Developmental plasticity links local adaptation and evolutionary diversification in foraging morphology

Abstract

Developmental plasticity is thought to reconcile the constraining role of natural selection in maintaining local adaptation with evolutionary diversification under novel conditions, but empirical documentations are rare. In vertebrates, growth and development of bones is partially guided by contractions of attached musculature and such muscle activity changes progressively through embryonic development from sporadic motility to direct functional effects. In species with short generation times, delayed skull maturation extends the guiding effects of muscle activity on formation of foraging morphology into adulthood, providing an opportunity to directly examine the links between plasticity of bone development, ecological adaptations, and evolutionary diversification in foraging morphology. In this case, the morphological consequences of inputs due to local functional requirements should be evident in adaptive divergence across taxa. Here we provide evidence that epigenetic regulation of bone growth in Soricid shrews may enable both development of local adaptations and evolutionary divergence in mandibular morphology. We contrast the effects of muscle stimulation on early- vs. late-maturing components of, foraging apparatus to show that the morphology of late-maturing components is more affected by functional requirements than are early-ossifying traits. Further, the divergence in foraging morphology across shrew species occurs along the directions delineated by inductive effects of muscle loading and bite force on bone formation in late-maturing but not early-maturing mandible components within species. These results support the hypothesis that developmental plasticity can link maintenance of local adaptations with evolutionary diversification in morphology.