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Natural and sexual selection on cuticular hydrocarbons: a quantitative genetic analysis.

ABSTRACT: While the reproductive benefits of sexual displays have been widely studied, we have relatively limited evidence of the fitness costs associated with most display traits. Insect cuticular hydrocarbon (CHC) profiles are sexually selected traits that also protect against desiccation. These two functions are thought to oppose each other, with investment in particular compounds believed to increase attractiveness at the expense of compounds that protect against water loss. We investigated this potential trade-off in a quantitative genetic framework using the Australian field cricket, Teleogryllus oceanicus. Several compounds were significantly genetically correlated with either attractiveness or desiccation resistance. Of these compounds, one was negatively genetically correlated with attractiveness but positively genetically correlated with desiccation resistance. Furthermore, scoring each individual's overall CHC profile for its level of attractiveness and desiccation resistance indicated a negative genetic correlation between these multivariate phenotypes. Together, our results provide evidence for a genetic trade-off between sexually and naturally selected functions of the CHC profile. We suggest that the production of an attractive CHC profile may be costly for males, but highlight the need for further work to support this finding experimentally. Genetic covariation between the CHC profile and attractiveness suggests that females can gain attractive sons through female choice.

SUBMITTER: Berson JD

PROVIDER: S-EPMC6532523 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Natural and sexual selection on cuticular hydrocarbons: a quantitative genetic analysis.

Berson Jacob D JD Zuk Marlene M Simmons Leigh W LW

Proceedings. Biological sciences 20190501 1902

While the reproductive benefits of sexual displays have been widely studied, we have relatively limited evidence of the fitness costs associated with most display traits. Insect cuticular hydrocarbon (CHC) profiles are sexually selected traits that also protect against desiccation. These two functions are thought to oppose each other, with investment in particular compounds believed to increase attractiveness at the expense of compounds that protect against water loss. We investigated this poten ...[more]

PMID: 31064302

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Project description:Chemical communication is the oldest form of communication, spreading across all forms of life. In insects, cuticular hydrocarbons (CHC) function as chemical cues for the recognition of mates, species, and nest-mates in social insects. Although much is known about the function of individual hydrocarbons and their biosynthesis, a phylogenetic overview is lacking. Here, we review the CHC profiles of 241 species of Hymenoptera, one of the largest and most important insect orders, which includes the Symphyta (sawflies), the polyphyletic Parasitica (parasitoid wasps), and the Aculeata (wasps, bees, and ants). We investigated whether these taxonomic groups differed in the presence and absence of CHC classes and whether the sociality of a species (solitarily vs. social) had an effect on CHC profile complexity. We found that the main CHC classes (i.e., n-alkanes, alkenes, and methylalkanes) were all present early in the evolutionary history of the Hymenoptera, as evidenced by their presence in ancient Symphyta and primitive Parasitica wasps. Throughout all groups within the Hymenoptera, the more complex a CHC the fewer species that produce it, which may reflect the Occam's razor principle that insects' only biosynthesize the most simple compound that fulfil its needs. Surprisingly, there was no difference in the complexity of CHC profiles between social and solitary species, with some of the most complex CHC profiles belonging to the Parasitica. This profile complexity has been maintained in the ants, but some specialization in biosynthetic pathways has led to a simplification of profiles in the aculeate wasps and bees. The absence of CHC classes in some taxa or species may be due to gene silencing or down-regulation rather than gene loss, as demonstrated by sister species having highly divergent CHC profiles, and cannot be predicted by their phylogenetic history. The presence of highly complex CHC profiles prior to the vast radiation of the social Hymenoptera indicates a 'spring-loaded' system where the diversity of CHC needed for the complex communication systems of social insects were already present for natural selection to act upon, rather than having evolved independently. This diversity may have aided the multiple independent evolution of sociality within the Aculeata.

Project description:Background:Cuticular hydrocarbons (CHC) have been documented to play crucial roles as species- and sex-specific cues in the chemical communication systems of a wide variety of insects. However, whether they are sufficient by themselves as the sole cue triggering sexual behavior as well as preference of con- over heterospecific mating partners is rarely assessed. We conducted behavioral assays in three representative species of parasitoid wasps (Hymenoptera: Pteromalidae) to determine their reliance on CHC as species-specific sexual signaling cues. Results:We found a surprising degree of either unspecific or insufficient sexual signaling when CHC are singled out as recognition cues. Most strikingly, the cosmopolitan species Nasonia vitripennis, expected to experience enhanced selection pressure to discriminate against other co-occurring parasitoids, did not discriminate against CHC of a partially sympatric species from another genus, Trichomalopsis sarcophagae. Focusing on the latter species, in turn, it became apparent that CHC are even insufficient as the sole cue triggering conspecific sexual behavior, hinting at the requirement of additional, synergistic sexual cues particularly important in this species. Finally, in the phylogenetically and chemically most divergent species Muscidifurax uniraptor, we intriguingly found both CHC-based sexual signaling as well as species discrimination behavior intact although this species is naturally parthenogenetic with sexual reproduction only occurring under laboratory conditions. Conclusions:Our findings implicate a discrepancy in the reliance on and specificity of CHC as sexual cues in our tested parasitioid wasps. CHC profiles were not sufficient for unambiguous discrimination and preference behavior, as demonstrated by clear cross-attraction between some of our tested wasp genera. Moreover, we could show that only in T. sarcophagae, additional behavioral cues need to be present for triggering natural mating behavior, hinting at an interesting shift in signaling hierarchy in this particular species. This demonstrates the importance of integrating multiple, potentially complementary signaling modalities in future studies for a better understanding of their individual contributions to natural sexual communication behavior.

Dataset Information

Natural and sexual selection on cuticular hydrocarbons: a quantitative genetic analysis.

Publications

Natural and sexual selection on cuticular hydrocarbons: a quantitative genetic analysis.

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