Uncovering the Genetic Architecture of Replicated Adaptation

Identifying the genetic architecture underlying adaptive traits has been a longstanding goal in evolutionary biology. Yet, this is an extremely challenging task in natural populations – not only do evolutionary forces generate associations between traits, but they also create patterns of genomic divergence that hinder our ability to distinguish causal from correlated genetic effects. We use a powerful approach which combines parallel population genomics with association mapping in an advanced recombinant population to uncover the genetic mechanisms underlying adaptive trait evolution. In advanced recombinant populations, genetic linkage is broken down and traits are decoupled from one another, enabling variants to be associated with adaptive traits. Here, we show how repeated evolution of the auxin hormone pathway in populations of an Australian wildflower,  Senecio lautus, has led to adaptive divergence of shoot gravitropism – a complex trait defined as the ability of a plant to curve upwards in response to gravity. We sequenced 80 genomes from six natural populations that have evolved in parallel as well as 133 genomes from an advanced recombinant population derived from two of the natural populations. With these natural and recombinant populations, we link genetic variation in the auxin pathway to gravitropism and reveal a set of 45 gene regions that are directly associated with gravitropism and have been preferentially targeted by natural selection during the evolution of the species. Our work paves the way to understand how polygenic adaptation contributes to replicated genomic patterns of divergence in natural populations.