Parallel genomic architecture underlies repeated sexual signal divergence in Hawaiian Laupala crickets

Abstract

When the same phenotype evolves repeatedly, we can explore the predictability of genetic changes underlying phenotypic evolution. Theory suggests that genetic parallelism is less likely when phenotypic changes are governed by many small-effect loci compared to few of major effect, because different combinations of genetic changes can result in the same quantitative outcome. However, some genetic trajectories might be favored over others, making a shared genetic basis to repeated polygenic evolution more likely. To examine this, we studied the genetics of parallel male mating song evolution in the Hawaiian cricket Laupala. We compared quantitative trait loci (QTL) underlying song divergence in three species pairs varying in phenotypic distance. We tested whether replicated song divergence between species involves the same QTL and the likelihood that sharing QTL is related to phenotypic effect sizes. Contrary to theoretical predictions, we find substantial parallelism in polygenic genetic architectures underlying repeated song divergence. QTL overlapped more than expected based on simulated QTL analyses. Interestingly, QTL effect size did not predict QTL sharing, but did correlate with magnitude of phenotypic divergence. We highlight potential mechanisms driving these constraints on cricket song evolution and discuss a scenario that consolidates empirical quantitative genetic observations with micro-mutational theory.