The Influence of Modularity on Cranial Morphological Disparity in Carnivora and Primates (Mammalia)

Abstract

BackgroundAlthough variation provides the raw material for natural selection and evolution, few empirical data exist about the factors controlling morphological variation. Because developmental constraints on variation are expected to act by influencing trait correlations, studies of modularity offer promising approaches that quantify and summarize patterns of trait relationships. Modules, highly-correlated and semi-autonomous sets of traits, are observed at many levels of biological organization, from genes to colonies. The evolutionary significance of modularity is considerable, with potential effects including constraining the variation of individual traits, circumventing pleiotropy and canalization, and facilitating the transformation of functional structures. Despite these important consequences, there has been little empirical study of how modularity influences morphological evolution on a macroevolutionary scale. Here, we conduct the first morphometric analysis of modularity and disparity in two clades of placental mammals, Primates and Carnivora, and test if trait integration within modules constrains or facilitates morphological evolution.Principal FindingsWe used both randomization methods and direct comparisons of landmark variance to compare disparity in the six cranial modules identified in previous studies. The cranial base, a highly-integrated module, showed significantly low disparity in Primates and low landmark variance in both Primates and Carnivora. The vault, zygomatic-pterygoid and orbit modules, characterized by low trait integration, displayed significantly high disparity within Carnivora. 14 of 24 results from analyses of disparity show no significant relationship between module integration and morphological disparity. Of the ten significant or marginally significant results, eight support the hypothesis that integration within modules constrains morphological evolution in the placental skull. Only the molar module, a highly-integrated and functionally important module, showed significantly high disparity in Carnivora, in support of the facilitation hypothesis.ConclusionsThis analysis of within-module disparity suggested that strong integration of traits had little influence on morphological evolution over large time scales. However, where significant results were found, the primary effect of strong integration of traits was to constrain morphological variation. Thus, within Primates and Carnivora, there was some support for the hypothesis that integration of traits within cranial modules limits morphological evolution, presumably by limiting the variation of individual traits.

Genome of the Tasmanian tiger provides insights into the evolution and demography of an extinct marsupial carnivore

“…Taxon sampling was largely based on a previous study 6 , which itself was an expansion of the 3D cranial dataset assembled by Wroe & Milne 5 to examine morphological convergence in carnivorous eutherians (order Carnivora) and marsupials, including the thylacine (Thylacinus cynocephalus). The Carnivora is divided into two suborders, the Feliformia and Caniformia, which together comprise over 280 living species 44 . Among these are the well-known large-bodied carnivores such as lions, wolves and hyenas, but also omnivores (some bears), insectivores (aardwolf and bateared fox) and a diversity of small-to medium-sized mustelids, raccoons, civets, mongooses and others with varying ecologies.…”

Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications

“…Some authors have argued that modularity facilitates evolutionary change [418][419][420][421], a hypothesis that has been investigated with the methods of geometric morphometrics [172,[422][423][424]. Also, some authors have hypothesized that the patterns of genetic and developmental modularity should evolve to match the patterns of functional modularity [399,419,[425][426][427].…”

The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

“…Fewer studies have tried to directly estimate the relationship between integration and morphological variation or disparity in empirical datasets (16,64). Analyses of morphological disparity and integration have compared trait variances in strongly and weakly integrated traits across a few clades of mammals, suggesting that strong integration may constrain trait variation across taxa although its effect is relatively weak (64).…”

“…Analyses of morphological disparity and integration have compared trait variances in strongly and weakly integrated traits across a few clades of mammals, suggesting that strong integration may constrain trait variation across taxa although its effect is relatively weak (64). Interestingly, this weak effect on disparity may not translate simply to evolutionary rates because some of the most strongly integrated cranial traits showed limited disparity but high rates of evolution in an analysis across carnivorans (63).…”