Competing adaptations maintain non-adaptive variation in a wild cricket population

Abstract

How emerging adaptive variants interact is an important factor in the evolution of wild populations. However, the opportunity to empirically study this interaction is rare. We recently documented the emergence of an adaptive phenotype 'curly-wing' in Hawaiian populations of field crickets (Teleogryllus oceanicus). Curly-wing inhibits males' ability to sing, protecting them from eavesdropping parasitoid flies (Ormia ochracea). Surprisingly, curly-wing co-occurs with similarly protective silent 'flatwing' phenotypes in multiple populations, in which neither phenotype has spread to fixation. These two phenotypes are frequently co-expressed, but since either phenotype sufficiently reduces song amplitude to evade the fly, co-expression confers no additional fitness benefit. Numerous negative fitness consequences are known to accompany flatwing, and we find that curly-wing, too, incurs fitness costs via reduced male courtship success and reduced female longevity. We show through crosses, genomic and mRNA sequencing that curly-wing expression is associated with variation on a single autosome. In parallel analyses of flatwing, our results reinforce previous findings of X-linked single-locus inheritance, with the phenotype likely arising through down-regulation of doublesex. By combining insights about the genetic architecture of these alternative phenotypes with simulations and field observations, we show that the co-occurrence of these two adaptations impedes either from fixing, despite extreme fitness benefits. Interestingly, both flatwing and curly-wing are statistically associated with nearby inversions, which are also retained as polymorphisms. This co-occurrence of similar adaptive forms in the same populations might be more common than generally considered, and could be an important force inhibiting adaptive evolution in wild populations.