The role of gene duplication in facilitating divergent patterns of gene expression across a complex life cycle

Abstract

Explaining the processes that facilitate divergence in the morphologies and functions expressed by organisms throughout their life cycles is fundamental for understanding life cycle evolution. Theory suggests that the expression of traits is decoupled across life stages, thus allowing for evolutionary independence. Although trait decoupling between stages has been described in many studies, explanations of how said decoupling evolves have seldom been considered. Here, we propose evolutionary divergence between duplicate genes as an important mechanism by which life cycle complexity evolves. Because the different phenotypes expressed by organisms throughout their life cycles are coded by the same genome, trait decoupling between stages must be mediated through their divergence in gene expression. Gene duplication has been identified as an important mechanism that enables divergence in gene function and expression between cells and tissues. Here, we examined the temporal changes in gene expression across the monarch butterfly (Danaus plexippus) metamorphosis. We found that within homologous groups, more phylogenetic divergent genes exhibited more distinct temporal expression patterns, and that this relationship scaled such that more phylogenetically diverse homologous groups showed more diverse patterns of gene expression. Furthermore, we found that duplicate genes showed increased stage-specificity relative to singleton genes. Overall, our findings suggest an important role of gene duplication in the evolution of trait decoupling across complex life cycles. SignificanceThe proliferation of many of the worlds most diverse groups of eukaryotes is frequently attributed to their life cycle complexity. By allowing organisms to express different traits throughout their lives, complex life cycles enable individuals to utilize multiple ecological niches. However, the mechanisms that facilitate life cycle evolution are not well understood. We drew inspiration from studies on functional divergence between different tissues and examined the role of gene duplication in generating different patterns of gene expression between stages across the metamorphosis of Danaus plexippus (the monarch butterfly). Our findings suggest that the role of gene duplication in generating differences between cell and tissue types likely extends to trait differentiation between stages within complex life cycles.