Transcriptomics of differences in thermal plasticity associated with selection for an exaggerated male sexual trait

Abstract

BackgroundThe information about the magnitude of between-individual differences in thermal plasticity and identification of the underlying molecular mechanisms are key to understand the evolution of thermal plasticity. In particular, genes underlying variation in the physiological response to temperature can provide raw material for selection acting on plastic traits. Using RNAseq, we investigate the transcriptional response to temperature in males and females from the bulb mite populations selected for the increased frequency of one of two discrete male morphs (fighter- and scrambler-selected populations) that differ in relative fitness depending on temperature.ResultsAt decreased temperature, males from fighter-selected populations showed higher transcriptomic plasticity, as indicated by a significant selection treatment by temperature (decreased vs. control) interaction effect on the expression of 40 genes, 38 of which were overexpressed in fighter-selected populations in response to temperature decrease. These genes were mostly associated with carbohydrate metabolism. At increased temperature, no selection-by-temperature interaction in gene expression was detected. Hence, between-morph differences in response to increased temperature are most likely determined by genes consistently differing in expression between morphs. These genes were associated with protein metabolism, ion transport, lipid metabolism and oxidoreductase activity among others. In females, we did not find genes with selection-treatment-specific response to temperature decrease or increase, but both sexes differed between selection treatments in expression of 79 genes. They can be treated as candidates for genes underlying temperature sensitivity of fitness differences between females from fighter- and scrambler-selected populations.ConclusionDifferent mechanisms underly the divergence in thermal response between populations differing in sexually selected traits prevalence at decreased vs. increased temperature. While temperature decrease was associated with higher transcriptomic plasticity of males with more elaborate armaments, differential response to temperature increase likely depended on genes associated with their distinct thermal tolerance. Selection on males drove gene expression patterns in females. These patterns could be associated with temperature-dependent fitness differences between females from fighter- vs. scrambler-selected populations reported in previous studies. Our study shows that selection for divergent male sexually selected morphologies and behaviors has a potential to drive divergence in metabolic pathways underlying plastic response to temperature in both sexes.

Fertility loss under thermal stress: males have lower fertility limits but no evidence of sex differences in sensitivity

“…Nonetheless, these results suggest that despite scramblers being more burdened with deleterious mutations compared to fighters (Łukasiewicz et al 2020, this does not influence their fertility under thermal stress. One possible explanation for why we did not observe any morph-specific difference in TFL or TSF is that there are limited morph-specific changes in gene expression when exposed to higher temperatures (Plesnar-Bielak et al 2022), suggesting that differences between fighter and scrambler plastic responses to thermal stress may be limited. We also find no support for the view that bearing costly weaponry amplifies the costs of thermal stress in a way that also influences fertility, or indeed mating rates.…”

“…This suggests that both spermatogenesis and oogenesis are sensitive to temperatures that do not cause complete sterilisation. The expression of a large number of genes has been shown to be altered in R. robini due to exposure to different thermal conditions (Plesnar-Bielak et al 2022), and it is possible that expression of genes involved in pathways associated with both oogenesis and spermatogenesis have been altered. We found that these thermal effects on male and female fertility appear to be additive, as the greatest declines in reproductive output occur when both males and females are heat stressed.…”

Sex-specific recombination landscape in a species with holocentric chromosomes

“…We downloaded the bulb mite genome’s predicted gene annotation from ORCAE (Parrett et al, 2022; Sterck et al, 2012), https://bioinformatics.psb.ugent.be/gdb/Rhizoglyphus_robini), which contains an unexpectedly high number of predicted genes (60,310 genes), suggesting the presence of pseudogenes or gene prediction errors. To refine the dataset, we excluded genes with expression levels below 1 FPKM, based on expression data from Plesnar-Bielak et al (2022). This filtering retained 27,363 genes mapped to chromosomes.…”