BackgroundThe maintenance of considerable genetic variation in sexually selected traits (SSTs) is puzzling given directional selection expected to act on these traits. A possible explanation is the existence of a genotype-by-environment (GxE) interaction for fitness, by which elaborate SSTs are favored in some environments but selected against in others. In the current study, we look for such interactions for fitness-related traits in the bulb mite, a male-dimorphic species with discontinuous expression of a heritable SST in the form of enlarged legs that are used as weapons.ResultsWe show that evolution at 18 °C resulted in populations with a higher prevalence of this SST compared to evolution at 24 °C. We further demonstrate that temperature modified male reproductive success in a way that was consistent with these changes. There was a genotype-by-environment interaction for reproductive success – at 18 °C the relative reproductive success of armored males competing with unarmored ones was higher than at the moderate temperature of 24 °C. However, male morph did not have interactive effects with temperature with respect to other life history traits (development time and longevity).ConclusionsA male genotype that is associated with the expression of a SST interacted with temperature in determining male reproductive success. This interaction caused an elaborate SST to evolve in different directions (more or less prevalent) depending on the thermal environment. The implication of this finding is that seasonal temperature fluctuations have the potential to maintain male polymorphism within populations. Furthermore, spatial heterogeneity in thermal conditions may cause differences among populations in SST selection. This could potentially cause selection against male immigrants from populations in different environments and thus strengthen barriers to gene flow.

Selection for secondary sexual trait (SST) elaboration may increase intralocus sexual conflict over the optimal values of traits expressed from shared genomes. This conflict can reduce female fitness, and the resulting gender load can be exacerbated by environmental stress, with consequences for a population's ability to adapt to novel environments. However, how the evolution of SSTs interacts with environment in determining female fitness is not well understood. Here, we investigated this question using replicate lines of bulb mites selected for increased or decreased prevalence of a male SST—thickened legs used as weapons. The fitness of females from these lines was measured at a temperature to which the mites were adapted (24°C), as well as at two novel temperatures: 18°C and 28°C. We found the prevalence of the SST interacted with temperature in determining female fecundity. At 28°C, females from populations with high SST prevalence were less fecund than females from populations in which the SST was rare, but the reverse was true at 18°C. Thus, a novel environment does not universally depress female fitness more in populations with a high degree of sexually selected dimorphism. We discuss possible consequences of the interaction we detected for adaptation to novel environments.

Enzyme polymorphism in phosphogluconate dehydrogenase (Pgdh) is a striking example of single gene polymorphism involved in sexual conflict in bulb mite Rhizoglyphus robini. Males homozygous for the S Pgdh allele were shown to achieve higher reproductive success than FF homozygous males, while negatively influencing fecundity of their female partners. Here, we investigate proximate mechanisms responsible for the increased reproductive success of SS males and find that the S allele is associated with shorter time until copulation, higher copulation frequency and increased sperm production. We also show that Pgdh alleles are probably codominant, with SS males gaining the highest reproductive success, FF males - the lowest - and FS-heterozygous males taking an intermediate position in all fitness parameters differentiating males of different genotypes. Additionally, we confirm the negative effect that S-bearing males impose on the fecundity of females they mate with, showing a clear pattern of interlocus sexual conflict. We discuss that this effect is probably associated with increased copulation frequency. Whereas, contrary to what we have predicted, the S allele does not cause increased general male mobility, we speculate that the S allele-bearing males are more efficient in forcing copulation and/or detecting females.

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Sexual conflict is often associated with arms race dynamics, which can lead to enhancement of traits involved in the conflict or their replacement with new traits that are more effective in securing reproductive interests of their bearers (Brockhurst et al., 2014; Rowe, Chenoweth, & Agrawal, 2018). Such dynamics result in a series of selective sweeps at one or more loci (Rowe et al., 2018) or generate positive selection in a group of molecules of similar function (Swanson, Clark, Waldrip-Dail, Wolfner, & Aquadro, 2001). In theory, however, sexual conflict could also promote polymorphism at the underlying genes (Brockhurst et al., 2014; Rowe et al., 2018). Such polymorphism could increase the potential of a population to respond to environmental change, which often initially relies on standing genetic variation (Barrett & Schluter, 2008). Yet, processes driving polymorphism in genes involved in sexual conflict received far less attention compared to those leading to escalatory arms race. One mechanism potentially maintaining polymorphism in genes involved in sexual conflict is negative frequency-dependent selection, resulting from Red-Queen dynamics analogous to antagonistic coevolution between hosts and parasites (Brockhurst et al., 2014; Rowe et al., 2018). Another potential mechanism involves negative pleiotropy (Zajitschek & Connallon, 2018), where a trait beneficial to male competitiveness is associated with detrimental pleiotropic effects on other fitness components. For example, in the soay sheep, a gene causing expression of enlarged horns, a trait beneficial to male reproductive success, has a negative pleiotropic effect on survival (Johnston et al., 2013). However, this sexually selected trait does not seem to be involved in sexual conflict.