
The high rhinoceros diversity reflects the overall high diversity of Barstovian faunas from the Texas Gulf Coastal Plain. The first appearance of several High Plains mammals in these faunas indicates “ecotone”-like conditions as faunal composition changed. Study of living continental dwarfs shows that there is commonly an ecological separation between browsing forest dwarfs and their larger forebears, which are frequently savannah grazers. This suggests that the dwarf rhinoceroses might have been forest browsers which were sympatric with the larger grazing rhinos of the High Plains during the Barstovian invasion. The continental dwarf model also suggests that insular dwarfism may be explained by the browsing food resources that predominate on islands.
Fifteen variables, selected primarily to reflect functionally significant aspects of cranial morphology, were measured on one skull each of 62 species of modern carnivores, including viverrids, canids, mustelids and felids. To allow comparisons between species of different sizes without the potentially confounding effects of allometric shape changes, the measurements were transformed to dimmensionless variables, based on the residuals from allometric equations. Fourteen out of 15 of the transformed variables distinguish one or more of the four family groups and the rotated first two axes of a principal components analysis distinguish all four families from each other. The following functional hypotheses are proposed: mustelids and felids have the most powerful bites and canids the weakest among the four family groups studied; mustelids and, to a lesser degree, felids have more powerful neck musculature than do canids and viverrids; and visual abilities are best developed among felids and least developed among mustelids. The first two functional hypotheses suggest possible differences in killing behaviour, which are supported by a preliminary survey of the literature on such behaviour. Allometric analysis of the 15 cranial measures shows that the neurocranial components scale with negative allometry, while most of the other measures scale approximately isometrically.
As body size increases, so do the biomechanical challenges of terrestrial locomotion. In the appendicular skeleton, increasing size is met with allometry of limb posture and structure, but much less is known about adaptations of the axial skeleton. It has been hypothesized that stabilization of the lumbar region against sagittal bending may be a response to increasing size in running mammals. However, empirical data on lumbar allometry in running mammals are scarce. This study presents quantitative data on allometry of the penultimate lumbar vertebra in two mammal families: Bovidae and Felidae. One hundred and twenty 3D landmarks were collected on the penultimate lumbar vertebra of 34 bovid (N = 123) and 23 felid (N = 93) species. Multivariate phylogenetically informed regressions were computed, and the shape variation associated with increasing size calculated. The influence of locomotor and habitat variables on size-corrected lumbar shape was tested using phylogenetic multivariate analysis of variance (MANOVAs). Results demonstrate that the scaling patterns in both groups are consistent with the hypothesis of allometric stabilization of the lumbar region, and suggest convergent evolution of allometric responses in distantly related lineages of mammals. However, there was a relatively smaller effect of size in felids than bovids, even when size range disparities were accounted for, suggesting a trade-off between size and running behaviour. Despite the strong influence of size and phylogeny on lumbar shape, there was no correlation with either habitat or diet within families, though certain specialized taxa (i.e., cheetah) did have divergent morphology.
Convergence in morphology can result from evolutionary adaptations in species living in environments with similar selective pressures. Here, we investigate whether the shape of the forelimb long bones has converged in environments imposing similar functional constraints, using musteloid carnivores as a model. The limbs of quadrupeds are subjected to many factors that may influence their shape. They need to support body mass without collapsing or breaking, yet at the same time resist the stresses and strains induced by locomotion. This likely imposes strong constraints on their morphology. Our geometric morphometric analyses show that locomotion, body mass and phylogeny all influence the shape of the forelimb. Furthermore, we find a remarkable convergence between: (i) aquatic and semi-fossorial species, both displaying a robust forelimb, with a shape that improves stability and load transfer in response to the physical resistance imposed by the locomotor environment; and (ii) aquatic and arboreal/semi-arboreal species, with both groups displaying a broad capitulum. This augments the degree of pronation/supination, an important feature for climbing as well as grasping and manipulation ability, behaviors common to aquatic and arboreal species. In summary, our results highlight how musteloids with different locomotor ecologies show differences in the anatomy of their forelimb bones. Yet, functional demands for limb movement through dense media also result in convergence in forelimb long-bone shape between diverse groups, for example, otters and badgers.
© 2015 Anatomical Society.
Several theories predict that rapidly diversifying clades will also rapidly diverge phenotypically; yet, there are also reasons for suspecting that diversification and divergence might not be correlated. In the widely distributed squirrel clade (Sciuridae), we test for correlations between per-lineage speciation rates, species richness, disparity and a time-invariant measure of disparity that allows for comparing rates when evolutionary modes differ, as they do in squirrels. We find that species richness and speciation rates are not correlated with clade age or with each other. Disparity appears to be positively correlated with clade age because young, rapidly diversifying Nearctic grassland clades are strongly pulled to a single stable optimum but older, slowly diversifying Paleotropical forest clades contain lineages that diverge along multiple ecological and morphological lines. That contrast is likely due to both the environments they inhabit and their phylogenetic community structure. Our results argue against a shared explanation for diversity and disparity in favor of geographically mediated modes of speciation and ecologically mediated modes of phenotypic evolution. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Mammals have evolved a remarkable range of body sizes, yet their overall body plan remains unaltered. One challenge of evolutionary biology is to understand the mechanisms by which this size diversity is achieved, and how the mechanical challenges associated with changing body size are overcome. Despite the importance of the axial skeleton in body support and locomotion, and much interest in the allometry of the appendicular skeleton, little is known about vertebral allometry outside primates. This study compares evolutionary allometry of the thoracolumbar centra in two families of quadrupedal running mammals: Felidae and Bovidae. I test the hypothesis that, as size increases, the thoracolumbar region will resist increasing loads by becoming a) craniocaudally shorter, and b) larger in cross-sectional area, particularly in the sagittal plane. Length, width, and height of the thoracolumbar centra of 23 felid and 34 bovid species were taken. Thoracic, prediaphragmatic, lumbar, and postdiaphragmatic lengths were calculated, and diameters were compared at three equivalent positions: the midthoracic, the diaphragmatic and the midlumbar vertebra. Allometric slopes were calculated using a reduced major axis regression, on both raw and independent contrasts data. Slopes and elevations were compared using an ANCOVA. As size increases the thoracolumbar centra become more robust, showing preferential reinforcement in the sagittal plane. There was less allometric shortening of the thoracic than the lumbar region, perhaps reflecting constraints due to its connection with the respiratory apparatus. The thoracic region was more robust in bovids than felids, whereas the lumbar region was longer and more robust in felids than bovids. Elongation of lumbar centra increases the outlever of sagittal bending at intervertebral joints, increasing the total pelvic displacement during dorsomobile running. Both locomotor specializations and functional regionalization of the axial skeleton appear to have influenced its response to increasing size. J. Morphol., 2015. © 2015 Wiley Periodicals, Inc.
© 2015 Wiley Periodicals, Inc.
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.
The structure and dimensions of the lumbar vertebrae from 18 genera of African bovids (with a body weight range of 4–900 kg) were studied with reference to allometric and biomechanical factors. Centrum height scales with body weight according to McMahon's elastic similarity theory, but centrum width scales geometrically with body weight. Thus, the dimensions of bones need not scale according to a single principle. Transverse process orientation, as measured in two planes, varies allometrically with body weight; this trend may reflect size‐related differences in abdominal girth and spinal musculature. Bovids exhibit decreasing lumbar mobility in the sagittal plane with increasing body size, a phenomenon related to an increase in centrum height and the appearance of interlocking mechanisms (postzygapophysial ridges and prezygapophysial labra). Geometric scaling of centrum width and zygapophysial curvature is evidence that lateral flexion of the spine occurs throughout the family. In all taxa examined, the last lumbar vertebra exhibits an absolutely wider centrum and straight postzygapophyses, thus reducing lateral mobility at the lumbosacral joint. In heavier bovids, the observed restriction of lumbar flexion and extension to the lumbosacral joint is a consequence of the distribution of the shapes of the centra and the interlocking mechanisms of the zygapophyses.
Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.
The evolutionary history of the Order Carnivora is marked by episodes of iterative evolution. Although this pattern is widely reported in different carnivoran families, the mechanisms driving the evolution of carnivoran skull morphology remain largely unexplored. In this study we use coordinate-point extended eigenshape analysis (CP-EES) to summarize aspects of skull shape in large fissiped carnivores. Results of these comparisons enable the evaluation of the role of different factors constraining the evolution of carnivoran skull design. Empirical morphospaces derived from mandible anatomy show that all hypercarnivores (i.e., those species with a diet that consists almost entirely of vertebrate flesh) share a set of traits involved in a functional compromise between bite force and gape angle, which is reflected in a strong pattern of morphological convergence. Although the paths followed by different taxa to reach this "hypercarnivore shape-space" differ because of phylogenetic constraints, the morphological signature of hypercarnivory in the mandible is remarkably narrow and well constrained. In contrast, CP-EES of cranial morphology does not reveal a similar pattern of shape convergence among hypercarnivores. This suggests a lesser degree of morphological plasticity in the cranium compared to the mandible, which probably results from a compromise between different functional demands in the cranium (e.g., feeding, vision, olfactory sense, and brain processing) whereas the mandible is only involved in food acquisition and processing. Combined analysis of theoretical and empirical morphospaces for these skull data also show the lower anatomical disparity of felids and hyaenids compared to canids and ursids. This indicates that increasing specialization within the hypercarnivorous niche may constrain subsequent morphological and ecological flexibility. During the Cenozoic, similar skull traits appeared in different carnivoran lineages, generated by similar selection pressures (e.g., toward hypercarnivory) and shared developmental pathways. These pathways were likely the proximate source of constraints on the degree of variation associated with carnivoran skull evolution and on its direction.
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.
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.
Vertebrates exhibit tremendous diversity in body shape, though quantifying this variation has been challenging. In the past, researchers have used simplified metrics that either describe overall shape but reveal little about its anatomical basis or that characterize only a subset of the morphological features that contribute to shape variation. Here, we present a revised metric of body shape, the vertebrate shape index (VSI), which combines the four primary morphological components that lead to shape diversity in vertebrates: head shape, length of the second major body axis (depth or width), and shape of the precaudal and caudal regions of the vertebral column. We illustrate the usefulness of VSI on a data set of 194 species, primarily representing five major vertebrate clades: Actinopterygii, Lissamphibia, Squamata, Aves, and Mammalia. We quantify VSI diversity within each of these clades and, in the course of doing so, show how measurements of the morphological components of VSI can be obtained from radiographs, articulated skeletons, and cleared and stained specimens. We also demonstrate that head shape, secondary body axis, and vertebral characteristics are important independent contributors to body shape diversity, though their importance varies across vertebrate groups. Finally, we present a functional application of VSI to test a hypothesized relationship between body shape and the degree of axial bending associated with locomotor modes in ray-finned fishes. Altogether, our study highlights the promise VSI holds for identifying the morphological variation underlying body shape diversity as well as the selective factors driving shape evolution.
Patterns of morphological variation in the skulls of extant bears were studied as they relate to diet and feeding behaviour. Measurements of craniodental features were used to compute indices that reflect dietary adaptations of the dentition and biomechanical properties of the skull, jaw and related musculature. Species were classified as either carnivores, omnivores, herbivores or insectivores. Differences among dietary groups were assessed with analysis of variance and discriminant factor analysis. Results demonstrated significant morphological separation among all four groups. Carnivores were distinguished by, among other features, molar size reduction, flexible mandibles and, most surprisingly, relatively small carnassial blades. In contrast, herbivores displayed, among other features, large molar grinding areas, rigid mandibles and large carnassial blades. The insectivorous sloth bear was characterized by extreme reduction of the post-canine teeth. As expected, omnivores tended to have morphology intermediate between that of carnivorous and herbivorous ursids. Comparison with previous studies revealed that bears exhibit a different set of morphological specializations for diet than other carnivoran groups. Carnivorous ursids, for example, were found to share aspects of craniodental morphology with omnivorous canids. The relatively weak adaptations for carnivory observed in bears may be the result of selection for the ability to cope with temporal fluctuations in dietary components. The giant panda Ailuropoda
melanoleuca was found to have a relatively stiff jaw and great mechanical advantage of the jaw-closing muscles, features previously observed in carnivorous canids and unexpected in this herbivorous bear. Comparison of patterns of morphological variation and patterns of phylogenetic relationships among species revealed surprisingly strong congruence between morphology and phylogenetics.