Evolution and Development of Diversity: An Example in Foraging Morphology of Soricid Shrews

Divergent natural selection for use of locally abundant resources can lead to diversification within and across species. However, the consequences of divergent selection for phenotypic evolution also depend on the development of variation. Because relationships among traits such as shared developmental timing or common involvement in an organismal function can channel variation generated during development, these relationships strongly influence the direction of evolution.During development of the mammalian mandible multiple tissues of distinct developmental origins interact with inputs from the functioning of attached muscles to produce a cohesive and well integrated trait. In soricid shrews, part of the mandible matures late in ontogeny, coinciding with the onset of foraging. In this case, foraging-linked muscle activity should influence the development of the late maturing mandibular region. Here, I show that variation in this late ossifying region reveals the local functional requirements of the jaw and results in an opportunity to decouple internal and external sources of variation (developmental and environmental respectively) in the mandible. Capitalizing on this feature of the Sorex system, I empirically examined the historical persistence of internal and external patterns of variation, the consequences of variation patterning for ecological and morphological diversification across taxa, and differences between early and late ossifying regions in their contribution to local adaptation in mandible morphology.I found that the functional requirements of diet directed mandible development and determined species similarity in both mandible morphology and function. Timing of bone maturation determined the morphological effects of foraging-linked muscle activity, resulting in differential expression of adaptive variation in the late maturing region. Further, I found higher levels of interspecific variation in the late maturing region of the mandible, and showed that interspecific divergence in foraging morphology occurs along the lines delineated by epigenetic inputs of muscle on bone formation during late ontogeny within species. These findings indicate that differences in functional requirements are critical for divergence among taxa in this system. Further, these results suggest that, when external inputs into trait development are indicative of local functional requirements, the same epigenetic mechanism of development can generate diversity both within and among taxa