Evolution of ontogeny: linking epigenetic remodeling and genetic adaptation in skeletal structures

Evolutionary diversifications are commonly attributed to thecontinued modifications of a conserved genetic toolkit of developmentalpathways, such that complexity and convergence in organismalforms are assumed to be due to similarity in genetic mechanismsor environmental conditions. This approach, however, confoundsthe causes of organismal development with the causes of organismaldifferences and, as such, has only limited utility for addressingthe cause of evolutionary change. Molecular mechanisms thatare closely involved in both developmental response to environmentalsignals and major evolutionary innovations and diversificationsare uniquely suited to bridge this gap by connecting explicitlythe causes of within-generation variation with the causes ofdivergence of taxa. Developmental pathways of bone formationand a common role for bone morphogenetic proteins (BMPs) inboth epigenetic bone remodeling and the evolution of major adaptivediversifications provide such opportunity. We show that variationin timing of ossification can result in similar phenotypic patternsthrough epigenetically induced changes in gene expression andpropose that both genetic accommodation of environmentally induceddevelopmental pathways and flexibility in development acrossenvironments evolve through heterochronic shifts in bone maturationrelative to exposure to unpredictable environments. We suggestthat such heterochronic shifts in ossification can not onlybuffer development under fluctuating environments while maintainingepigenetic sensitivity critical for normal skeletal formation,but also enable epigenetically induced gene expression to generatespecialized morphological adaptations. We review studies ofenvironmental sensitivity of BMP pathways and their regulationof formation, remodeling, and repair of cartilage and bone toexamine the hypothesis that BMP-mediated skeletal adaptationsare facilitated by evolved reactivity of BMPs to external signals.Surprisingly, no empirical study to date has identified themolecular mechanism behind developmental plasticity in skeletaltraits. We outline a conceptual framework for future studiesthat focus on mediation of phenotypic plasticity in skeletaldevelopment by the patterns of BMP expression.