A shift to shorter cuticular hydrocarbons accompanies sexual isolation amongDrosophila americanagroup populations

Abstract

Because sensory signals often evolve rapidly, they could be instrumental in the emergence of reproductive isolation between species. However, pinpointing their specific contribution to isolating barriers, and the mechanisms underlying their divergence, remains challenging. Here, we demonstrate sexual isolation due to divergence in chemical signals between two populations of Drosophila americana (SC and NE) and one population of D. novamexicana, and dissect its underlying phenotypic and genetic mechanisms. Mating trials revealed strong sexual isolation between Drosophila novamexicana males and SC Drosophila americana females, as well as more moderate bi‐directional isolation between D. americana populations. Mating behavior data indicate SC D. americana males have the highest courtship efficiency and, unlike males of the other populations, are accepted by females of all species. Quantification of cuticular hydrocarbon (CHC) profiles—chemosensory signals that are used for species recognition and mate finding in Drosophila—shows that the SC D. americana population differs from the other populations primarily on the basis of compound carbon chain‐length. Moreover, manipulation of male CHC composition via heterospecific perfuming—specifically perfuming D. novamexicana males with SC D. americana males—abolishes their sexual isolation from these D. americana females. Of a set of candidates, a single gene—elongase CG17821—had patterns of gene expression consistent with a role in CHC differences between species. Sequence comparisons indicate D. novamexicana and our Nebraska (NE) D. americana population share a derived CG17821 truncation mutation that could also contribute to their shared “short” CHC phenotype. Together, these data suggest an evolutionary model for the origin and spread of this allele and its consequences for CHC divergence and sexual isolation in this group.

Two different adaptive speciation mechanisms operate during adaptation to a novel hot environment

“…The assortative mating between the ancestral and each evolved population clearly reflects a by-product of temperature adaptation. Consistent with several experimental speciation studies in Drosophila (Davis et al, 2021;, which showed that a modified CHC profile can result in assortative mating, we also found that the CHC profile in all evolved populations changed in the same direction. Further support for environmental factors, such as temperature, shaping CHC composition comes from latitudinal clines of multiple Drosophila species (Frentiu and Chenoweth, 2010).…”

Seasonal changes in photoperiod and temperature lead to changes in cuticular hydrocarbon profiles and affect mating success in Drosophila suzukii

“…There is evidence that CHC profiles containing more longer-chain hydrocarbons have evolved in several species of Drosophila against desiccation stress 36 . However, not all species-specific CHC profile compositions can be explained by adaptation to environments with low humidity or high temperatures 37,38 . Both, shorter-chain and longer-chain hydrocarbons can function as sex pheromones in Drosophila as shown in D. melanogaster.…”

“…Alternatively, the latency of mating could be explained by the immaturity of the individuals of the 1-day-old winter morph. To test these hypotheses, perfuming experiments should be conducted as shown in Davis et al 37 . Ala-Honkola et al 22 reported similar CHC profile differences between diapausing and reproductive adults of D. montana, where mating success correlated with CHC profiles, i.e., diapause-induced pairs had lower mating rates and offspring, corresponding to the differences in CHC profiles of diapausing and non-diapausing individuals.…”