Comparison of developmental genome expression in rodent molars reveals extensive developmental system drift

Abstract

AbstractIn evolution, it is widely believed that phenotypic changes root in developmental changes and phenotype conservation, in developmental conservation. Seeming phenotype conservation may however hide evolutionary changes in the underlying developmental mechanisms by which a trait is produced. This cryptic evolution is also called Developmental System Drift, and the extent of this phenomenon unclear. We used a well-characterized evo-devo model system, rodent molars, to test the correlation between phenotypic and developmental evolution. Between mouse and hamster, the morphology of the lower molars has much less diverged than the morphology of the upper molars. Is development accordingly more conserved? We compared molar crown formation with a standard approach, and with a tight transcriptome time-series to get a quantitative molecular profiling of developmental states. Our data identify common trends in the development of all molars. Upper and lower molars have their specificities since the early steps of morphogenesis, at the levels of the pattern of cusp formation, cellular composition and biased gene expression. The extent of difference in lower vs. upper molar development within one species does correlate with the extent of difference in final morphology. However, the specificity of lower vs. upper molar development is drowned among the rapid evolution of development, which is highly species-specific in term of expression levels and temporal profiles. Divergence in developmental systems is almost as high for lower as it is for upper molar, despite much lesser morphological changes in lower molar crown. Hence, our results point an extensive drift in this developmental system. Because serial organs are largely sharing gene networks, it supports previous theoretical work that suggest a causal link between pleiotropy and DSD.