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Showing papers in "Evolutionary Biology-new York in 2009"


Journal ArticleDOI
TL;DR: The powerful visualization tools of geometric morphometrics and the typically large amount of shape variables give rise to a specific exploratory style of analysis, allowing the identification and quantification of previously unknown shape features.
Abstract: Geometric morphometrics is the statistical analysis of form based on Cartesian landmark coordinates. After separating shape from overall size, position, and orientation of the landmark configurations, the resulting Procrustes shape coordinates can be used for statistical analysis. Kendall shape space, the mathematical space induced by the shape coordinates, is a metric space that can be approximated locally by a Euclidean tangent space. Thus, notions of distance (similarity) between shapes or of the length and direction of developmental and evolutionary trajectories can be meaningfully assessed in this space. Results of statistical techniques that preserve these convenient properties—such as principal component analysis, multivariate regression, or partial least squares analysis—can be visualized as actual shapes or shape deformations. The Procrustes distance between a shape and its relabeled reflection is a measure of bilateral asymmetry. Shape space can be extended to form space by augmenting the shape coordinates with the natural logarithm of Centroid Size, a measure of size in geometric morphometrics that is uncorrelated with shape for small isotropic landmark variation. The thin-plate spline interpolation function is the standard tool to compute deformation grids and 3D visualizations. It is also central to the estimation of missing landmarks and to the semilandmark algorithm, which permits to include outlines and surfaces in geometric morphometric analysis. The powerful visualization tools of geometric morphometrics and the typically large amount of shape variables give rise to a specific exploratory style of analysis, allowing the identification and quantification of previously unknown shape features.

1,017 citations


Journal ArticleDOI
TL;DR: It is argued that the direct study of the developmental determinants of integration in model systems is necessary to fully interpret patterns of covariation in natural populations, to link covariation patterns to the processes that generate them, and to understand their significance for evolutionary explanation.
Abstract: Organisms represent a complex arrangement of anatomical structures and individuated parts that must maintain functional associations through development. This integration of variation between functionally related body parts and the modular organization of development are fundamental determinants of their evolvability. This is because integration results in the expression of coordinated variation that can create preferred directions for evolutionary change, while modularity enables variation in a group of traits or regions to accumulate without deleterious effects on other aspects of the organism. Using our own work on both model systems (e.g., lab mice, avians) and natural populations of rodents and primates, we explore in this paper the relationship between patterns of phenotypic covariation and the developmental determinants of integration that those patterns are assumed to reflect. We show that integration cannot be reliably studied through phenotypic covariance patterns alone and argue that the relationship between phenotypic covariation and integration is obscured in two ways. One is the superimposition of multiple determinants of covariance in complex systems and the other is the dependence of covariation structure on variances in covariance-generating processes. As a consequence, we argue that the direct study of the developmental determinants of integration in model systems is necessary to fully interpret patterns of covariation in natural populations, to link covariation patterns to the processes that generate them, and to understand their significance for evolutionary explanation.

377 citations


Journal ArticleDOI
TL;DR: The data provide evidence that mammalian skull evolution can be viewed as a history of inter-module parcellation, with the modules themselves being more clearly marked in those lineages with lower overall magnitude of integration.
Abstract: Morphological integration refers to the modular structuring of inter-trait relationships in an organism, which could bias the direction and rate of morphological change, either constraining or facilitating evolution along certain dimensions of the morphospace. Therefore, the description of patterns and magnitudes of morphological integration and the analysis of their evolutionary consequences are central to understand the evolution of complex traits. Here we analyze morphological integration in the skull of several mammalian orders, addressing the following questions: are there common patterns of inter-trait relationships? Are these patterns compatible with hypotheses based on shared development and function? Do morphological integration patterns and magnitudes vary in the same way across groups? We digitized more than 3,500 specimens spanning 15 mammalian orders, estimated the correspondent pooled within-group correlation and variance/covariance matrices for 35 skull traits and compared those matrices among the orders. We also compared observed patterns of integration to theoretical expectations based on common development and function. Our results point to a largely shared pattern of inter-trait correlations, implying that mammalian skull diversity has been produced upon a common covariance structure that remained similar for at least 65 million years. Comparisons with a rodent genetic variance/covariance matrix suggest that this broad similarity extends also to the genetic factors underlying phenotypic variation. In contrast to the relative constancy of inter-trait correlation/covariance patterns, magnitudes varied markedly across groups. Several morphological modules hypothesized from shared development and function were detected in the mammalian taxa studied. Our data provide evidence that mammalian skull evolution can be viewed as a history of inter-module parcellation, with the modules themselves being more clearly marked in those lineages with lower overall magnitude of integration. The implication of these findings is that the main evolutionary trend in the mammalian skull was one of decreasing the constraints to evolution by promoting a more modular architecture.

271 citations


Journal ArticleDOI
TL;DR: Simulation of the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull found them to be quite variable among mammals, providing evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skulls had important consequences in termsof evolutionary flexibility of the mammalian lineages.
Abstract: Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.

201 citations


Journal ArticleDOI
TL;DR: It is suggested that the standard deviation of the eigenvalues is a better reflection of the overall morphological integration than the average correlation and a relative measure that is independent of the number of traits and can thus be readily compared across datasets.
Abstract: The concept of morphological integration describes the pattern and the amount of correlation between morphological traits. Integration is relevant in evolutionary biology as it imposes constraint on the variation that is exposed to selection, and is at the same time often based on heritable genetic correlations. Several measures have been proposed to assess the amount of integration, many using the distribution of eigenvalues of the correlation matrix. In this paper, we analyze the properties of eigenvalue variance as a much applied measure. We show that eigenvalue variance scales linearly with the square of the mean correlation and propose the standard deviation of the eigenvalues as a suitable alternative that scales linearly with the correlation. We furthermore develop a relative measure that is independent of the number of traits and can thus be readily compared across datasets. We apply this measure to examples of phenotypic correlation matrices and compare our measure to several other methods. The relative standard deviation of the eigenvalues gives similar results as the mean absolute correlation (W.P. Cane, Evol Int J Org Evol 47:844–854, 1993) but is only identical to this measure if the correlation matrix is homogenous. For heterogeneous correlation matrices the mean absolute correlation is consistently smaller than the relative standard deviation of eigenvalues and may thus underestimate integration. Unequal allocation of variance due to variation among correlation coefficients is captured by the relative standard deviation of eigenvalues. We thus suggest that this measure is a better reflection of the overall morphological integration than the average correlation.

180 citations


Journal ArticleDOI
TL;DR: Results indicate that integration decreases as hands and feet become functionally divergent, and that the strongly integrated hand and foot skeletons of quadrupedal monkeys respond to selection in a highly collinear manner, even when simulated selective pressures acting on each autopod are in opposite directions in phenotypic space.
Abstract: Morphological integration theory predicts that sets of phenotypic traits that covary strongly due to developmental and/or functional connections between them eventually co-evolve because of a coordinated response to selection, and accordingly become less independently evolvable. This process is not irreversible, however, and phenotypic traits can become less integrated, and hence more independently evolvable, in the context of selection for divergent functions and morphologies. This study examines the reciprocal relationship between shared function, integration and evolvability by comparing integration patterns among serially homologous skeletal elements in the hands and feet of a functionally diverse sample of catarrhine primates. Two hypotheses are tested: (1) species in which the autopods are functionally more similar (e.g. quadrupedal monkeys) have more strongly integrated autopods than species in which the autopods are functionally divergent (e.g. gibbons, humans) and (2) the latter have autopods that are more evolvable, collectively and independently. Morphometric data from selected hand and foot digital rays were used to derive phenotypic variance/covariance matrices. The strength of integration among autopods was quantified using eigenanalysis and a measure of trait variational autonomy. Evolvability was estimated by subjecting phenotypic variance/covariance matrices to simulated random selection gradients, and comparing evolutionary responses among species. Results indicate that integration decreases as hands and feet become functionally divergent, and that the strongly integrated hand and foot skeletons of quadrupedal monkeys respond to selection in a highly collinear manner, even when simulated selective pressures acting on each autopod are in opposite directions in phenotypic space. Results confirm that the evolvability of morphological traits depends largely on how strongly they covary with other traits, but also with body size. The role of pleiotropy as a developmental mechanism underlying integration and evolvability is also discussed.

99 citations


Journal ArticleDOI
TL;DR: The structure of integration suggests that the mandible cannot be decomposed into parts but rather is a single connected unit, a result consistent with its functional integration, which may arise from function-induced growth.
Abstract: The mammalian mandible is a developmentally modular but functionally integrated system. Whether morphological integration can evolve to match the optimal pattern of functional integration may depend on the developmental origin of integration, specifically, on the role that direct epigenetic interactions play in shaping integration. These interactions are hypothesized to integrate modules and also to be highly conservative, potentially constraining the evolution of integration. Using the fox squirrel (Sciurus niger) mandible as a model system, we test five a priori developmental hypotheses that predict mandibular integration and we also explore for correlations between shapes of mandibular regions not anticipated by any of the developmental models. To determine whether direct epigenetic interactions are highly conserved in rodents, we examine the correlation structure of fluctuating asymmetry, and compare integration patterns between fox squirrels and prairie deer mice (Peromyscus maniculatus bairdii). In fox squirrels, we find a correlation structure unanticipated by all a priori developmental models: adjacent parts along the proximodistal jaw axis are correlated whereas more distant ones are not. The most notable exception is that the shape of the anterior incisor alveolus is correlated with the shape of the ramus (FA component) or coronoid (symmetric component). Those exceptions differ between species; in prairie deer mice, the molar alveolus is connected to more parts, and the incisor alveolus to fewer, than in fox squirrels. The structure of integration suggests that the mandible cannot be decomposed into parts but rather is a single connected unit, a result consistent with its functional integration. That match between functional and developmental integration may arise, at least in part, from function-induced growth, building developmental integration into the functional system and enabling direct epigenetic interactions to evolve when function does.

94 citations


Journal ArticleDOI
M. Yao1, J. Rosenfeld1, S. Attridge1, S. Sidhu1, Vadim Aksenov1, C. D. Rollo1 
TL;DR: This work hypothesized that necromones are a phylogenetically ancient class of related signals and predicted that terrestrial Isopoda would avoid body fluids and corpses using fatty acid “necromones,” and predicted a priori that social caterpillars (lacking known dispersants) would be repelled by their own body fluid and unsaturated fatty acids.
Abstract: Illness, death, and costs of immunity and injury strongly select for avoidance of predators or contagion. Ants, cockroaches, and collembola recognize their dead using unsaturated fatty acids (e.g., oleic or linoleic acid) as “necromone” cues. Ants, bees, and termites remove dead from their nests (necrophoric behavior) whereas semi-social species seal off corpses or simply avoid their dead or injured (necrophobic behavior). Alarm and avoidance responses to exudates from injured conspecifics are widespread. This involves diverse pheromones, complex chemistry and learning. We hypothesized that necromones are a phylogenetically ancient class of related signals and predicted that terrestrial Isopoda (that strongly aggregate and lack known dispersants) would avoid body fluids and corpses using fatty acid “necromones.” Isopods were repelled by crushed conspecifics (blood), intact corpses, and alcohol extracts of bodies. As predicted, the repellent fraction contained oleic and linoleic acids and authentic standards repelled several isopod species. We further predicted a priori that social caterpillars (lacking known dispersants) would be repelled by their own body fluids and unsaturated fatty acids. Both tent caterpillars and fall webworms avoided branches treated with conspecific body fluid. Oleic and linoleic acids were also strongly avoided by both species. Necromone signaling appears widespread and likely traces to aquatic ancestors pre-dating the divergence of the Crustacea and Hexapoda at least 420 million years ago.

85 citations


Journal ArticleDOI
TL;DR: The evo-devo concept of modularity concurs only at this macroevolutionary level with the quantitative notion of variational modularity and a combination of pleiotropic factors and more local developmental effects with a hierarchical, overlapping, and more or less continuous distribution appears most likely.
Abstract: Groups of correlated characters (variational modules) often are considered to be the result of dissociated local developmental factors, i.e., of a modular genotype–phenotype map. But certain sets of pleiotropic factors can equally well induce modular phenotypic variation—no local developmental factors are necessary for a modular covariance structure. It is thus not possible to infer genetic or developmental modularity from standing variation alone. Yet, only for approximately linear genotype–phenotype maps is the induced covariance structure stable over changes of the phenotypic mean. For larger genetic and phenotypic variation, such as on a macroevolutionary level, developmental effects often are nonlinear and variational modularity remains stable only when it is realized by local dissociated developmental factors with no overlap of pleiotropic ranges. The evo-devo concept of modularity concurs only at this macroevolutionary level with the quantitative notion of variational modularity. Empirical evidence on the genetic and developmental architecture underlying phenotypic variation is inconclusive and partly subject to methodological problems. Many studies seem to indicate modularized phenotypic variation and local clusters of QTL effects, whereas other studies find support for several alternative models of modularity and report continuous distributions of QTL effects. This inconsistency partly results from the neglect of spatial relationships among the measured traits. Given the complex development of higher organisms, a combination of pleiotropic factors and more local developmental effects with a hierarchical, overlapping, and more or less continuous distribution appears most likely.

83 citations


Journal ArticleDOI
TL;DR: The results support the hypothesis of mosaic evolution and suggest a modular nature of basicranial development, which may underlie the mosaic evolution of the hominin basicranium.
Abstract: Mosaic evolution describes different rates of evolutionary change in different body units. Morphologically these units are described by more relationships within a unit than between different units which relates mosaic evolution with morphological integration and modularity. Recent evidence suggests mosaic evolution at the human basicranium due to different evolutionary rates of midline and lateral cranial base morphology but this hypothesis has not yet been addressed explicitly. We this hypothesis and explore how mosaic evolution relates to modular development. Evolutionary data sets on midline (N = 186) and lateral (N = 86) basicranial morphology are compared with 3D data on pre- and postnatal basicranial ontogeny (N = 71). Our results support the hypothesis of mosaic evolution and suggest a modular nature of basicranial development. Different embryological basicranial units likely became differently modified during evolution, with relatively stable midline elements and more variable lateral elements. In addition, developmental data suggests that modularity patterns change throughout ontogeny. During prenatal ontogeny lateral basicranial elements (greater sphenoid wings and petrosal pyramids) change together compared with the midline base. Close to birth the greater sphenoid wings keep a spatially stable position, while the petrosal pyramids become dissociated and shifted posteriorly. After birth the greater sphenoid wings and petrosal pyramids change again jointly and with respect to midline cranial base elements. This sequential pattern of integration and modularization and re-integration describes human basicranial ontogeny in a way that is potentially important for the understanding of evolutionary change. Phylogenetic modifications of this pattern during morphogenesis, growth, and development may underlie the mosaic evolution of the hominin basicranium.

70 citations


Journal ArticleDOI
TL;DR: This work identifies patterns of genetic correlations that provide insight to the genetic architecture of the baboon dentition and hypothesizes a common pattern of genetic integration across the dental arcade in the Cercopithecoidea.
Abstract: Variation in the mammalian dentition is highly informative of adaptations and evolutionary relationships, and consequently has been the focus of considerable research. Much of the current research exploring the genetic underpinnings of dental variation can trace its roots to Olson and Miller’s 1958 book Morphological Integration. These authors explored patterns of correlation in the post-canine dentitions of the owl monkey and Hyopsodus, an extinct condylarth from the Eocene. Their results were difficult to interpret, as was even noted by the authors, due to a lack of genetic information through which to view the patterns of correlation. Following in the spirit of Olson and Miller’s research, we present a quantitative genetic analysis of dental variation in a pedigreed population of baboons. We identify patterns of genetic correlations that provide insight to the genetic architecture of the baboon dentition. This genetic architecture indicates the presence of at least three modules: an incisor module that is genetically independent of the post-canine dentition, and a premolar module that demonstrates incomplete pleiotropy with the molar module. We then compare this matrix of genetic correlations to matrices of phenotypic correlations between the same measurements made on museum specimens of another baboon subspecies and the Southeast Asian colobine Presbytis. We observe moderate significant correlations between the matrices from these three primate taxa. From these observations we infer similarity in modularity and hypothesize a common pattern of genetic integration across the dental arcade in the Cercopithecoidea.

Journal ArticleDOI
TL;DR: A view of evolutionary radiations driven fundamentally by external abiotic factors—geology and climate—that cause range expansion and opportunities for geographic isolation with resultant rapid speciation is presented.
Abstract: Evolutionary radiations, times of profound diversification of species against a broader background of more muted evolutionary change, have long been considered one of the fundamental patterns in the fossil record. Further, given the important role geological, environmental, and climatic processes play in causing speciation, analyzing the biogeographic context of radiations can yield important insight into their evolutionary mechanisms. In this study we examine biogeographic patterns and quantify rates of speciation in a diverse group of Devonian trilobites, the calmoniids, that has been hailed as a classic paleontological example of an evolutionary radiation. In particular, a phylogenetic biogeographic analysis—modified Brooks Parsimony Analysis—was used to examine the processes and geographic setting of speciation within the group. Results indicate that the Malvinokaffric Realm was a geographically complex area, and this geographic complexity created various opportunities for speciation via geodispersal and vicariance that created the fuel that fed the speciation in these taxa. Part of the geographic complexity was created not only by the inherent geologic backdrop of the region, but the overlying changes of sea level rise and fall. Rates of speciation were highest when sea level was lowest. Low sea level encouraged isolation of faunas in different tectonic basins. By contrast, sea level rise facilitated range expansion and geodispersal to other distinct tectonic basins, and speciation rates concomitantly fell; however, the taxa with the expanded ranges were later fodder for diversification when sea level fell again. Here we present a view of evolutionary radiations driven fundamentally by external abiotic factors—geology and climate—that cause range expansion and opportunities for geographic isolation with resultant rapid speciation.

Journal ArticleDOI
TL;DR: It is argued that the treatment of transformational and taxic homologies, respectively, as dynamic and static aspects of the same homeostatic property cluster kind represents a good perspective for supporting the conceptualization of taxa as kinds.
Abstract: Taxa and homologues can in our view be construed both as kinds and as individuals. However, the conceptualization of taxa as natural kinds in the sense of homeostatic property cluster kinds has been criticized by some systematists, as it seems that even such kinds cannot evolve due to their being homeostatic. We reply by arguing that the treatment of transformational and taxic homologies, respectively, as dynamic and static aspects of the same homeostatic property cluster kind represents a good perspective for supporting the conceptualization of taxa as kinds. The focus on a phenomenon of homology based on causal processes (e.g., connectivity, activity-function, genetics, inheritance, and modularity) and implying relationship with modification yields a notion of natural kinds conforming to the phylogenetic-evolutionary framework. Nevertheless, homeostatic property cluster kinds in taxonomic and evolutionary practice must be rooted in the primacy of epistemological classification (homology as observational properties) over metaphysical generalization (series of transformation and common ancestry as unobservational processes). The perspective of individuating characters exclusively by historical-transformational independence instead of their developmental, structural, and functional independence fails to yield a sufficient practical interplay between theory and observation. Purely ontological and ostensional perspectives in evolution and phylogeny (e.g., an ideographic character concept and PhyloCode’s ‘individualism’ of clades) may be pragmatically contested in the case of urgent issues in biodiversity research, conservation, and systematics.

Journal ArticleDOI
TL;DR: Anderson (2008) argues that the LH is mainly supported by loss char-acters, and that this is problematic ‘’given the relative easethat these losses can arise via paedomorphosis, which appears to evolve repeatedly’’, and emphasizes develop-ment characters such as digit development and skull ossi-fication order, which are known to be homoplastic.
Abstract: Anderson(2008)recentlyreviewedthecontroversialtopicofextant amphibian origins, on which three (groups of)hypotheses exist at the moment. Anderson favors the‘‘polyphyly hypothesis’’ (PH), which considers the extantamphibians to be polyphyletic with respect to many Paleo-zoic limbed vertebrates and was most recently supported bythe analysis of Anderson et al. (2008). Another is the‘‘temnospondyl hypothesis’’ (TH—lissamphibians nestedwithintemnospondyls),mostrecentlysupportedbyRutaandCoates (2007). We prefer the ‘‘lepospondyl hypothesis’’(LH—lissamphibians nested within ‘‘lepospondyls’’; mostrecently supported by Vallin and Laurin 2004 and Marja-novic´ and Laurin 2008a). We would like to clarify importantpoints that were not discussed in Anderson’s review, or forwhich crucial arguments were left out.Anderson (2008) argues that most molecular dates favorthe PH because they suggest a Devonian or Early Car-boniferous diversification of Lissamphibia. This is inac-curate, since the confidence intervals of the dates obtainedby Hugall et al. (2007) range from Early Carboniferous toMiddle Permian, and our own molecular dating suggests aPermian origin. Indeed, three methods (molecular dating, apaleontological supertree and a confidence interval on thestratigraphic range of Lissamphibia) all hint at a Permian or(less likely) a Late Carboniferous origin of Lissamphibia(Marjanovic´ and Laurin 2007, 2008b).Citing Schoch and Milner (2004), Anderson (2008,p.234) argues that the LH is mainly supported by loss char-acters, and that this is problematic ‘‘given the relative easethat these losses can arise via paedomorphosis, whichappears to evolve repeatedly.’’ This is especially surprisingbecause we count (Supplementary Table 1) about fifty losscharacters in the matrix by Anderson et al. (2008)—morethan one out of five characters—, including several thatdescribethelossofbones thatossified lateintheontogenyofbranchiosaurids (Schoch 1992) and/or the ai¨stopod Phlege-thontia (Anderson 2002) and are absent in lissamphibians.Furthermore, Anderson’s remark amounts to criticizingthe use of loss characters simply because they could behomoplastic. Yet, Anderson (2008) emphasizes develop-ment characters such as digit development and skull ossi-fication order, which are known to be homoplastic. Forinstance, under Anderson’s version of the PH, the similaritybetween the digit development orders of the branchiosauridtemnospondyl Apateon and the urodeles is either conver-gent, or homologous between these two taxa but reversed inanurans; indeed, Johanson et al. (2007) suggest that thedigits of tetrapods are homologous to the ‘‘radials’’ of othersarcopterygians and find the ‘‘radials’’ of the Australianlungfish to develop independently of the rest of the forelimb(pectoral fin), like in urodeles and Apateon (and unlike inanurans and amniotes, where the limb chondrifies in a strictproximal-to-distal sequence), strongly suggesting that theurodele-Apateon pattern is plesiomorphic—regardless ofwhether the PH, the TH, or the LH is (closest to) correct.Anderson (2008, p. 242) furthermore mentions that ‘‘thepattern of cranial ossification […] has compared very clo-sely with the sequence of cranial ossification seen in sala-manders’’ (making explicit on the next page that these

Journal ArticleDOI
TL;DR: It is found that patterns of integration are broadly similar for baboon and mouse mandibles, with both species displaying a modular pattern of integration.
Abstract: In this study we compare patterns of mandibular integration between mice and baboons using both phenotypic and quantitative genetic data. Specifically, we test how well each species fits with the mosaic model of mandibular integration suggested by Atchley and Hall (Biol Rev Camb Philos Soc 66:101–157, 1991) based on developmental modules. We hypothesize that patterns of integration will be similar for mice and baboons and that both species will show strong integration within developmental modules and weaker integration between modules. Corresponding landmark data were collected from the hemi-mandibles of an advanced intercross mouse sample (N = 1239) and mandibles from a baboon sample of known pedigree from the Southwest Foundation for Biomedical Research (N = 430). We used four methods of analysis to quantify and compare the degree of mandibular integration between species including two methods based on a priori assumptions, and two a posteriori analyses. We found that patterns of integration are broadly similar for baboon and mouse mandibles, with both species displaying a modular pattern of integration. While there is a general trend of similarity in integration patterns between species, there were some marked differences. Mice are strongly correlated among distances within the coronoid process and the incisive alveolar region, whereas baboons are strongly integrated within the condylar process. We discuss the potential evolutionary implications of the similar patterns of integration between these species with an emphasis on the role of modularity.

Journal ArticleDOI
TL;DR: Examples using covariation patterns estimated from modern humans and African great apes are provided to demonstrate the extent to which divergence in covariance structure might affect the authors' interpretations of hominin diversity.
Abstract: The fossil record of primate and human evolution cannot provide accurate estimates of within species variation and integration. This means that we cannot directly observe how patterns of integration have evolved over time in this lineage. And yet, our interpretations of fossil diversity are awash with assumptions about variation patterning in precisely these fossil taxa. Most commonly, researchers rely on extant models of variation for interpreting past diversity, by assuming equality of variation (and occasionally covariation) among extant and fossil populations. Yet one of the things we know from studies of integration in primates is that patterns of morphological covariation can differ among even closely related taxa, indicating that they have diverged over evolutionary time, either in response to selection or as the result of neutral evolution. At the same time, overall patterns of integration remain remarkably similar, meaning that in many respects they are highly conserved evolutionarily. Taken together, these seemingly contradictory observations offer an important conceptual framework for interpreting patterns that we observe in the fossil past. This framework dictates that while we can use patterns of covariation in extant taxa as proxies for extinct diversity, and indeed their conserved nature makes them superior to approaches that rely on variation alone, we also need to account for the fact that such patterns change over time, and incorporate that into our models. Here I provide examples using covariation patterns estimated from modern humans and African great apes to demonstrate the extent to which divergence in covariance structure might affect our interpretations of hominin diversity.

Journal ArticleDOI
TL;DR: The results indicate that putative developmental constraints help to preserve some aspects of normal morphological integration even in the deformed skulls and find that the response to selection in neurocranial globularity is pervasive, indicating that departures from normal patterns of neuroc Cranial Globularity are genetically constrained.
Abstract: Neurocranial globularity is one of the few derived traits defining anatomically modern humans. Variations in this trait derive from multiple and complex interactions between portions of the brain and the size and shape of the cranial base, among other factors. Given their evolutionary and functional importance, neurocranial globularity is expected to present high genetic and developmental constraints on their phenotypic expression. Here we applied two independent approaches to investigate both types of constraints. First, we assessed if patterns of morphological integration are conserved or else disrupted on a series of artificially deformed skulls in comparison to non-deformed (ND) ones. Second, after the estimation of the genetic covariance matrix for human skull shape, we explored how neurocranial globularity would respond to putative selective events disrupting the normal morphological patterns. Simulations on these deviations were explicitly set to replicate the artificial deformation patterns in order to compare developmental and genetic constraints under the same biomechanical conditions. In general terms, our results indicate that putative developmental constraints help to preserve some aspects of normal morphological integration even in the deformed skulls. Moreover, we find that the response to selection in neurocranial globularity is pervasive. In other words, induced changes in the vault generate a global response, indicating that departures from normal patterns of neurocranial globularity are genetically constrained. In summary, our combined results suggest that neurocranial globularity behaves as a highly genetic and developmental constrained trait.

Journal ArticleDOI
TL;DR: It is argued that the vagility of taxa should be explicitly incorporated in biogeographic analyses, and likelihood-based methods with models in which more realistic probabilities of dispersal and modes of speciation can be specified are arguably the way ahead.
Abstract: The conceptual gap between ecological and historical biogeography is wide, although both disciplines are concerned with explaining how distributions have been shaped. A central aim of modern historical biogeography is to use a phylogenetic framework to reconstruct the geographic history of a group in terms of dispersals and vicariant events, and a number of analytical methods have been developed to do so. To date the most popular analytical methods in historical biogeography have been parsimony-based. Such methods can be classified into two groups based on the assumptions used. The first group assumes that vicariance between two areas creates common patterns of disjunct distributions across several taxa whereas dispersals and extinctions generate clade specific patterns. The second group of methods assumes that passive vicariance and within-area speciation have a higher probability of occurrence than active dispersal events and extinction. Typically, none of these methods takes into account the ecology of the taxa in question. I discuss why these methods can be potentially misleading if the ecology of the taxon is ignored. In particular, the vagility or dispersal ability of taxa plays a pivotal role in shaping the distributions and modes of speciation. I argue that the vagility of taxa should be explicitly incorporated in biogeographic analyses. Likelihood-based methods with models in which more realistic probabilities of dispersal and modes of speciation can be specified are arguably the way ahead. Although objective quantification will pose a challenge, the complete ignorance of this vital aspect, as has been done in many historical biogeographic analyses, can be dangerous. I use worked examples to show a simple way of utilizing such information, but better methods need to be developed to more effectively use ecological knowledge in historical biogeography.

Journal ArticleDOI
TL;DR: Simulations show that adoption of superimposition procedures that incorporate biological assumptions about the nature of size and of the variation in shape can dramatically improve the ability to infer the pattern of variation in geometric morphometric data.
Abstract: The form of an organism is the combination of its size and its shape. For a sample of forms, biologists wish to characterize both mean form and the variation in form. For geometric data, where form is characterized as the spatial locations of homologous points, the first step in analysis superimposes the forms, which requires an assumption about what measure of size is appropriate. Geometric morphometrics adopts centroid size as the natural measure of size, and assumes that variation around the mean form is isometric with size. These assumptions limit the interpretation of the resulting estimates of mean and variance in form. We illustrate these problems using allometric variation in shape. We show that superimposition based on subsets of relatively isometric points can yield superior inferences about the overall pattern of variation. We propose and demonstrate two superimposition techniques based on this idea. In subset superimposition, landmarks are progressively discarded from the data used for superimposition if they result in significant decreases in the variation among the remaining landmarks. In outline superimposition, regularly distributed pseudolandmarks on the continuous outline of a form are used as the basis for superimposition of the landmarks contained within it. Simulations show that these techniques can result in dramatic improvements in the accuracy of estimated variance-covariance matrices among landmarks when our assumptions are roughly satisfied. The pattern of variation inferred by means of our superimposition techniques can be quite different from that recovered from full generalized Procrustes superimposition. The pattern of shape variation in the wings of drosophilid flies appears to meet these assumptions. Adoption of superimposition procedures that incorporate biological assumptions about the nature of size and of the variation in shape can dramatically improve the ability to infer the pattern of variation in geometric morphometric data.

Journal ArticleDOI
TL;DR: It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene.
Abstract: A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.

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TL;DR: There is a clear tendency for pleiotropic effects of QTL to be localized but that the localization may be best thought of as occurring in a continuous space rather being clustered in discrete modules.
Abstract: Theories of phenotypic integration have relied heavily on the concept of modularity in order to model the ways in which traits in an organism correlate and covary. Recent investigations suggest that, while some functional and developmental processes may be morphologically and ontogenetically localized, and thus modular in a developmental sense, there is a great deal of overlap among these influences on patterns of integration in the adult form. This can result in blurry boundaries between hypothesized modules constructed to test hypotheses about phenotypic integration. This investigation tests hypotheses about the contribution of pleiotropic quantitative trait loci (QTL) to phenotypic integration in the mouse mandible without using a priori categorical hypotheses about which traits constitute a module. We ask two main questions: (1) Are the effects of pleiotropic QTL localized to highly correlated traits or more spread out among traits than one might expect by chance? (2) Does the pattern of trait influence when all pleiotropic QTL are considered together deviate from what we might expect if QTL affect traits without regard for the correlations among traits? We find that a large proportion of pleiotropic QTL affect traits that are more highly correlated than we expect by chance with the remainder having effects that are distributed as if by chance. Furthermore, the overall distribution of the effects of pleiotropic QTL differs significantly from the null distribution of no association between pleiotropic effects on traits and correlations among traits. The main modular hypothesis used by earlier studies often does not predict the distribution of sets of traits sharing a common QTL. These results suggest that there is a clear tendency for pleiotropic effects of QTL to be localized but that the localization may be best thought of as occurring in a continuous space rather being clustered in discrete modules.

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TL;DR: Sexual selection in eastern tiger salamanders was roughly equal between sexes, and the role of body size on reproductive success was not correlated with mating or reproductive success in either sex.
Abstract: Variation in reproductive success is most pronounced in species with strongly biased operational sex ratios, prominent sexual dimorphisms, and where mate competition and choice are likely. We studied sexual selection in eastern tiger salamanders (Ambystoma t. tigrinum) and examined the role of body size on reproductive success. We genotyped 155 adults and 1,341 larvae from 90 egg masses at six microsatellite loci. Parentage analyses revealed both sexes engaged in multiple matings, but was more common among females (64%) than males (27%). However, the standardized variance in mating and reproductive success was higher in males. Bateman gradients were significant and nearly identical in both sexes, suggesting that sexual selection was roughly equal between sexes. Body size was not correlated with mating or reproductive success in either sex. The apparent lack of sexual selection on body size may be a result of sperm storage, sperm competition, alternative mating tactics, and/or random induction of spermatophores.

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TL;DR: If selection can indeed affect the stability of G to facilitate evolution, the overall structure of G might not be as important to consider as the past selective conditions that G was subject to.
Abstract: The genetic variance-covariance matrix (G) has long been considered to summarize the genetic constraints biasing evolution in its early stages, although in some instances, G can enhance divergence and facilitate adaptation. However, the effects of G on the response to selection might be of less importance than previously thought. In addition, it has been suggested that selection itself, under certain conditions, might rapidly alter the genetic covariance structure. If selection can indeed affect the stability of G to facilitate evolution, the overall structure of G might not be as important to consider as the past selective conditions that G was subject to. Thus, more empirical work is needed on the stability of G in the early stages of divergence before one can really assess to what extent G constrains evolution.

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TL;DR: The articles published in this issue of Evolutionary Biology were originally presented in a symposium entitled ‘‘Patterns and Processes of Morphological Integration in Primate and Human Evolution’’, held at the 77th annual meeting of the American Association of Physical Anthropologists in Columbus, Ohio, in April 2008.
Abstract: The articles published in this issue of Evolutionary Biology were originally presented in a symposium entitled ‘‘Patterns and Processes of Morphological Integration in Primate and Human Evolution’’, held at the 77th annual meeting of the American Association of Physical Anthropologists in Columbus, Ohio, in April 2008. The symposium marked the 50th anniversary of Everett Olson and Robert Miller’s seminal book ‘‘Morphological Integration’’, and sought to capture the current state of affairs in studies of morphological integration, particularly in relation to primate and human evolutionary biology. In its simplest form, morphological integration is the inter-dependence between sets of traits within an individual, reflecting a common influence from functional and/or developmental factors. The concept of integration is not a new one. In fact, the Principle of the Correlation of Parts, the idea that in order to be viable, organisms must be comprised of organs that are functionally coordinated with each other, was a major theme in the work of French anatomist Georges Cuvier (1769–1832, see Mayr 1982:460). Perhaps not surprisingly, Charles Darwin also discussed this ubiquitous feature of complex organisms in the Origin of Species under the term ‘‘Correlation of Growth’’: ‘‘I mean by this expression that the whole organization is so tied together during its growth and development, that when slight variations in one part occur, and are accumulated through natural selection, other parts become modified’’ (On the Origin of Species, 1859: 147). Thus, whereas Cuvier’s work emphasized the influence of shared functions on covariation and correlation among traits, Darwin recognized that interactions between these structures during ontogeny could also bias the production of variation within and among traits, and understood the consequences of such a bias on the evolution of complex organisms. Olson and Miller synthesized these earlier views, suggesting that both developmental and functional interactions were important sources of correlation among parts, each contributing towards building ‘integrated’ organisms in which different parts function in harmony with all others. The process by which such holistic phenotypes are built is what Olson and Miller called morphological integration, i.e., ‘‘the summation of the totality of characters which, in their interdependency of form, produce an organism’’ (1958, p. v). Olson and Miller were also aware of the importance of integration—as a variational property of populations—for the capacity of organismal traits to evolve independently of one another. Olson and Miller also deserve credit for providing the first quantitative methods, mostly based on statistical correlation, for empirically identifying groups of phenotypic traits that are more strongly integrated on the basis of shared developmental and/or functional factors (q-groups). Despite this important insight into a fundamental emergent property of organisms, Olson and Miller’s theory of integration did not immediately gain traction among evolutionary biologists. Reasons for this might be that their approach was pattern-based, relying heavily on statistical rather than biological criteria for grouping sets of correlated traits, and inferring in a post-hoc manner developmental and functional reasons for increased correlation among C. Rolian (&) Department of Cell Biology and Anatomy, University of Calgary, G503-3330 Hospital Dr NW, Calgary, AB T2N 4N1, USA e-mail: cprolian@ucalgary.ca

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TL;DR: There is evidence for moderate dissociation of hind limb evolution in some lineages, while tail length has evolved effectively independently of the substantial alterations to the lengths of the body and limbs, indicating a significant role of evolutionary and developmental modularity in the divergence of body form within Lerista.
Abstract: The scincid lizard clade Lerista provides an exceptional model for studying the mode of substantial evolutionary transformations, comprising more than 90 species displaying a remarkable variety of body forms. Patterns of character evolution in this clade, inferred from reconstructed ancestral states, are at least partly consistent with the correlated progression model of macroevolutionary change. At each stage in the transition to a highly elongate, limb-reduced body plan, alterations to the lengths of the forelimb and hind limb are accompanied by compensatory changes in snout-vent length (or vice versa), preserving locomotory ability. Nonetheless, there is evidence for moderate dissociation of hind limb evolution in some lineages, while tail length has evolved effectively independently of the substantial alterations to the lengths of the body and limbs. This indicates a significant role of evolutionary and developmental modularity in the divergence of body form within Lerista, and emphasises the potential variability of the strength of functional constraints within organisms and among lineages. Trends toward a highly elongate, functionally limbless body plan may be attributed primarily to a combination of the interdependence of changes in snout-vent length and limb lengths and the very low probability of re-elaborating structurally reduced limbs. Similar asymmetries in the probabilities of interrelated phenotypic changes may be a significant cause of evolutionary trends resulting in the emergence of higher taxa.

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TL;DR: Investigations into disrupted epigenetic processes are required to further test hypotheses about how canalization or integration of limb variation is affected by epigenetic factors, because whereas baseline levels of postnatal activity may help to maintain patterns of variance and integration, increased levels of activity do not further increase these measures.
Abstract: Mammals exhibit a similar pattern of integration among homologous limb elements, the strength of which is believed to vary in response to selection for functional coordination or similarity. Although integration is hypothesized to primarily reflect the effect of genes intrinsic to limbs, extrinsic genetic or epigenetic factors may also affect the strength of integration through their impact on the magnitude and direction of skeletal variance or covariance. Such factors as neuromuscular coordination or bone-muscle interactions may therefore play a role in both canalization and the structure or magnitude of limb integration. If this were the case, then increased levels of locomotor activity would be predicted to increase canalization and the magnitude of covariation between limbs. To investigate whether postnatal activity levels can have a significant effect on variance within or covariance among homologous limb elements, we compared four groups of male mice from a long-term selective breeding experiment: (1) mice from lines bred for increased voluntary activity on running wheels and allowed free access to a wheel for 8 weeks beginning at weaning (“active”), (2) selected mice that did not have wheel access (“sedentary”), (3) active mice from non-selected control lines, and (4) sedentary control mice. Mice from selected lines that had wheel access ran significantly more than control-line mice. However, when controlled for activity, linetype, and body mass, results indicate few significant differences in means, variance, or covariation structure, and no significant differences in integration between limbs, suggesting that postnatal activity levels do not significantly affect canalization or integration of limb lengths. A possible explanation for this result is that whereas baseline levels of postnatal activity may help to maintain patterns of variance and integration, increased levels of activity do not further increase these measures. Investigations into disrupted epigenetic processes (e.g., via models in which neuromuscular coordination is impaired) are required to further test hypotheses about how canalization or integration of limb variation is affected by epigenetic factors.

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TL;DR: This procedure aims to evaluate the robustness of biogeographical hypotheses as scientific theories, which are reliable descriptions of how life changes its form both in space and time, putting historical biogeography close to Croizat's statement of evolution as a three dimensional phenomenon.
Abstract: Biogeography deals with the combined analysis of the spatial and temporal components of the evolutionary process. To this purpose, biogeographical analysis should consider two extra steps: a reciprocal illumination step, and a consilience step. Even if the traditional challenges of biogeography were successfully handled, the obtained hypothesis is not necessarily meaningful in biogeographical terms––it needs continuous test in the light of external hypotheses. For this reason, a concept analogous to Hennig’s reciprocal illumination is valuable, as well as a sort of biogeographical consilience in Whewell’s sense. Firstly, through the search for different classes of evidence, information useful to improve the hypothesis can be accessed via reciprocal illumination. Following, a more general hypothesis would arise through a consilience process, when the hypothesis explains phenomena not contemplated during its construction, as the distribution of other taxa or the existence (or absence) of fossils. This procedure aims to evaluate the robustness of biogeographical hypotheses as scientific theories. Such theories are reliable descriptions of how life changes its form both in space and time, putting historical biogeography close to Croizat’s statement of evolution as a three dimensional phenomenon.

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TL;DR: This study focuses on the morphology of the dorsal epithelium and internal structure of the tongue of the Leopard Gecko, Eublepharis macularius, emphasizing the foretongue and its relation to fluid uptake.
Abstract: Detailed descriptions of tongue morphology of members of Squamata that refer to functional implications other than food processing are rare. Herein we focus on the morphology of the dorsal epithelium and internal structure of the tongue of the Leopard Gecko, Eublepharis macularius, emphasizing the foretongue and its relation to fluid uptake. We employ both scanning electron microscopy and serial histology to examine the morphology of the entire tongue, its component regions, and its situation in the oral chamber. We recognize five distinct morphological regions of the dorsal tongue surface, each of which is distinctive both morphologically and histologically. The foretongue bears papillae quite different in structure and spacing from those of all other tongue regions, and these non-glandular structures are involved in gathering and transporting fluid from the environment. Fluid unloaded from the foretongue in the region of the vomeronasal sinus is channeled through the network of cuboidal papillae and directed towards a pair of compartments lateral to the tongue in which fluid pools during a drinking bout. This allows the dorsal surface of the mid- and hind-tongue, which are involved in food processing and manipulation, to be largely segregated from the pathway of fluid flow. We relate our findings to descriptions of the tongue of other taxa, and propose functional hypotheses for the observed morphology. This study provides new anatomical information upon which future studies of the functional morphology of the buccal apparatus in the Gekkota can be based.

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TL;DR: The results indicate that P might not only reflect ancestral developmental pathways but might also be influenced by current ecology, and this finding suggests that divergent selection on wing patch length might have affected the stability of P.
Abstract: Comparing species differences in covariance patterns of traits subject to divergent selection pressures can increase our understanding to the mechanisms of phenotypic divergence. Different species of calopterygid damselflies have diverged in the melanized wing patch of males. This trait serves multiple ecological functions and has behavioral consequences in terms of sexual selection, interspecific interactions, reproductive isolation. We compared the phenotypic variance-covariance matrices (P) of wing traits among nine populations of four European species of calopterygid damselflies. We found modest divergence in covariance structure among populations of the same species, but strong divergence between species. Interestingly, the orientation of the first eigenvector of P (P (max) ) differed more between closely related species than between distantly related species, although this pattern was absent when overall covariance structures were compared. We also found that distantly related species but geographically closer had converged towards a similar covariance structure. Finally, divergence in covariance structure was correlated with divergence in wing patch length, but not with other wing traits. This last finding suggests that divergent selection on wing patch length might have affected the stability of P. These results indicate that P might not only reflect ancestral developmental pathways but might also be influenced by current ecology.

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TL;DR: This study shows that the powerful formalism of network theory can be applied to the discovery of modules in complex phenotypes and opens the possibility of an integrated approach to the study of modularity at all levels of organizational complexity.
Abstract: The notion of modularity has become a unifying principle to understand structural and functional aspects of biological organization at different levels of complexity. Recently, deciphering the modular organization of molecular systems has been greatly aided by network theory. Nevertheless, network theory is completely absent from the investigation of modularity of complex macroscopic phenotypes, a fundamental level of organization at which organisms experience and interact with the environment. Here, we used geometric descriptors of phenotypic variation to derive a network representation of a complex morphological structure, the mammalian mandible, in terms of nodes and links. Then, by integrating the network representation and description with random matrix theory, we uncovered a modular organization for the mammalian mandible, which deviates significantly from an equivalent random network. The modules revealed by the network analysis correspond to the four morphogenetic units recognized for the mammalian mandible on a developmental basis. Furthermore, these modules are known to be affected only by particular genes and are also functionally differentiated. This study shows that the powerful formalism of network theory can be applied to the discovery of modules in complex phenotypes and opens the possibility of an integrated approach to the study of modularity at all levels of organizational complexity.