Article

Different Evolutionary Pathways Lead to Incomplete Convergence of Elongate Body Shapes in Carnivoran Mammals

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Abstract

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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... Recently developed methods for identifying and measuring convergence are often accompanied by statistical tests for comparing observed convergence to that which is expected by chance (Arbuckle et al., 2014;Castiglione et al., 2019;Ingram & Mahler, 2013;Mahler et al., 2013;Speed & Arbuckle, 2017;Stayton, 2015a). The increased accessibility of quantitative tests for phenotypic convergence has led to a flood of recent studies on that topic (e.g., Alfieri et al., 2022;Arbour & Zanno, 2020;Baliga & Mehta, 2018;Baumgart et al., 2021;Bennion et al., 2022;Button & Zanno, 2020;Canale et al., 2022;Da Silva et al., 2018;Friedman et al., 2016;Grossnickle et al., 2020;Huie et al., 2021;Law, 2022;Martinez et al., 2020;Rincon-Sandoval et al., 2020;Rovinsky et al., 2021;Serio et al., 2020;Spear & Williams, 2020;Tamagnini et al., 2021;Zelditch et al., 2017). ...
... The C1-C4 measures (hereafter, "C-measures") developed by Stayton (2015a) are a popular means of quantifying morphological convergence (e.g., Alfieri et al., 2022;Arbour & Zanno, 2020;Baliga & Mehta, 2018;Baumgart et al., 2021;Bennion et al., 2022;Button & Zanno, 2020;Canale et al., 2022;Da Silva et al., 2018;Friedman & et al., 2016;Grossnickle et al., 2020;Huie et al., 2021;Law, 2022;Martinez et al., 2020;Rincon-Sandoval et al., 2020;Rovinsky et al., 2021;Spear & Williams, 2020;Tamagnini et al., 2021;Zelditch et al., 2017). C-measures are calculated using geometric distances in phenotypic space between focal lineages, relying on ancestral reconstructions for morphologies at ancestral nodes. ...
... an OU process (and inferred convergence) is an appropriate explanation for the simulated evolutionary patterns Cooper et al., 2016;Grabowksi et al., 2023;Ho & Ané, 2014). This procedure is prevalent in the literature (e.g., Baliga & Mehta, 2018;Collar et al., 2014;Friedman et al., 2016;Grossnickle et al., 2020;Law, 2022;Rincon-Sandoval et al., 2020). In these studies, support for multiple-regime OU models is usually interpreted as evidence that the focal lineages (assigned to a single regime) have convergently shifted toward a shared adaptive peak. ...
Article
Tests of phenotypic convergence can provide evidence of adaptive evolution, and the popularity of such studies has grown in recent years due to the development of novel, quantitative methods for identifying and measuring convergence. These methods include the commonly applied C1–C4 measures of Stayton (2015), which measure morphological distances between lineages, and Ornstein-Uhlenbeck (OU) model-fitting analyses, which test whether lineages converged on shared adaptive peaks. We test the performance of C-measures and other convergence measures under various evolutionary scenarios and reveal a critical issue with C-measures: they often misidentify divergent lineages as convergent. We address this issue by developing novel convergence measures— Ct1–Ct4-measures —that calculate distances between lineages at specific points in time, minimizing the possibility of misidentifying divergent taxa as convergent. Ct-measures are most appropriate when focal lineages are of the same or similar geologic ages (e.g., extant taxa), meaning that the lineages’ evolutionary histories include considerable overlap in time. Beyond C-measures, we find that all convergence measures are influenced by the position of focal taxa in phenotypic space, with morphological outliers often statistically more likely to be measured as strongly convergent. Further, we mimic scenarios in which researchers assess convergence using OU models with a priori regime assignments (e.g., classifying taxa by ecological traits) and find that multiple-regime OU models with phenotypically divergent lineages assigned to a shared selective regime often outperform simpler models. This highlights that model support for these multiple-regime OU models should not be assumed to always reflect convergence among focal lineages of a shared regime. Our new Ct1–Ct4-measures provide researchers with an improved comparative tool, but we emphasize that all available convergence measures are imperfect, and researchers should recognize the limitations of these methods and use multiple lines of evidence to test convergence hypotheses.
... Convergent evolution is interpreted as the recurrent evolution of similar characters between phylogenetically distant taxa (Stayton, 2008(Stayton, , 2015Wake et al., 2011;Losos, 2017;Morinaga & Bergmann, 2017). Convergence is considered to be ubiquitous throughout the tree of life, being recognized as a central subject in evolutionary biology (Stayton, 2015;Sackton & Clark, 2019;Law, 2021). It has been proposed that convergent characters can be produced by deterministic means driven through similar selective pressures or constraints acting on similar aspects of organisms, resulting in the predictability of evolution (Morris, 2003;Stayton, 2008;Losos, 2017;Blount et al., 2018). ...
... For example, in tunas the primary forcetransmitting tendons are in the horizontal septum; however, in the lamnid sharks, as in other sharks, the horizontal septum is reduced in the posterior half of the body, hence the primary linkage to the tail appears to be the hypaxial lateral tendons (Donley et al., 2004). Also, the convergence of elongated phenotypes in salamanders and carnivoran mammals has been associated with different morphological mechanisms of body elongation (Wake et al., 2011;Law, 2021). The increase of body length in salamanders can be associated with the elongation of individual vertebrae, whereas in carnivoran mammals it can be attributable to the elongation of the thoracic region, thoracic vertebrae or the lumbar region (Wake et al., 2011;Law, 2021). ...
... Also, the convergence of elongated phenotypes in salamanders and carnivoran mammals has been associated with different morphological mechanisms of body elongation (Wake et al., 2011;Law, 2021). The increase of body length in salamanders can be associated with the elongation of individual vertebrae, whereas in carnivoran mammals it can be attributable to the elongation of the thoracic region, thoracic vertebrae or the lumbar region (Wake et al., 2011;Law, 2021). In the particular case of anurans, Moen et al. (2016) suggested repeated convergence at large spatial and temporal scales, based on phenotypic similarity in relationship to microhabitat use, revealing that specialists in similar microhabitats (e.g. ...
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Convergent evolution has been shown to be a prominent feature of anuran evolutionary history. Studying the morphological pathways involved in the evolution of a convergent character allows us to test whether deterministic or contingent forces drive the evolution of characters. Here, we have assessed the morphological pathways associated with arboreal habits in species of six families of anurans (Hylidae, Eleutherodactylidae, Strabomantidae, Centrolenidae, Bufonidae and Hemiphractidae) through a comparative analysis of 19 phenotypic characters related to climbing ability. All species showed differences in the assessed characters, exhibiting variations in the distribution of their states and different ranges in all limb lengths. These variations implied a wide distribution across the morphospace as defined by a non-metric multidimensional scaling analysis (NMDS), with Rhinella paraguas (Bufonidae) being the most distinctive species, presenting unique characters such as the absence of intercalary elements, adhesive pads, subarticular tubercles and interphalangealis muscles of the hands. Our findings demonstrate that the morphological mechanisms involved in climbing ability of the ten species are different, suggesting distinct morphological pathways. Consequently, we advocate that historical contingency has an essential role in the evolution of arboreal habits among the species studied.
... Although there are only eight extant species, Malagasy carnivorans exhibit remarkable phenotypic and ecological diversity [22][23][24][25], so much so that no anatomical character can be used to define them. As a result, Malagasy carnivorans have traditionally been thought to belong to or originate from multiple feliform families (i.e. ...
... There is some evidence that the fossa and felids share a similar adaptive zone in cranial shape (∆AIC = 1.47; electronic supplementary material, table S2), but there is no statistical support for convergence in skull shape between the fossa and felids. These results suggest that cranial adaptations towards hypercarnivory in the fossa do not quite reach the felid morphotype (figures 5a and 6a) because the fossa and felids share an adaptive zone characterized by broad adaptive slopes rather than distinct adaptive peaks with steep slopes [24,52,68,69]. Euplerines occupy overlapping regions of cranial and mandibular morphospace with viverrids, the family to which they have been compared or classified with historically (figure 2). ...
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... The rise of adaptive landscape analyses enables researchers to investigate the adaptive evolution of performance by elucidating the underlying links between morpholog y, ecolog y, and fitness benefits (i.e., adaptiveness) at the macroevolutionary level (Arnold et al. 2001 ). Although Ornstein-Uhlenbeck (OU) models (Hansen 1997 ;Butler and King 2004 ;Beaulieu et al. 2012 ;Uyeda and Harmon 2014 ;Bastide et al. 2018 ) are widely used to test for the presence of adaptive zones or peaks (e.g., Collar et al. 2014 ;Price and Hopkins 2015 ;Friedman et al. 2016 ;Zelditch et al. 2017 ;Arbour et al. 2019 ;Law 2022 ;Slater 2022 ), it remains difficult to characterize the full topology (i.e., peaks, valleys, and slope) of the adaptive landscape as well as assess the relative importance of multiple performance traits and their contributions to overall adaptive landscape using these models. Adaptive landscape analyses (Polly et al. 2016 ;Dickson and Pierce 2019 ;Dickson et al. 2021 ) can overcome these limitations by examining the distribution of species in morphospace and its relationship to the relative importance of various functional traits on the topology of the adaptive landscape. ...
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Synopsis Analyses of form–function relationships are widely used to understand links between morphology, ecology, and adaptation across macroevolutionary scales. However, few have investigated functional trade-offs and covariance within and between the skull, limbs, and vertebral column simultaneously. In this study, we investigated the adaptive landscape of skeletal form and function in carnivorans to test how functional trade-offs among these skeletal regions contribute to ecological adaptations and the topology of the landscape. We found that morphological proxies of function derived from carnivoran skeletal regions exhibit trade-offs and covariation across their performance surfaces, particularly in the appendicular and axial skeletons. These functional trade-offs and covariation correspond as adaptations to different adaptive landscapes when optimized by various factors including phylogeny, dietary ecology, and, in particular, locomotor mode. Lastly, we found that the topologies of the optimized adaptive landscapes and underlying performance surfaces are largely characterized as a single gradual gradient rather than as rugged, multipeak landscapes with distinct zones. Our results suggest that carnivorans may already occupy a broad adaptive zone as part of a larger mammalian adaptive landscape that masks the form and function relationships of skeletal traits.
... Uhlenbeck (OU) models [18][19][20][21][22] are widely used to test for the presence of adaptive zones or 46 peaks (e.g., [7, [23][24][25][26][27][28]. However, it remains difficult to characterize the full topology (i.e., peaks, 47 valleys, and slope) of the adaptive landscape as well as assess the relative importance of multiple 48 and axial skeletons [34,45,47]. ...
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Full-text available
Analyses of form-function relationships are widely used to understand links between morphology, ecology, and species fitness across macroevolutionary scales. However, few have investigated functional trade-offs and covariance among functional traits within and between the skull, limbs, and vertebral column simultaneously. In this study, we investigated the adaptive landscape of skeletal form and function in carnivorans to test how functional trade-offs between these skeletal regions contribute to ecological adaptations and the topology of the landscape. We found that functional traits derived from carnivoran skeletal regions exhibit trade-offs and covariation across their performance surfaces, particularly in the appendicular and axial skeletons. These functional trade-offs and covariation corresponded as specializations to different adaptive landscapes when optimized by locomotor mode, diet, or family. Lastly, we found that the topologies of the optimized adaptive landscapes and underlying performance surfaces are largely characterized as smooth, gradual gradients between regions of low and high adaptive zones rather than as rugged, multipeak landscapes. Our results suggest that carnivorans may already occupy a broad adaptive zone as part of a larger mammalian adaptive landscape that masks the form and function relationships of skeletal traits.
... ; https://doi.org/10.1101/2024.03.25.586658 doi: bioRxiv preprint suggest that cranial adaptations towards hypercarnivory in the fossa do not quite reach the felid 299 morphotype (Fig. 5A, 6A) because the fossa and felids share an adaptive zone characterized by 300 broad adaptive slopes rather than distinct adaptive peaks with steep slopes [24,50,65,66]. 301 ...
Preprint
Full-text available
Madagascar is one of the world's foremost biodiversity hotspots with more than 90% of its species endemic to the island. Malagasy carnivorans are one of only four extant terrestrial mammalian clades endemic to Madagascar. Although there are only eight extant species, these carnivorans exhibit remarkable phenotypic and ecological diversity that is often hypothesized to have diversified through an adaptive radiation. Here, we investigated the evolution of skull diversity in Malagasy carnivorans and tested if they exhibited characteristics of convergence and an adaptive radiation. We found that their skull disparity exceeds that of any other feliform family, as their skulls vary widely and capture a large amount of the morphological variation found across all feliforms. We also found evidence of shared adaptive zones in cranial shape between euplerid subclades and felids, herpestids, and viverrids. Lastly, contrary to predictions of adaptive radiation, we found that Malagasy carnivorans do not exhibit rapid lineage diversification and only marginally faster rates of mandibular shape evolution, and to a lesser extent cranial shape evolution, compared to other feliforms. These results reveal that exceptional diversification rates are not necessary to generate the striking phenotypic diversity that evolved in carnivorans after their dispersal to and isolation on Madagascar.
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Tests of phenotypic convergence can provide evidence of adaptive evolution, and the popularity of such studies has grown in recent years due to the development of novel, quantitative methods for identifying and measuring convergence. These methods include the commonly applied C 1– C 4 measures of Stayton (2015), which measure morphological distances between lineages in phylomorphospace, and Ornstein-Uhlenbeck evolutionary model-fitting analyses to test whether lineages have convergently evolved toward adaptive peaks. We test the performance of C -measures and other convergence measures under various evolutionary scenarios. We reveal critical issues with C -measures, which we help to address by developing novel convergence measures ( Ct 1– Ct 4-measures) that measure distances between lineages at specific points in time. The most substantial issue with C -measures is that they will often misidentify divergent lineages as convergent; this is most common when focal taxa are morphological outliers. In contrast, our new Ct -measures minimize the possibility of misidentifying divergent taxa as convergent. Ct -measures are most appropriate when putatively convergent lineages are of the same or similar geologic ages (e.g., extant taxa), meaning that all or most of the evolutionary histories of the lineages overlap in time. Beyond C -measures, we demonstrate issues with other convergence measures. We find that all distance-based convergence measures are influenced by the position of putatively convergent taxa in morphospace, with morphological outliers often statistically more likely to be categorized as convergent by chance. Further, we demonstrate that multiple-regime Ornstein-Uhlenbeck models often outperform simpler models when fit to divergent lineages, highlighting that model support for multiple-regime models should not always be assumed to reflect convergence among focal lineages. The issues with convergence measures highlighted here are especially relevant because they influence the degree of inferred convergence in many past studies, raising the concern that many lineages have been mistakenly identified as convergent. Our new convergence measures provide researchers with an improved comparative tool for future studies. Nonetheless, we emphasize that all available convergence measures are imperfect, and researchers should recognize the limitations of these methods and use multiple lines of evidence when inferring and measuring convergence.
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Morphological convergence is an intensely studied macroevolutionary phenomenon. It refers to the morphological resemblance between phylogenetically distant taxa. Currently available methods to explore evolutionary convergence either: rely on the analysis of the phenotypic resemblance between sister clades as compared to their ancestor, fit different evolutionary regimes to different parts of the tree to see whether the same regime explains phenotypic evolution in phylogenetically distant clades, or assess deviations from the congruence between phylogenetic and phenotypic distances. We introduce a new test for morphological convergence working directly with non-ultrametric (i.e. paleontological) as well as ultrametric phylogenies and multivariate data. The method (developed as the function search.conv within the R package RRphylo) tests whether unrelated clades are morphologically more similar to each other than expected by their phylogenetic distance. It additionally permits using known phenotypes as the most recent common ancestors of clades, taking full advantage of fossil information. We assessed the power of search.conv and the incidence of false positives by means of simulations, and then applied it to three well-known and long-discussed cases of (purported) morphological convergence: the evolution of grazing adaptation in the mandible of ungulates with high-crowned molars, the evolution of mandibular shape in sabertooth cats, and the evolution of discrete ecomorphs among anoles of Caribbean islands. The search.conv method was found to be powerful, correctly identifying simulated cases of convergent morphological evolution in 95% of the cases. Type I error rate is as low as 4–6%. We found search.conv is some three orders of magnitude faster than a competing method for testing convergence.
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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.
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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.
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An elongate body with reduced or absent limbs has evolved independently in many ectothermic vertebrate lineages. While much effort has been spent examining the morphological pathways to elongation in these clades, quantitative investigations into the evolution of elongation in endothermic clades are lacking. We quantified body shape in 61 musteloid 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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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.
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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. This article is protected by copyright. All rights reserved.
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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.
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Skull shape convergence is pervasive among vertebrates. Although this is frequently inferred to indicate similar functional underpinnings, neither the specific structure-function linkages nor the selective environments in which the supposed functional adaptations arose are commonly identified and tested. We demonstrate that nonfeeding factors relating to sexual maturity and precipitation-related arboreality also can generate structure-function relationships in the skulls of carnivorans (dogs, cats, seals, and relatives) through covariation with masticatory performance. We estimated measures of masticatory performance related to ecological variables that covary with cranial shape in the mammalian order Carnivora, integrating geometric morphometrics and finite element analyses. Even after accounting for phylogenetic autocorrelation, cranial shapes are significantly correlated to both feeding and nonfeeding ecological variables, and covariation with both variable types generated significant masticatory performance gradients. This suggests that mechanisms of obligate shape covariation with nonfeeding variables can produce performance changes resembling those arising from feeding adaptations in Carnivora.
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Recent years have seen increased interest in phylogenetic comparative analyses of multivariate datasets, but to date the varied proposed approaches have not been extensively examined. Here we review the mathematical properties required of any multivariate method, and specifically evaluate existing multivariate phylogenetic comparative methods in this context. Phylogenetic comparative methods based on the full multivariate likelihood are robust to levels of covariation among trait dimensions and are insensitive to the orientation of the dataset, but display increasing model misspecification as the number of trait dimensions increases. This is because the expected evolutionary covariance matrix (V) used in the likelihood calculations becomes more ill-conditioned as trait dimensionality increases, and as evolutionary models become more complex. Thus, these approaches are only appropriate for datasets with few traits and many species. Methods that summarize patterns across trait dimensions treated separately (e.g., SURFACE) incorrectly assume independence among trait dimensions, resulting in nearly a 100% model misspecification rate. Methods using pairwise composite likelihood are highly sensitive to levels of trait covariation, the orientation of the dataset, and the number of trait dimensions. The consequences of these debilitating deficiencies is that a user can arrive at differing statistical conclusions, and therefore biological inferences, simply from a dataspace rotation, like principal component analysis. By contrast, algebraic generalizations of the standard phylogenetic comparative toolkit that use the trace of covariance matrices are insensitive to levels of trait covariation, the number of trait dimensions, and the orientation of the dataset. Further, when appropriate permutation tests are used, these approaches display acceptable Type I error and statistical power. We conclude that methods summarizing information across trait dimensions, as well as pairwise composite likelihood methods should be avoided, while algebraic generalizations of the phylogenetic comparative toolkit provide a useful means of assessing macroevolutionary patterns in multivariate data. Finally, we discuss areas in which multivariate phylogenetic comparative methods are still in need of future development; namely highly multivariate Ornstein-Uhlenbeck models and approaches for multivariate evolutionary model comparisons.
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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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Recent developments in quantitative-genetic theory have shown that natural selection can be viewed as the multivariate relationship between fitness and phenotype. This relationship can be described by a multidimensional surface depicting fitness as a function of phenotypic traits. We examine the connection between this surface and the coefficients of phenotypic selection that can be estimated by multiple regression and show how the interpretation of multivariate selection can be facilitated through the use of the method of canonical analysis. The results from this analysis can be used to visualize the surface implied by a set of selection coefficients. Such a visualization provides a compact summary of selection coefficients, can aid in the comparison of selection surfaces, and can help generate testable hypotheses as to the adaptive significance of the traits under study. Further, we discuss traditional definitions of directional, stabilizing, and disruptive selection and conclude that selection may be more usefully classified into two general modes, directional and nonlinear selection, with stabilizing and disruptive selection as special cases of nonlinear selection.
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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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Phylogenetic comparative methods are increasingly used to give new insights into the dynamics of trait evolution in deep time. For continuous traits the core of these methods is a suite of models that attempt to capture evolutionary patterns by extending the Brownian constant variance model. However, the properties of these models are often poorly understood, which can lead to the misinterpretation of results. Here we focus on one of these models - the Ornstein Uhlenbeck (OU) model. We show that the OU model is frequently incorrectly favoured over simpler models when using Likelihood ratio tests, and that many studies fitting this model use datasets that are small and prone to this problem. We also show that very small amounts of error in datasets can have profound effects on the inferences derived from OU models. Our results suggest that simulating fitted models and comparing with empirical results is critical when fitting OU and other extensions of the Brownian model. We conclude by making recommendations for best practice in fitting OU models in phylogenetic comparative analyses, and for interpreting the parameters of the OU model.
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Striking evolutionary convergence can lead to similar sets of species in different locations, such as in cichlid fishes and Anolis lizards, and suggests that evolution can be repeatable and predictable across clades. Yet most examples of convergence involve relatively small temporal and/or spatial scales. Some authors have speculated that at larger scales (e.g. across continents), differing evolutionary histories will prevent convergence. However, few studies have compared the contrasting roles of convergence and history, and none have done so at large scales. Here we develop a two-part approach to test the scale over which convergence can occur, comparing the relative importance of convergence and history in macroevolution using phylogenetic models of adaptive evolution. We apply this approach to data from morphology, ecology, and phylogeny from 167 species of anuran amphibians (frogs) from ten local sites across the world, spanning ~160 million years of evolution. Mapping ecology on the phylogeny revealed that similar microhabitat specialists (e.g. aquatic, arboreal) have evolved repeatedly across clades and regions, producing many evolutionary replicates for testing for morphological convergence. By comparing morphological optima for clades and microhabitat types (our first test), we find that convergence associated with microhabitat use dominates frog morphological evolution, producing recurrent ecomorphs that together encompass all sampled species in each community in each region. However, our second test, which examines whether and how much species differ from their inferred optima, shows that convergence is incomplete: that is, phenotypes of most species are still somewhat distant from the estimated optimum for each microhabitat, seemingly because of insufficient time for more complete adaptation (an effect of history). Yet these effects of history are related to past ecologies, and not clade membership. Overall, our study elucidates the dominant drivers of morphological evolution across a major vertebrate clade and shows that evolution can be repeatable at much greater temporal and spatial scales than commonly thought. It also provides an analytical framework for testing other potential examples of large-scale convergence.
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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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windex is a package developed for the R statistical environment to provide novel tools for the analysis of convergent evolution. The recently described Wheatsheaf index provides quantitative measures of the strength of convergence and opens up new possibilities for exploring this evolutionary phenomenon. The windex package allows implementation of this method with additional functions that can be used to create plots and perform statistical tests. R provides compatibility with other packages, and the R environment is familiar to many researchers. The windex package is freely available from CRAN: http://cran.r-project.org/web/packages/windex/. Consequently, windex can be installed directly from R and is distributed under the GNU General Public License 2.0.
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Performance capacity influences ecology, behavior and fitness, and is determined by the underlying phenotype. The phenotype-performance relationship can influence the evolutionary trajectory of an organism. Several types of phenotype-performance relationships have been described, including one-to-one relationships between a single phenotypic trait and performance measure, trade-offs and facilitations between a phenotypic trait and multiple performance measures, and redundancies between multiple phenotypic traits and a single performance measure. The F-matrix is an intraspecific matrix of measures of statistical association between phenotype and performance that is used to quantify these relationships. We extend the F-matrix in two ways. First, we use the F-matrix to describe how the different phenotype-performance relationships occur simultaneously and interact in functional systems, a phenomenon we call many-to-many mapping. Second, we develop methods to compare F-matrices among species and compare phenotype-performance relationships at microevolutionary and macroevolutionary levels. We demonstrate the expanded F-matrix approach with a dataset of eight phrynosomatine lizard species, including six phenotypic traits and two measures of locomotor performance. Our results suggest that all types of relationships occur in this system and that phenotypic traits involved in trade-offs are more functionally constrained and tend evolve slower interspecifically than those involved in facilitations or one-to-one relationships.
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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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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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Recent developments in quantitative-genetic theory have shown that natural selection can be viewed as the multivariate relationship between fitness and phenotype. This relationship can be described by a multidimensional surface depicting fitness as a function of phenotypic traits. We examine the connection between this surface and the coefficients of phenotypic selection that can be estimated by multiple regression and show how the interpretation of multivariate selection can be facilitated through the use of the method of canonical analysis. The results from this analysis can be used to visualize the surface implied by a set of selection coefficients. Such a visualization provides a compact summary of selection coefficients, can aid in the comparison of selection surfaces, and can help generate testable hypotheses as to the adaptive significance of the traits under study. Further, we discuss traditional definitions of directional, stabilizing, and disruptive selection and conclude that selection may be more usefully classified into two general modes, directional and nonlinear selection, with stabilizing and disruptive selection as special cases of nonlinear selection.
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Many ecological and evolutionary studies seek to explain patterns of shape variation and its covariation with other variables. Geometric morphometrics is often used for this purpose, where a set of shape variables are obtained from landmark coordinates following a P rocrustes superimposition. We introduce geomorph: a software package for performing geometric morphometric shape analysis in the r statistical computing environment. Geomorph provides routines for all stages of landmark‐based geometric morphometric analyses in two and three‐dimensions. It is an open source package to read, manipulate, and digitize landmark data, generate shape variables via P rocrustes analysis for points, curves and surfaces, perform statistical analyses of shape variation and covariation, and to provide graphical depictions of shapes and patterns of shape variation. An important contribution of geomorph is the ability to perform P rocrustes superimposition on landmark points, as well as semilandmarks from curves and surfaces. A wide range of statistical methods germane to testing ecological and evolutionary hypotheses of shape variation are provided. These include standard multivariate methods such as principal components analysis, and approaches for multivariate regression and group comparison. Methods for more specialized analyses, such as for assessing shape allometry, comparing shape trajectories, examining morphological integration, and for assessing phylogenetic signal, are also included. Several functions are provided to graphically visualize results, including routines for examining variation in shape space, visualizing allometric trajectories, comparing specific shapes to one another and for plotting phylogenetic changes in morphospace. Finally, geomorph participates to make available advanced geometric morphometric analyses through the r statistical computing platform.
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Comparative methods used to study patterns of evolutionary change in a continuous trait on a phylogeny range from Brownian motion processes to models where the trait is assumed to evolve according to an Ornstein-Uhlenbeck (OU) process. Although these models have proved useful in a variety of contexts, they still do not cover all the scenarios biologists want to examine. For models based on the OU process, model complexity is restricted in current implementations by assuming that the rate of stochastic motion and the strength of selection do not vary among selective regimes. Here, we expand the OU model of adaptive evolution to include models that variously relax the assumption of a constant rate and strength of selection. In its most general form, the methods described here can assign each selective regime a separate trait optimum, a rate of stochastic motion parameter, and a parameter for the strength of selection. We use simulations to show that our models can detect meaningful differences in the evolutionary process, especially with larger sample sizes. We also illustrate our method using an empirical example of genome size evolution within a large flowering plant clade.
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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.
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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.
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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
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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. This article is protected by copyright. All rights reserved
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Convergent evolution of phenotypes is considered evidence that evolution is deterministic. Establishing if such convergent phenotypes arose through convergent evolutionary pathways is a stronger test of determinism. We studied the evolution of snake‐like body shapes in six clades of lizards, each containing species ranging from short‐bodied and pentadactyl to long‐bodied and limbless. We tested whether body shapes that evolved in each clade were convergent, and whether clades evolved snake‐like body shapes following convergent evolutionary pathways. Our analyses showed that indeed species with the same numbers of digits in each clade evolved convergent body shapes. We then compared evolutionary pathways among clades by considering patterns of evolutionary integration and shape of relationship among body parts, patterns of vertebral evolution, and models of digit evolution. We found that all clades elongated their bodies through the addition, not elongation, of vertebrae, and had similar patterns of integration. However, patterns of integration, the body parts that were related by a linear or a threshold model, and patterns of digit evolution differed among clades. These results showed that clades followed different evolutionary pathways. This suggests an important role of historical contingency as opposed to determinism in the convergent evolution of snake‐like body shapes. This article is protected by copyright. All rights reserved
Article
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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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.
Article
Among extinct ichthyosaurs the Jurassic forms Ichthyosaurus and Stenopterygius share a number of anatomical specializations with lamnid sharks, characterized in the white shark, Carcharodon carcharias. These features allow their inclusion within the mode of high-speed thunniform swimming to which only two other equally distinctive phylogenetic groups belong, tuna and dolphins—a striking testaments to evolutionary convergence. Jurassic ichthyosaurs evolved from reptiles that had returned to the sea (secondarily adapted) about 250 million years ago (MYA) while lamnid sharks evolved about 50 MYA from early cartilaginous fishes (originating ca. 400 MYA). Their shared independently evolved anatomical characteristics are discussed. These include a deep tear-drop body shape that helped initially define members as thunniform swimmers. Later, other critical structural characteristics were discovered such as the crossed-fiber architecture of the skin, high-speed adapted dorsal and caudal fins, a caudal peduncle and series of ligaments to enable transmission of power from the musculature located anteriorly to the caudal fin. Both groups also share a similar chemistry of the dermal fibers, i.e., the scleroprotein collagen.
Article
Convergent evolution is an important phenomenon in the history of life. Despite this, there is no common definition of convergence used by biologists. Instead, several conceptually different definitions are employed. The primary dichotomy is between pattern-based definitions, where independently evolved similarity is sufficient for convergence, and process-based definitions, where convergence requires a certain process to produce this similarity. The unacknowledged diversity of definitions can lead to problems in evolutionary research. Process-based definitions may bias researchers away from studying or recognizing other sources of independently-evolved similarity, or lead researchers to interpret convergent patterns as necessarily caused by a given process. Thus, pattern-based definitions are recommended. Existing measures of convergence are reviewed, and two new measures are developed. Both are pattern-based and conceptually minimal, quantifying nothing but independently-evolved similarity. One quantifies the amount of phenotypic distance between two lineages that is closed by subsequent evolution; the other simply counts the number of lineages entering a region of phenotypic space. The behavior of these measures is explored in simulations; both show acceptable Type I and Type II error. The study of convergent evolution will be facilitated if researchers are explicit about working definitions of convergence and adopt a standard toolbox of convergence measures. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
Article
1. We present mvMORPH, a package of multivariate phylogenetic comparative methods for the R statistical environment. mvMORPH is freely available on the CRAN package repository (http://cran.r-project.org/web/packages/mvMORPH/). 2. mvMORPH allows fitting a range of multivariate evolutionary models under a maximum-likelihood criterion. Initially developed in the context of phylogenetic analysis of multiple morphometric traits, its use can be extended to any biological dataset with one or multiple covarying continuous traits. All the fitting models include the possibility to use SIMMAP-like mapping, which may be useful for fitting changes along lineages at a given point in time. All models provide diagnostic metrics for convergence and reliability of estimates, as well as the possibility to include trait measurement errors in model estimates. 3. New features provided by the mvMORPH package include the possibility of fitting models with changes in the mode of evolution along the phylogeny, which will be particularly meaningful in comparative analyses that include extinct taxa, e.g., when testing changes in evolutionary mode associated with global biotic/abiotic events. 4. We briefly describe the models already included in mvMORPH, and provide some demonstration of the use of the package with two simulated worked examples.
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
Abstract Convergence is central to the study of evolution because it demonstrates the power of natural selection to deterministically shape phenotypic diversity. However, the conditions under which a common morphology repeatedly evolves may be restrictive. Many factors, such as differing genetic and environmental backgrounds and many-to-one mapping of form to function, contribute to variability in responses to selection. Nevertheless, lineages may evolve similar, even if not identical, forms given a shared selective regime, providing opportunities to examine the relative importance of natural selection, constraint, and contingency. Here, we show that following 10 transitions to durophagy (eating hard-shelled prey) in moray eels (Muraenidae), cranial morphology repeatedly evolved toward a novel region of morphological space indicative of enhanced feeding performance on hard prey. Disparity among the resulting 15 durophagous species, however, is greater than disparity among ancestors that fed on large evasive prey, contradicting the pattern expected under convergence. This elevated disparity is a consequence of lineage-specific responses to durophagy, in which independent transitions vary in the suites of traits exhibiting the largest changes. Our results reveal a pattern of imperfect convergence, which suggests shared selection may actually promote diversification because lineages often differ in their phenotypic responses to similar selective demands.
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.
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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.
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Stochastic computer simulation is an important method for comparing the evolu-tionary patterns and processes associated with radically different intervals of time. This paper demonstrates how to simulate the evolution of complex morphologies over geological timescales of millions of generations. The simulations are used to test how various assumptions about microevolutionary parameters and processes manifest themselves on macroevolutionary timescales. Complex morphology is modelled using geometric representations of shape (e.g., landmarks or outlines), and so the procedure described here is limited to single rigid structures. The procedure is based on empiri-cally measured phenotypic correlations, which constrain the evolutionary outcomes in biologically realistic ways. Different microevolutionary assumptions about covariances, population size, and evolutionary mode can be tested by incorporating them into the simulation parameters. The evolution of molar tooth morphology in shrews is simulated under four differ-ent evolutionary modes: (1) randomly fluctuating selection; (2) directional selection; (3) stabilizing selection; and (4) genetic drift. Each of these modes leaves a distinctive imprint on the distribution of morphological distances, a feature that can be used to reconstruct the mode from real comparative data. A comparison of the results with real data on shrew molar diversity suggests that teeth have evolved predominantly by ran-domly fluctuating selection. The rate of divergence in shrew molars is greater than expected under drift, but it is neither linear nor static as expected with directional or stabilizing selection. The evolution of morphology with randomly fluctuating selection is also simulated on a phylogenetic tree. Daughter species share derived morphologies and positions within the principal components spaces in which the simulation is run. This result sug-gests that phylogeny can be successfully reconstructed from multivariate morphomet-ric data when organisms have evolved under any mode except strong stabilizing selection.
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Within the ray-finned fishes, eel-like (extremely elongate) body forms have evolved multiple times from deeper-bodied forms. Previous studies have shown that elongation of the vertebral column may be associated with an increase in the number of vertebrae, an increase in the length of the vertebral centra, or a combination of both. Because the vertebral column of fishes has at least two anatomically distinct regions (i.e. abdominal and caudal), an increase in the number and relative length of the vertebrae could be region-specific or occur globally across the length of the vertebral column. In the present study, we recorded vertebral counts and measurements of vertebral aspect ratio (vertebral length/width) from museum specimens for 54 species representing seven groups of actinopterygian fishes. We also collected, from published literature, vertebral counts for 813 species from 14 orders of actinopterygian and elasmobranch fishes. We found that the number of vertebrae can increase independently in the abdominal and caudal regions of the vertebral column, but changes in aspect ratio occur similarly in both regions. These findings suggest that abdominal vertebral number, caudal vertebral number, and vertebral aspect ratio are controlled by separate developmental modules. Based on these findings, we suggest some candidate developmental mechanisms that may contribute to vertebral column patterning in fishes. Our study is an example of how comparative anatomical studies of adults can generate testable hypotheses of evolutionary changes in developmental mechanisms. (c) 2007 The Linnean Society of London, Biological Journal of the Linnean Society.