Causes and Consequences of Variation in Cuticular Hydrocarbons
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Understanding how phenotypic variation arises and contributes to reproductive isolation is a central goal in evolutionary biology. The “magic trait” hypothesis posits that traits subject to divergent ecological selection and pleiotropically causing assortative mating can facilitate speciation, even in the face of gene flow. I tested this hypothesis using cuticular hydrocarbons (CHCs) in Hawaiian swordtail crickets of the genus Laupala, a rapidly speciating invertebrate clade with striking chemical diversity. Using gas chromatography, I found that L. makaio had significantly greater amounts of longer-chain hydrocarbons compared with its sister species, L. orientalis. These CHC differences corresponded to differences in rainfall at the localities for these species, such that L. makaio was present in drier conditions than L. orientalis. L. makaio also trended towards greater survival in moderate humidity conditions than L. orientalis. I then tested for correlation between variation in CHCs and environmental variables in populations of L. makaio along an elevational gradient. Seven compounds, of varying chain lengths, were significantly positively correlated with rainfall. I tested if there were correlated changes in CHCs and mating behavior during the transition to behavioral maturity in L. makaio. I found that there were three compounds that increased in their relative abundance, paralleling the increases in courtship behavior, as well as two compounds that were significantly greater in females than males. Finally, I documented high prezygotic barriers to mating success between L. makaio and L. orientalis, and after generating a hybrid cross between them, I found that in F2 females, CHC profiles predicted female rejection of L. makaio, indicating CHC-driven mate choice. Together, these findings provide evidence that CHCs in Laupala may act as magic traits by linking ecological selection with mating preferences. This work advances our understanding of how complex chemical traits can contribute to reproductive isolation and offers a foundation for future mechanistic studies of speciation phenotypes.