ADAPTIVE RADIATIONS,ECOLOGICAL SPECIALIZATION,AND THE EVOLUTIONARY INTEGRATION OF COMPLEX MORPHOLOGICAL STRUCTURES

The evolutionary integration of complex morphological structures is a macroevolutionary pattern in which morphogenetic components evolve in a coordinated fashion, which can result from the interplay among processes of developmental, genetic integration, and different types of selection. We tested hypotheses of ecological versus developmental factors underlying patterns of within‐species and evolutionary integration in the mandible of phyllostomid bats, during the most impressive ecological and morphological radiation among mammals. Shape variation of mandibular morphogenetic components was associated with diet, and the transition of integration patterns from developmental to within‐species to evolutionary was examined. Within‐species (as a proxy to genetic) integration in different lineages resembled developmental integration regardless of diet specialization, however, evolutionary integration patterns reflected selection in different mandibular components. For dietary specializations requiring extensive functional changes in mastication patterns or biting, such as frugivores and sanguivores, the evolutionary integration pattern was not associated with expected within‐species or developmental integration. On the other hand, specializations with lower mastication demands or without major functional reorganization (such as nectarivores and carnivores), presented evolutionary integration patterns similar to the expected developmental pattern. These results show that evolutionary integration patterns are largely a result of independent selection on specific components regardless of developmental modules.     

Cranial evolution in sakis (Pithecia, Platyrrhini). II: Evolutionary processes and morphological integration

Patterns of interspecific differentiation in saki monkeys (Pithecia) are quantitatively described and possible evolutionary processes producing them are examined. The comparison of species correlation matrices to expected patterns of morphological integration reveal significant and similar patterns of development-based cranial integration among species. Aspects of the facial region are more heavily influenced by general size variation than features of the neural region. The comparison of pooled within- and between-groups V/CV matrices suggests that genetic drift might be a sufficient explanation for saki cranial evolution. Differential natural selection gradients are also reconstructed because selection may also have caused population differentiation through evolutionary time. These gradients illustrate the inherent multivariate nature of selection, being a consequence of the interaction between existing morphological integration (correlation) among traits and the action of natural selection. Yet, our attempt to interpret selection gradients in terms of their functional significance did not result in any clear association between selection and function. Perhaps this is also an indication that morphological evolution in sakis was mostly neutral.     

The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure

Abstract Patterns of genetic variation and covariation strongly affect the rate and direction of evolutionary change by limiting the amount and form of genetic variation available to natural selection. We studied evolution of morphological variance-covariance structure among seven populations of house finches (Carpodacus mexicanus) with a known phylogenetic history. We examined the relationship between within- and among-population covariance structure and, in particular, tested the concordance between hierarchical changes in morphological variance-covariance structure and phylogenetic history of this species. We found that among-population morphological divergence in either males or females did not follow the within-population covariance patterns. Hierarchical patterns of similarity in morphological covariance matrices were not congruent with a priori defined historical pattern of population divergence. Both of these results point to the lack of proportionality in morphological covariance structure of finch populations, suggesting that random drift alone is unlikely to account for observed divergence. Furthermore, drift alone cannot explain the sex differences in within- and among-population covariance patterns or sex-specific patterns of evolution of covariance structure. Our results suggest that extensive among-population variation in sexual dimorphism in morphological covariance structure was produced by population differences in local selection pressures acting on each sex.     

Ecological and evolutionary factors in the morphological diversification of South American spiny rats

Understanding the processes underlying morphological diversification is a central goal in ecology and evolutionary biology and requires the integration of information about phylogenetic divergence and ecological niche diversity. In the present study, we use geometric morphometrics and comparative methods to investigate morphological diversification in Neotropical spiny rats of the family Echimyidae. Morphological diversification is studied as shape variation in the skull, comprising a structure composed of four distinct units: vault, base, orognathofacial complex, and mandible. We demonstrate association among patterns of variation in shape in different cranial units, levels of phylogenetic divergence, and ecological niche diversification. At the lower level of phylogenetic divergence, there is significant and positive concordance between patterns of phylogenetic divergence and cranial shape variation in all cranial units. This concordance may be attributable to the phylogenetic and shape distances being calculated between species that occupy the same niche. At higher phylogenetic levels of divergence and with ecological niche diversity, there is significant concordance between shape variation in all four cranial units and the ecological niches. In particular, the orognathofacial complex revealed the most significant association between shape variation and ecological niche diversity. This association may be explained by the great functional importance of the orognathofacial complex.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 646–660.     

Characterizing the evolution of genetic variance using genetic covariance tensors

Determining how genetic variance changes under selection in natural populations has proved to be a very resilient problem in evolutionary genetics. In the same way that understanding the availability of genetic variance within populations requires the simultaneous consideration of genetic variance in sets of functionally related traits, determining how genetic variance changes under selection in natural populations will require ascertaining how genetic variance–covariance (G) matrices evolve. Here, we develop a geometric framework using higher-order tensors, which enables the empirical characterization of how G matrices have diverged among populations. We then show how divergence among populations in genetic covariance structure can then be associated with divergence in selection acting on those traits using key equations from evolutionary theory. Using estimates of G matrices of eight male sexually selected traits from nine geographical populations of Drosophila serrata, we show that much of the divergence in genetic variance occurred in a single trait combination, a conclusion that could not have been reached by examining variation among the individual elements of the nine G matrices. Divergence in G was primarily in the direction of the major axes of genetic variance within populations, suggesting that genetic drift may be a major cause of divergence in genetic variance among these populations.     

Metabolic Rate and Climatic Fluctuations Shape Continental Wide Pattern of Genetic Divergence and Biodiversity in Fishes

Taxonomically exhaustive and continent wide patterns of genetic divergence within and between species have rarely been described and the underlying evolutionary causes shaping biodiversity distribution remain contentious. Here, we show that geographic patterns of intraspecific and interspecific genetic divergence among nearly all of the North American freshwater fish species (>750 species) support a dual role involving both the late Pliocene-Pleistocene climatic fluctuations and metabolic rate in determining latitudinal gradients of genetic divergence and very likely influencing speciation rates. Results indicate that the recurrent glacial cycles caused global reduction in intraspecific diversity, interspecific genetic divergence, and species richness at higher latitudes. At the opposite, longer geographic isolation, higher metabolic rate increasing substitution rate and possibly the rapid accumulation of genetic incompatibilities, led to an increasing biodiversity towards lower latitudes. This indicates that both intrinsic and extrinsic factors similarly affect micro and macro evolutionary processes shaping global patterns of biodiversity distribution. These results also indicate that factors favouring allopatric speciation are the main drivers underlying the diversification of North American freshwater fishes.     

Morphological evolution in the mandible of spiny rats, genus Trinomys (Rodentia: Echimyidae)

The development and evolution of the rodent mandible have been studied in depth in recent years. The mandible is a complex structure because it consists of six morphogenetic components formed by different condensations of mesenchymal cells. Using recent techniques for the geometric analysis of shape, we have combined developmental information with a powerful quantification of shape variation and an independent estimate of phylogeny (molecular data) to assess the evolutionary patterns of shape change in mandibles of the rodent genus Trinomys . In general, the major trends in shape variation did not agree with the expected phylogenetic pattern. However, for small-scale morphological differences, one species ( T. yonenagae ) was responsible for the lack of association between morphology and molecular divergence. This species is genetically similar to but morphologically different from other Trinomys . The coronoid process was considered to be the most conservative morphogenetic component in the mandible.     

Location-specific sympatric morphological divergence as a possible response to species interactions in West Virginia Plethodon salamander communities

1. The competitive interactions of closely related species have long been considered important determinants of community composition and a major cause of phenotypic diversification. However, while patterns such as character displacement are well documented, less is known about how local adaptation influences diversifying selection from interspecific competition. 2. We examined body size and head shape variation among allopatric and sympatric populations of two salamander species, the widespread Plethodon cinereus and the geographically restricted P. nettingi. We quantified morphology from 724 individuals from 20 geographical localities throughout the range of P. nettingi. 3. Plethodon nettingi was more robust in cranial morphology relative to P. cinereus, and sympatric localities were more robust relative to allopatric localities. Additionally, there was significantly greater sympatric head shape divergence between species relative to allopatric communities, and sympatric localities of P. cinereus exhibited greater morphological variation than sympatric P. nettingi. 4. The sympatric morphological divergence and increase in cranial robustness of one species (P. nettingi) were similar to observations in other Plethodon communities, and were consistent with the hypothesis of interspecific competition. These findings suggest that interspecific competition in Plethodon may play an important role in phenotypic diversification in this group. 5. The increase in among-population variance in sympatric P. cinereus suggests a species-specific response to divergent natural selection that is influenced in part by other factors. We hypothesize that enhanced morphological flexibility and ecological tolerance allow P. cinereus to more rapidly adapt to local environmental conditions, and initial differences among populations have allowed the evolutionary response of P. cinereus to vary across replicate sympatric locations, resulting in distinct evolutionary trajectories of morphological change.     

Relationships among ontogenetic,static, and evolutionary allometry

The relationship between ontogenetic, static, and evolutionary levels of allometry is investigated. Extrapolation from relative size relationships in adults to relative growth in ontogeny depends on the variability of slopes and intercepts of ontogenetic vectors relative to variability in length of the vector. If variability in slopes and intercepts is low relative to variability in length, ontogenetic and static allometries will be similar. The similarity of ontogenetic and static allometries was tested by comparing the first principal component, or size vector, for correlations among 48 cranial traits in a cross-sectional ontogenetic sample of rhesus macaques from Cayo Santiago with a static sample from which all age- and sex-related variation had been removed. The vector correlation between the components is high but significantly less than one while two of three allometric patterns apparent in the ontogenetic component are not discernable in the static component. This indicates that there are important differences in size and shape relationships among adults and within ontogenies. Extrapolation from intra- or interspecific phenotypic allometry to evolutionary allometry is shown to depend on the similarity of genetic and phenotypic allometry patterns. Similarity of patterns was tested by comparing the first principal components of the phenotypic, genetic, and environmental correlation matrices calculated using standard quantitative genetic methods. The patterns of phenotypic, genetic, and environmental allometry are dissimilar; only the environmental allometries show ontogenetic allometric patterns. This indicates that phenotypic allometry may not be an accurate guide to patterns of evolutionary change in size and shape.     

Linking movement behaviour to dispersal and divergence in plethodontid salamanders

To better understand the evolutionary and ecological effects of dispersal, there is growing emphasis on the need to integrate direct data on movement behaviour into landscape-scale analyses. However, little is known about the general link between movement behaviour and large-scale patterns of dispersal and gene flow. Likewise, although recent studies suggest that nonrandom, directionally biased movement and dispersal can promote evolutionary divergence, the generality of this mechanism is unknown. We test the hypothesis that directionally biased movement and dispersal by plethodontid salamanders interact with the topography of headwater areas to affect genetic and phenotypic divergence. Movements by Gyrinophilus porphyriticus and Eurycea bislineata show contrasting directional biases: upstream bias in G. porphyriticus and downstream bias in E. bislineata. Consistent with predictions of how these biases interact with slope to affect dispersal and gene flow, genetic distance increased with slope in G. porphyriticus and decreased with slope in E. bislineata over a standardized distance of 1 km along six headwater streams. In both species, phenotypic divergence in relative trunk length was positively related to genetic divergence. These results indicate that landscape-scale patterns of dispersal and gene flow are closely related to movement behaviour in G. porphyriticus and E. bislineata, and underscore the value of information on movement behaviour for predicting and interpreting patterns of dispersal and gene flow in complex landscapes. This study also provides new evidence that directionally biased movement and dispersal can be important sources of intra- and interspecific variation in population divergence, and highlights the value of explicit, a priori predictions in landscape genetic studies.     

Phylogeography and evolution of two closely related oak species (<Emphasis Type="Italic">Quercus</Emphasis>) from north and northeast China

Orographic and climatic influences during the Pleistocene have had a crucial role on interspecific divergence and population demography during speciation. However, associations between demographic histories of closely related species and related climatic events, especially in north and northeast China, are still underexplored. Genetic analyses with four chloroplast DNA and two nuclear genes and species distribution modeling were used for two closely related oak species (Quercus liaotungensis and Quercus mongolica) to test if their interspecific divergence and phylogeographical histories were possibly related to the Pleistocene-era climatic events. Potential divergence of the two oak species was estimated at about 0.92–2.15 Ma. Species distribution models and genetic data showed varying phylogeographical histories and spatial population structures between the two oaks, leading to different patterns of interspecific gene flow between the chloroplast and nuclear genes. The results indicate that speciation event between the two species is recent and may have been triggered by geological and climatic fluctuations linked to the upheavals of the Qinghai-Tibetan Plateau at the Pliocene/Pleistocene boundary. The two closely related oaks possess varying population demography during the interglacial-glacial climatic oscillations of the Quaternary, probably due to the various niche adaptations among different distribution ranges across their species trajectories.     

Multilevel assessment of the Lacertid lizard cranial modularity

Different factors and processes that produce phenotypic variation at the individual, population, or interspecific level can influence or alter the covariance structure among morphological traits. Therefore, studies of the patterns of integration and modularity at multiple levels—static, ontogenetic, and evolutionary, can provide invaluable data on underlying factors and processes that structured morphological variation, directed, or constrained evolutionary changes. Our dataset, consisting of cranium shape data for 14 lizard species from the family Lacertidae, with substantial samples of hatchlings and adults along with their inferred evolutionary relationships, enabled us to assess modularity and morphological integration at all three levels. Five, not mutually exclusive modularity hypotheses of lizard cranium, were tested, and the effects of allometry on intensity and the pattern of integration and modularity were estimated. We used geometric morphometrics to extract symmetric and asymmetric, as well as allometric and nonallometric, components of shape variation. At the static level, firm confirmation of cranial modularity was found for hypotheses which separate anterior and posterior functional compartments of the skull. At the ontogenetic level, two alternative hypotheses (the “anteroposterior” and “neurodermatocranial” hypotheses) of ventral cranial modularity were confirmed. At the evolutionary level, the “neurodermatocranial” hypothesis was confirmed for the ventral cranium, which is in accordance with the pattern observed at the ontogenetic level. The observed pattern of static modularity could be driven by functional demands and can be regarded as adaptive. Ontogenetic modularity and evolutionary modularity show the same developmental origin, indicating conservatism of modularity patterns driven by developmental constraints.     

Evidence for morphological and adaptive genetic divergence between lake and stream habitats in European minnows (Phoxinus phoxinus, Cyprinidae)

Natural selection drives local adaptation, potentially even at small temporal and spatial scales. As a result, adaptive genetic and phenotypic divergence can occur among populations living in different habitats. We investigated patterns of differentiation between contrasting lake and stream habitats in the cyprinid fish European minnow (Phoxinus phoxinus) at both the morphological and genomic levels using geometric morphometrics and AFLP markers, respectively. We also used a spatial correlative approach to identify AFLP loci associated with environmental variables representing potential selective forces responsible for adaptation to divergent habitats. Our results identified different morphologies between lakes and streams, with lake fish presenting a deeper body and caudal peduncle compared to stream fish. Body shape variation conformed to a priori predictions concerning biomechanics and swimming performance in lakes vs. streams. Moreover, morphological differentiation was found to be associated with several environmental variables, which could impose selection on body and caudal peduncle shape. We found adaptive genetic divergence between these contrasting habitats in the form of 'outlier' loci (2.9%) whose genetic divergence exceeded neutral expectations. We also detected additional loci (6.6%) not associated with habitat type (lake vs. stream), but contributing to genetic divergence between populations. Specific environmental variables related to trophic dynamics, landscape topography and geography were associated with several neutral and outlier loci. These results provide new insights into the morphological divergence and genetic basis of adaptation to differentiated habitats.     

Phylin 2.0: Extending the phylogeographical interpolation method to include uncertainty and user‐defined distance metrics

Estimating geographical ranges of intra‐specific evolutionary lineages is crucial to the fields of biogeography, evolution, and biodiversity conservation. Models of isolation mechanisms often consider multiple distances in order to explain genetic divergence. Yet, the available methods to estimate the geographical ranges of lineages are based on direct geographical distances, neglecting other distance metrics that can better explain the spatial genetic structure. We extended the phylogeographical interpolation method (phylin ) in order to accommodate user‐defined distance metrics and to incorporate the uncertainty associated with genetic distance calculation. These new features were tested with simulated and empirical data sets. Multiple distance matrices were generated including geographical, resistance, and environmental distances to derive maps of lineage occurrence. The new additions to this method improved the ability to predict lineage occurrence, even with low sample size. We used a regression framework to quantify the relationship between the genetic divergence and competing distance matrices representing potential isolation processes that are subsequently used in the interpolation process. Including uncertainty in tree topology and the different distance matrices improved the robustness of the variograms, allowing a better fit of the theoretical model of spatial dependence. The improvements to the method increase its potential application in other fields. Accurately mapping genetic divergence can help to locate potential contact zones between lineages as well as barriers to gene flow, which has a broad interest in biogeographical and evolutionary studies. Additionally, conservation efforts could benefit from the integration of genetic variation and landscape features in a spatially explicit framework.     

Assessing Trait Covariation and Morphological Integration on Phylogenies Using Evolutionary Covariance Matrices

Morphological integration describes the degree to which sets of organismal traits covary with one another. Morphological covariation may be evaluated at various levels of biological organization, but when characterizing such patterns across species at the macroevolutionary level, phylogeny must be taken into account. We outline an analytical procedure based on the evolutionary covariance matrix that allows species-level patterns of morphological integration among structures defined by sets of traits to be evaluated while accounting for the phylogenetic relationships among taxa, providing a flexible and robust complement to related phylogenetic independent contrasts based approaches. Using computer simulations under a Brownian motion model we show that statistical tests based on the approach display appropriate Type I error rates and high statistical power for detecting known levels of integration, and these trends remain consistent for simulations using different numbers of species, and for simulations that differ in the number of trait dimensions. Thus, our procedure provides a useful means of testing hypotheses of morphological integration in a phylogenetic context. We illustrate the utility of this approach by evaluating evolutionary patterns of morphological integration in head shape for a lineage of Plethodon salamanders, and find significant integration between cranial shape and mandible shape. Finally, computer code written in R for implementing the procedure is provided.     

Convergent evolution of phenotypic integration and its alignment with morphological diversification in Caribbean Anolis ecomorphs

The adaptive landscape and the G-matrix are keys concepts for understanding how quantitative characters evolve during adaptive radiation. In particular, whether the adaptive landscape can drive convergence of phenotypic integration (i.e., the pattern of phenotypic variation and covariation summarized in the P-matrix) is not well studied. We estimated and compared P for 19 morphological traits in eight species of Caribbean Anolis lizards, finding that similarity in P among species was not correlated with phylogenetic distance. However, greater similarity in P among ecologically similar Anolis species (i.e., the trunk-ground ecomorph) suggests the role of convergent natural selection. Despite this convergence and relatively deep phylogenetic divergence, a large portion of eigenstructure of P is retained among our eight focal species. We also analyzed P as an approximation of G to test for correspondence with the pattern of phenotypic divergence in 21 Caribbean Anolis species. These patterns of covariation were coincident, suggesting that either genetic constraint has influenced the pattern of among-species divergence or, alternatively, that the adaptive landscape has influenced both G and the pattern of phenotypic divergence among species. We provide evidence for convergent evolution of phenotypic integration for one class of Anolis ecomorph, revealing yet another important dimension of evolutionary convergence in this group.     

QUANTITATIVE GENETICS OF GEOMETRIC SHAPE IN THE MOUSE MANDIBLE

Abstract We combine the methods of geometric morphometrics and multivariate quantitative genetics to study the patterns of phenotypic and genetic variation of mandible shape in random‐bred mice. The data are the positions of 11 landmarks on the mandibles of 1241 mice from a parent‐offspring breeding design. We use Procrustes superimposition to extract shape variation and restricted maximum likelihood to estimate the additive genetic and environmental components of variance and covariance. Matrix permutation tests showed that the genetic and phenotypic as well as the genetic and environmental covariance matrices were similar, but not identical. Likewise, principal component analyses revealed correspondence in the patterns of phenotypic and genetic variation. Patterns revealed in these analyses also showed similarities to features previously found in the effects of quantitative trait loci and in the phenotypes generated in gene knockout experiments. We used the multivariate version of the breeder's equation to explore the potential for short‐term response to selection on shape. In general, the correlated response is substantial and regularly exceeds the direct response: Selection applied locally to one landmark usually produces a response in other parts of the mandible as well. Moreover, even selection for shifts of the same landmark in different directions can yield dramatically different responses. These results demonstrate the role of the geometry and anatomical structure of the mandible, which are key determinants of the patterns of the genetic and phenotypic covariance matrices, in molding the potential for adaptive evolution.     

Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota, Rodentia)

The phenotype is a product of its phylogenetic history and its recent adaptation to local environments, but the relative importance of the two factors is controversial. We assessed the effects of diet, habitat, elevation, temperature, precipitation, body size, and mtDNA genetic divergence on shape variation in skulls, mandibles, and molars, structures that differ in their genetic and functional control. We asked whether these structures have adapted to environment to the same extent and whether they retain the same amount of phylogenetic signal. We studied these traits in intra- and interspecific populations of Eurasian marmots whose last common ancestor lived 2-5 million years ago. Path Analysis revealed that body size explained 10% of variation in skulls, 7% in mandibles, and 15% in molars. Local vegetation explained 7% of variation in skulls, 11% in mandibles, and 12% in molars. Dietary category explained 25% of variation in skulls, 11% in mandibles, and 9% in molars. Cyt b mtDNA divergence (phylogeny) explained 15% of variation in skulls, 7% in mandibles, and 5% in molars. Despite the percentages of phylogenetic variance, maximum-likelihood trees based on molar and skull shape recovered most phylogenetic groupings correctly, but mandible shape did not. The good performance of molars and skulls was probably due to different factors. Skulls are genetically and functionally more complicated than teeth, and they had more mathematically independent components of variation (5-6-in skulls compared to 3-in molars). The high proportion of diet-related variance was not enough to mask the phylogenetic signal. Molars had fewer independent components, but they also have less ecophenotypic variation and evolve more slowly, giving each component a proportionally stronger phylogenetic signal. Molars require larger samples for each operational taxonomic unit than the other structures because the proportion of within-taxon to between-taxon variation was higher. Good phylogenetic signal in quantitative skeletal morphology is likely to be found only when the taxa have a common ancestry no older than hundreds of thousands or millions of years (1% to 10% mtDNA divergence)--under these conditions skulls and molars provide stronger signal than mandibles.