Toward a theory of homology: development and the de-coupling of morphological and molecular evolution

Abstract

Advances in developmental genetics and evo-devo in the last several decades have enabled the growth of novel developmental approaches to the classic theme of homology. These approaches depart from the more standard phylogenetic view by contending that homology between morphological characters depends on developmental-genetic individuation and explanation. This article provides a systematic re-examination of the relationship between developmental and phylogenetic homology in light of current evidence from developmental and evolutionary genetics and genomics. I present a qualitative model of the processes that cause de-coupling of morphological and molecular evolution by developmental system drift (DSD), and hypothesize that DSD is a widespread and regular stochastic process that is predictable from parameters such as population size, pleiotropy, and regulatory redundancy. These theoretical findings support an integrative approach in which models of DSD aid in determining when developmental-genetic explanations of homology apply and when other explanations such as stabilizing selection are needed. I argue that a phylogenetic monism about the definition and criteria of homology supports the integration of different explanations into a theory of homology better than pluralism does.