Distyly supergenes as a model to understand the evolution of genetic architecture

Abstract

Genetic architecture, the relative positions of genes across the genome, can appear random with genes scattered without regard to function, but evidence suggests that it is shaped by evolution. In particular, the evolutionary trajectories of functional traits can both be influenced by and influence their underlying genetic architecture. Where multiple loci contribute to local adaptation, coadapted gene complexes can form that consist of combinations of alleles whose interactions have been shaped by selection to optimize trait expression (Prakash and Lewontin, 1968; Allard et al., 1972). Coadapted gene complexes, however, are vulnerable to disruption by recombination following gene flow from outside the zone of local adaptation if different zones have distinct sets of alleles. The power of recombination to disrupt allelic combinations is reduced if loci are situated close to each other in the genome. Simulation models of the evolution of genetic architecture show that divergent gene clusters can emerge under selection with gene movement and turnover across the genome (Yeaman, 2013; Lindtke and Buerkle, 2015). A growing body of empirical evidence of clustered genomic architectures underlying adaptive traits supports these ideas (Table 1). The extent to which adaptation avails of pre-existing genetic architecture or whether genetic architecture evolves in response to selective pressure is an open question, however. Answers will come from systems where the genetic architecture underlying an adaptive trait has important consequences for expression and function.