Mosaic Evolution of the Skull in Labrid Fishes Involves Differences in Both Tempo and Mode of Morphological Change

Abstract

Modularity is a ubiquitous feature of organismal design that plays an important role in structuring patterns of morphological diversification. Modularity can facilitate evolutionary changes by allowing subsets of traits to coevolve as integrated units and follow quasi-independent evolutionary trajectories, a pattern that may be particularly consequential in the case of highly complex morphological structures. Here we examine modularity in a complex and highly kinetic structure, the teleost skull, and ask if a modular organization of the skull has influenced the diversification dynamics of the shapes of its osteological components across the labrid phylogeny. We compiled one of the largest 3D morphological data sets of fishes to date and used geometric morphometrics to quantify patterns of cranial shape evolution across 184 species of wrasses (Labridae). We then tested several hypotheses of modularity inspired by functional and developmental relationships between cranial bones and compared phenotypic rates among modules. We also compared the fit of models of trait evolution for the entire skull and the various articulated bones that it comprises. Our analyses indicated strong support for a 2-module hypothesis, one that encompasses the oral and pharyngeal jaws and another module comprised of the neurocranium, hyoid apparatus, and operculum. This functional hypothesis yielded one of the highest significant rate differentials across modules, yet we also found that the best-fitting models of trait evolution differed among skull bones. These results suggest that modularity can influence morphological diversification in complex biological structures via differences in both the tempo and mode of evolutionary change. [3D geometric morphometrics, cranial morphology, evolutionary modularity, Labridae, phenotypic rates, structural complexity.].