Morphological integration in the carnivoran skull

The correlated evolution of traits may be a principal factor in morphological evolution, but it is typically studied in genetic or developmental systems. Most studies examining phenotypic trait correlations, through analysis of morphological integration, consider only few taxa, with limited ability to test hypotheses of the influence of trait integration on morphological variation and diversity. The few comparative studies in less inclusive groups have yielded varying relationships of integration to the key factors of phylogeny and diet. In this paper, I present analyses of cranial morphological integration in 30 species from the mammalian order Carnivora, spanning eight extant families and a wide range of ecological and morphological diversity. Fifty-five cranial landmarks were captured through three-dimensional digitization of 15-22 specimens for each species. Using a node-based phylogenetic distance matrix, a significant correlation was found between similarity in patterns of integration and phylogenetic relatedness within Felidae (cats) and Canidae (dogs), but not within more inclusive clades, when size-related variation was removed. When size was included, significant correlations were found across all Caniformia, Musteloidea, Mustelidae, and Felidae. There was a significant correlation between phylogeny and morphological integration only within the higher-level clade Feliformia (cats, civets, mongooses, and hyaenas) when a branch-length-based phylogenetic distance matrix was analyzed, with and without size. In contrast, diet was significantly correlated with similarity in morphological integration in arctoid carnivorans (bears, raccoons, and weasels), but had no significant relationship with integration in feliforms or canids. These results support the proposition that evolutionary history is correlated with cranial integration across large clades, although in some smaller clades diet also exerts significant influence on the correlated evolution of traits.     

Phylogeny, diet, and cranial integration in australodelphian marsupials

Studies of morphological integration provide valuable information on the correlated evolution of traits and its relationship to long-term patterns of morphological evolution. Thus far, studies of morphological integration in mammals have focused on placentals and have demonstrated that similarity in integration is broadly correlated with phylogenetic distance and dietary similarity. Detailed studies have also demonstrated a significant correlation between developmental relationships among structures and adult morphological integration. However, these studies have not yet been applied to marsupial taxa, which differ greatly from placentals in reproductive strategy and cranial development and could provide the diversity necessary to assess the relationships among phylogeny, ecology, development, and cranial integration. This study presents analyses of morphological integration in 20 species of australodelphian marsupials, and shows that phylogeny is significantly correlated with similarity of morphological integration in most clades. Size-related correlations have a significant affect on results, particularly in Peramelia, which shows a striking decrease in similarity of integration among species when size is removed. Diet is not significantly correlated with similarity of integration in any marsupial clade. These results show that marsupials differ markedly from placental mammals in the relationships of cranial integration, phylogeny, and diet, which may be related to the accelerated development of the masticatory apparatus in marsupials.     

A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys

Similarity of genetic and phenotypic variation patterns among populations is important for making quantitative inferences about past evolutionary forces acting to differentiate populations and for evaluating the evolution of relationships among traits in response to new functional and developmental relationships. Here, phenotypic co variance and correlation structure is compared among Platyrrhine Neotropical primates. Comparisons range from among species within a genus to the superfamily level. Matrix correlation followed by Mantel's test and vector correlation among responses to random natural selection vectors (random skewers) were used to compare correlation and variance/covariance matrices of 39 skull traits. Sampling errors involved in matrix estimates were taken into account in comparisons using matrix repeatability to set upper limits for each pairwise comparison. Results indicate that covariance structure is not strictly constant but that the amount of variance pattern divergence observed among taxa is generally low and not associated with taxonomic distance. Specific instances of divergence are identified. There is no correlation between the amount of divergence in covariance patterns among the 16 genera and their phylogenetic distance derived from a conjoint analysis of four already published nuclear gene datasets. In contrast, there is a significant correlation between phylogenetic distance and morphological distance (Mahalanobis distance among genus centroids). This result indicates that while the phenotypic means were evolving during the last 30 millions years of New World monkey evolution, phenotypic covariance structures of Neotropical primate skulls have remained relatively consistent. Neotropical primates can be divided into four major groups based on their feeding habits (fruit-leaves, seed-fruits, insect-fruits, and gum-insect-fruits). Differences in phenotypic covariance structure are correlated with differences in feeding habits, indicating that to some extent changes in interrelationships among skull traits are associated with changes in feeding habits. Finally, common patterns and levels of morphological integration are found among Platyrrhine primates, suggesting that functional/developmental integration could be one major factor keeping covariance structure relatively stable during evolutionary diversification of South American monkeys.     

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.     

Patterns of phenotypic covariation and correlation in modern humans as viewed from morphological integration

Proportionality of phenotypic and genetic distance is of crucial importance to adequately focus on population history and structure, and it depends on the proportionality of genetic and phenotypic covariance. Constancy of phenotypic covariances is unlikely without constancy of genetic covariation if the latter is a substantial component of the former. If phenotypic patterns are found to be relatively stable, the most probable explanation is that genetic covariance matrices are also stable. Factors like morphological integration account for such stability. Morphological integration can be studied by analyzing the relationships among morphological traits. We present here a comparison of phenotypic correlation and covariance structure among worldwide human populations. Correlation and covariance matrices between 47 cranial traits were obtained for 28 populations, and compared with design matrices representing functional and developmental constraints. Among-population differences in patterns of correlation and covariation were tested for association with matrices of genetic distances (obtained after an examination of 10 Alu-insertions) and with Mahalanobis distances (computed after craniometrical traits). All matrix correlations were estimated by means of Mantel tests. Results indicate that correlation and covariance structure in our species is stable, and that among-group correlation/covariance similarity is not related to genetic or phenotypic distance. Conversely, genetic and morphological distance matrices were highly correlated. Correlation and covariation patterns were largely associated with functional and developmental factors, which probably account for the stability of covariance patterns.     

A comparative study of morphological integration in Apis mellifera (Insecta, Hymenoptera)

Morphometric correlation matrices from 11 Mediterranean and European honey bee races have been compared. The degree of integration, measured by the eigenvalue variance of the correlation matrix or by Cheverud's index of integration, varies considerably between races but covaries neither with overall body size nor with the variance of the respective sample. Hence, the degree of morphological integration does not depend on body size or the level of variability The patterns of morphometric correlation are significantly similar among all races, but some minor differences in the patterns could be detected: The similarity between the correlation matrices is independent of the degree of phylogenetic relatedness between the respective races. In all races characters belonin to the same functional and/or developmental unit (leg, wing, abdominal characters) have Eiter correlations than the average. Most of the variation in the pattern of correlation can be expfained as a side effect of variation in the degree of integration. Races with high levels of integration tend to have hiher correlations between the main groups of characters, and races with low levels of integration tave smaller correlations between the main grous of characters, while the basic pattern remains undisturbed. In summary, the comparative analysis of morphometric correlation matrices reveals a picture of stability with respect to the pattern of integration and of variation in the degree of integration, which is random with respect to body size, degree of variability, and phylogeny.     

Building Developmental Integration into Functional Systems: Function-Induced Integration of Mandibular Shape

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.     

Functional equivalence of morphologies enables morphological and ecological diversity

Diversity in organismal forms among taxa is thought to reflect distinct selection pressures across environments. The central assumption underlying this expectation is that taxa experiencing similar selection have similar response to that selection. However, because selection acts on trait function, taxa similarity in selection response depends crucially on the relationship between function and morphology. Further, when a trait consists of multiple parts, changes in function in response to selection can result from modification of different parts, and adaptation to the same environment might result in functional but not morphological similarity. Here, we address the extent to which functional and morphological diversity in masticatory apparatus of soricid shrews reflects a shared ecological characteristic of their diet type. We examine the factors limiting morphological variation across shrew species by assessing the relative contribution of trait function (biomechanics of the jaw), ecology, and phylogeny to species similarity in mandibular traits. We found that species that shared diet type were functionally but not morphologically similar. The presence of multiple semi-independently varying traits enabled functional equivalence of composite foraging morphologies and resulted in variable response to selection exerted by similar diet. We show that functional equivalence of multiple morphologies enabled persistence of differences in habitat use (e.g., habitat moisture and coverage) among species that specialize on the same diet. We discuss the importance of developmental and functional integration among traits for evolutionary diversification of morphological structures that generate equivalent functions.     

Phylogenetic analysis of correlation structure in stalk-eyed flies (Diasemopsis,Diopsidae)

Morphological divergence among species may be constrained by the pattern of genetic variances and covariances among traits within species. Assessing the existence of such a relationship in nature requires information on the stability of intraspecific correlation and covariance structure and the correspondence of this structure to the pattern of evolutionary divergence within a lineage. Here, we investigate these issues for nine morphological traits and 15 species of stalk-eyed flies in the genus Diasemopsis. Within-species matrices for these traits were generated from phenotypic data for all the Diasemopsis species and from genetic data for a single Diasemopsis species, D. dubia. The among-species pattern of divergence was assessed by calculating the evolutionary correlations for all pairwise combinations of the morphological traits along the phylogeny of these species. Comparisons of intraspecific matrices reveal significant similarity among all species in the phenotypic correlations matrices but not the covariance matrices. In addition, the differences in correlation structure that do exist among species are not related to their phylogenetic placement or change in the means of the traits. Comparisons of the phenotypic and phylogenetic matrices suggest a strong relationship between the pattern of evolutionary change among species and both the intraspecific correlation structure and the stability of this structure among species. The phenotypic and the phylogenetic matrices are significantly similar, and pairs of traits whose intraspecific correlations are more stable across taxa exhibit stronger coevolution on the phylogeny. These results suggest either the existence of strong constraints on the pattern of evolutionary change or a consistent pattern of correlated selection shaping both the phenotypic and phylogenetic matrices. The genetic correlation structure for D. dubia, however, does not correspond with patterns found in the phenotypic and phylogenetic data. Possible reasons for this disagreement are discussed.     

Role of development in the evolution of the scapula of the giant sthenurine kangaroos (Macropodidae: Sthenurinae)

Extinct giant sthenurine kangaroos possessed scapulae morphologically distinct from those of all other extant and extinct adult macropodids, but qualitatively resembling those of newborn macropodids. The similarity between adult sthenurine and neonatal macropodid scapulae suggests that a developmental process, such as heterochrony, might have been behind the evolution of the unique sthenurine scapular morphology. By incorporating adult and ontogenetic data, this study examines the evolution and development of the sthenurine scapula. This study quantitatively upholds the previous qualitative morphological observations of macropodid scapulae and finds that ontogenetic and evolutionary morphological changes are correlated in macropodids. The similarity of scapula morphology in sthenurines and newborn macropodids, the correlation between ontogenetic and evolutionary morphological change, and information from other sources (i.e., sthenurine evolutionary history) suggests that pedomorphic shifts in morphology, most likely due to neotenic processes, occurred within the development of the scapula of giant sthenurines.     

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.     

Quantitative Comparison of Ontogenetic and Phylogenetic Character Changes in the Synapsid Mandible and Auditory Region

The dual transformations of the post-dentary bones into sound conducting elements of the basicranium in synapsid evolutionary and developmental histories are quantitatively compared using a modified version of a previously published methodology. Sensitivity analyses were performed to test the effects of using different phylogenies and statistics. The relative sequences of discrete osteological character transformations of the mandible and auditory region compared between the ontogeny of Monodelphis domestica. the gray short-tailed opossum, and two phylogenetic hypotheses for synapsids are statistically correlated using two different tests (Spearman's R correlation and Kendall's Tau). Presumably, the characters examined in this study form a functionally integrated morphological unit that is distinct throughout evolutionary and developmental history. Assuming a von Baerian developmental pattern, the methodology discussed here could potentially be used as a test of similarity between phylogenetic hypotheses; however, further work needs to be done to test this potential.     

Morphological integration and serial homology: A case study of the cranium and anterior vertebrae in salamanders

Serial homology or the repetition of equivalent developmental units and their derivatives is a phenomenon encountered in a variety of organisms, with the vertebrate axial skeleton as one of the most notable examples. Serially homologous structures can be viewed as an appropriate model system for studying morphological integration and modularity, due to the strong impact of development on their covariation. Here, we explored the pattern of morphological integration of the cranium and the first three serially homologous structures (atlas, first, and second trunk vertebrae) in salamandrid salamanders, using micro-CT scanning and three-dimensional geometric morphometrics. We explored the integration between structures at static and evolutionary levels. Effects of allometry on patterns of modularity were also taken into account. At the static level (within species), we analyzed inter-individual variation in shape to detect functional modules and intra-individual variation to detect developmental modules. Significant integration (based on inter-individual variation) among all structures was detected and allometry is shown to be an important integrating factor. The pattern of intra-individual, asymmetric variation indicates statistically significant developmental integration between the cranium and the atlas and between the first two trunk vertebrae. At the evolutionary level (among species), the cranium, atlas, and trunk vertebrae separate as different modules. Our results show that morphological integration at the evolutionary level coincides with morphological and functional differentiation of the axial skeleton, allowing the more or less independent evolutionary changes of the cranial skeleton and the vertebral column, regardless of the relatively strong integration at the static level. The observed patterns of morphological integration differ across levels, indicating different impacts of developmental and phylogenetic constraints and functional demands.     

Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves

The structure of compound leaves provides flexibility for morphological change by variation in the shapes, sizes and arrangement of leaflets. Here, we conduct a multilevel analysis of shape variation in compound leaves to explore the developmental plasticity and evolutionary potential that are the basis of diversification in leaf shape. We use the methods of geometric morphometrics to study the shapes of individual leaflets and whole leaves in 20 taxa of Potentilla (sensu lato). A newly developed test based on the bootstrap approach suggests that uncertainty in the molecular phylogeny precludes firm conclusions whether there is a phylogenetic signal in the data on leaf shape. For variation among taxa, variation within taxa, as well as fluctuating asymmetry, there is evidence of strong morphological integration. The patterns of variation are similar across all three levels, suggesting that integration within taxa may act as a constraint on evolutionary change.     

Evolutionary persistence of phenotypic integration: influence of developmental and functional relationships on complex trait evolution

Examination of historical persistence of integration patterns provides an important insight into understanding the origin and evolution of complex traits. Specifically, the distinct effects of developmental and functional integration on the evolution of complex traits are often overlooked. Because patterns of functional integration are commonly shaped by selection exerted by the external environment, whereas patterns of developmental integration can be determined by relatively environment-independent selection for developmental homeostasis, examination of historical persistence of morphological integration patterns among species should reveal the relative importance of current selection in the evolution of complex traits. We compared historical persistence of integration patterns produced by current developmental versus ecological requirements by examining the evolution of complex mandibular structures in nine species of soricid shrews. We found that, irrespective of phylogenetic relatedness of species, patterns of developmental and functional integration were highly concordant, suggesting that strong selection for developmental homeostasis favors concordant channeling of both internal and external variation. Overall, our results suggest that divergence in mandible shape among species closely follows variation in functional demands and ecological requirements regardless of phylogenetic relatedness among species.     

Pectoral girdle and forelimb variation in extant Crocodylia: the coracoid–humerus pair as an evolutionary module

To date, all statements about evolutionary morphological transformation in Crocodylia have essentially been based on qualitative observations. In the present study, we assessed the morphological variation and covariation (integration) between the scapula, coracoid, humerus, radius, and ulna of 15 species of Crocodylidae, Alligatoridae, and Gavialis + Tomistoma using three‐dimensional geometric morphometrics. The results obtained reveal that the variation of elements within species (intraspecific) is large. However, despite this variability, variation across species (interspecific) is mainly concentrated in two dimensions where the disparity is constrained: ‘robusticity’ and ‘twist’ (forelimbs) and ‘robusticity’ and ‘flexion’ (pectoral girdle). Robusticity (first dimension of variation) embodies a set of correlated geometrical features such as the broadening of the girdle heads and blades, or the enlargement of proximal and distal bone ends. The twist is related to the proximal and/or distal epiphyses in the forelimb elements, and flexion of the scapula and coracoid blades comprises the second dimension of variation. In all crocodylians, forelimb integration is characterized by the strong correlations of a humerus–ulna–radius triad and by a radius–ulna pair, thus forming a tight forelimb module. Unexpectedly, we found that the humerus and coracoid form the most integrated pair, whereas the scapula is a more variable and relatively independent element. The integration pattern of the humerus–coracoid pair distinguishes a relatively robust configuration in alligatorids from that of the remainder groups. The patterns of variation and integration shared by all the analyzed species have been interpreted as an inherited factor, suggesting that developmental and functional requirements would have interacted in the acquisition of a semi‐aquatic and versatile locomotion at the Crocodylia node at least 65 Mya. Our findings highlight the need to incorporate the humerus–coracoid pair in biodynamic and biomechanical studies. © 2012 The Linnean Society of London     

Morphological variation and covariation in mandibular molars of platyrrhine primates

Molars are highly integrated biological structures that have been used for inferring evolutionary relationships among taxa. However, parallel and convergent morphological traits can be affected by developmental and functional constraints. Here, we analyze molar shapes of platyrrhines in order to explore if platyrrhine molar diversity reflects homogeneous patterns of molar variation and covariation. We digitized 30 landmarks on mandibular first and second molars of 418 extant and 11 fossil platyrrhine specimens to determine the degree of integration of both molars when treated as a single module. We combined morphological and phylogenetic data to investigate the phylogenetic signal and to visualize the history of molar shape changes. All platyrrhine taxa show a common shape pattern suggesting that a relatively low degree of phenotypic variation is caused by convergent evolution, although molar shape carries significant phylogenetic signal. Atelidae and Pitheciidae show high levels of integration with low variation between the two molars, whereas the Cebinae/Saimiriinae, and especially Callitrichinae, show greater variation between molars and trend toward a modular organization. We hypothesize that biomechanical constraints of the masticatory apparatus, and the dietary profile of each taxon are the main factors that determine high covariation in molars. In contrast, low molar shape covariation may result from the fact that each molar exhibits a distinct ecological signal, as molars can be exposed to distinct occlusal loadings during food processing, suggesting that different selective pressures on molars can reduce overall molar integration.     

The "eyespot module" and eyespots as modules: development, evolution, and integration of a complex phenotype

Organisms are inherently modular, yet modules also evolve in response to selection for functional integration or functional specialization of traits. For serially repeated homologous traits, there is a clear expectation that selection on the function of individual traits will reduce the integration between traits and subdivide a single ancestral module. The eyespots on butterfly wings are one example of serially repeated morphological traits that share a common developmental mechanism but are subject to natural and sexual selection for divergent functions. Here, I test two hypotheses about the organization of the eyespot pattern into independent dorsal-ventral and anterior-posterior modules, using a graphical modeling technique to examine patterns of eyespot covariation among and within wing surfaces in the butterfly Bicyclus anynana. Although there is a hierarchical and complex pattern of integration among eyespots, the results show a surprising mismatch between patterns of eyespot integration and the developmental and evolutionary eyespot units identified in previous empirical studies. These results are discussed in light of the relationships between developmental, functional, and evolutionary modules, and they suggest that developmental sources of independent trait variation are often masked by developmental sources of trait integration.     

Mosaic heterochrony and evolutionary modularity: the trilobite genus Zacanthopsis as a case study

Logical connections exist between evolutionary modularity and heterochrony, two unifying and structuring themes in the expanding field of evolutionary developmental biology. The former sees complex phenotypes as being made up of semi-independent units of evolutionary transformation; the latter requires such a modular organization of phenotypes to occur in a localized or mosaic fashion. This conceptual relationship is illustrated here by analyzing the evolutionary changes in the cranidial ontogeny of two related species of Cambrian trilobites. With arguments from comparative developmental genetics and functional morphology, we delineate putative evolutionary modules within the cranidium and examine patterns of evolutionary changes in ontogeny at both global and local scales. Results support a case of mosaic heterochrony, that is, a combination of local heterochronies affecting the different parts individuated in the cranidium, leading to the complex pattern of allometric repatterning observed at the global scale. Through this example, we show that recasting morphological analyses of complex phenotypes with a priori knowledge or hypotheses about their organizational and variational properties can significantly improve our interpretation and understanding of evolutionary changes among related taxa, fossil and extant. Such considerations open avenues to investigate the large-scale dynamics of modularity and its role in phenotypic evolution.