A Comparison of Phenotypic Variation and Covariation Patterns and the Role of Phylogeny, Ecology, and Ontogeny During Cranial Evolution of New World Monkeys

Abstract

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.

Patterns of phenotypic correlations among morphological traits across plants and animals

“…These very broad trait groups do not show evidence of modularity as we defined it in the Introduction, because the within-group correlations are not on average greater than the among-group correlations (figure 3). However, modularity of mammal skull traits has often been discussed [10,11], so the within-head correlations could be lowest because they include lower inter-module correlations. Therefore, despite the lack of modularity in the broad categories used in figure 3, part of the reason that vertebrates have lower correlations than invertebrates could be modularity within the head.…”

“…One potential lack of independence in the invertebrate data is mentioned in Results. The New World monkey skull study by Marroig & Cheverud [10] included 39 traits for 40 species, so this one dataset contained almost 30 000 correlations. To avoid the database being numerically overwhelmed by this one study, we included the 40 species mean correlations, that is, the average of the 741 pairwise correlations among the 39 traits for each species.…”

Patterns of morphological integration in marine modular organisms: supra-module organization in branching octocoral colonies

“…Morphological integration in animals has been explained as a result of functional interactions during development (Zelditch 1988) and ecological adaptations (e.g. Marroig & Cheverud 2001), both of which generate a phenotype that evolves as an integrated entity (e.g. Gould 1977).…”

“…An important question in the study of phenotypic evolution is whether characters are independent of each other or behave and evolve as integrated modules or systems (Pigliucci 2002). Correlations among morphological traits across species depict patterns of integration during the evolutionary process (Olson & Miller 1958;Cheverud 1996;Marroig & Cheverud 2001). Such integration can be the product of common inheritance due to pleiotropy or linkage disequilibrium, or the result of the concerted evolution of morphological elements that operate together to perform a specific function (Cheverud 1996).…”

Genetic architecture of wing morphology in Drosophila simulans and an analysis of temperature effects on genetic parameter estimates

“…The maximum observable correlation between two matrices was then estimated by O(t 1 t 2 ), where t 1 and t 2 are the repeatabilities of the correlation matrices (Cheverud, 1995(Cheverud, , 1996. Therefore, we could evaluate the observed correlation between two matrices given by Mantel's test relative to their maximum observable correlation rather than relative to one (Cheverud, 1996;Marroig and Cheverud, 2001). Nevertheless, the maximum observable correlation between genetic and phenotypic matrices must take into account both sampling error and part-whole relationships because these matrices are not independent from each other.…”