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Kaufmann, P., J.M. Howie, E. Immonen. 2023. Sexually antagonistic selection maintains genetic variance when sexual dimorphism evolves. Proceedings. Biological sciences .
Abstract: Genetic variance (V(G)) in fitness related traits is often unexpectedly high, evoking the question how V(G) can be maintained in the face of selection. Sexually antagonistic (SA) selection favouring alternative alleles in the sexes is common and predicted to maintain V(G), while directional selection should erode it. Both SA and sex-limited directional selection can lead to sex-specific adaptations but how each affect V(G) when sexual dimorphism evolves remain experimentally untested. Using replicated artificial selection on the seed beetle Callosobruchus maculatus body size we recently demonstrated an increase in size dimorphism under SA and male-limited (ML) selection by 50% and 32%, respectively. Here we test their consequences on genetic variation. We show that SA selection maintained significantly more ancestral, autosomal additive genetic variance than ML selection, while both eroded sex-linked additive variation equally. Ancestral female-specific dominance variance was completely lost under ML, while SA selection consistently sustained it. Further, both forms of selection preserved a high genetic correlation between the sexes (r(m,f)). These results demonstrate the potential for sexual antagonism to maintain more genetic variance while fuelling sex-specific adaptation in a short evolutionary time scale, and are in line with predicted importance of sex-specific dominance reducing sexual conflict over alternative alleles.
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Koppik, M., J. Baur, D. Berger. 2023. Increased male investment in sperm competition results in reduced maintenance of gametes. PLoS biology e3002049.
Abstract: Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male bias is that competition over fertilization of female gametes leads to increased male investment into reproduction at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here, we provide evidence for this hypothesis by harnessing the power of experimental evolution to study effects of sexual selection on the male germline in the seed beetle Callosobruchus maculatus. We first show that 50 generations of evolution under strong sexual selection, coupled with experimental removal of natural selection, resulted in males that are more successful in sperm competition. We then show that these males produce progeny of lower quality if engaging in sociosexual interactions prior to being challenged to surveil and repair experimentally induced damage in their germline and that the presence of male competitors alone can be enough to elicit this response. We identify 18 candidate genes that showed differential expression in response to the induced germline damage, with several of these previously implicated in processes associated with DNA repair and cellular maintenance. These genes also showed significant expression changes across sociosexual treatments of fathers and predicted the reduction in quality of their offspring, with expression of one gene also being strongly correlated to male sperm competition success. Sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. While more work is needed to detail the exact molecular underpinnings of our results, our findings provide rare experimental evidence for a trade-off between male success in sperm competition and germline maintenance. This suggests that sex differences in the relative strengths of sexual and natural selection are causally linked to male mutation bias. The tenet advocated here, that the allocation decisions of an individual can affect plasticity of its germline and the resulting genetic quality of subsequent generations, has several interesting implications for mate choice processes.
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Arnqvist, G., J. Ronn, C. Watson, J. Goenaga, E. Immonen. 2022. Concerted evolution of metabolic rate, economics of mating, ecology, and pace of life across seed beetles. Proceedings of the National Academy of Sciences, USA 119:e2205564119.
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Kaufmann, P., M.E. Wolak, A. Husby, E. Immonen. 2021. Rapid evolution of sexual size dimorphism facilitated by Y-linked genetic variance. Nature ecology & evolution .
Abstract: Sexual dimorphism is ubiquitous in nature but its evolution is puzzling given that the mostly shared genome constrains independent evolution in the sexes. Sex differences should result from asymmetries between the sexes in selection or genetic variation but studies investigating both simultaneously are lacking. Here, we combine a quantitative genetic analysis of body size variation, partitioned into autosomal and sex chromosome contributions and ten generations of experimental evolution to dissect the evolution of sexual body size dimorphism in seed beetles (Callosobruchus maculatus) subjected to sexually antagonistic or sex-limited selection. Female additive genetic variance (VA) was primarily linked to autosomes, exhibiting a strong intersexual genetic correlation with males ([Formula: see text] = 0.926), while X- and Y-linked genes further contributed to the male VA and X-linked genes contributed to female dominance variance. Consistent with these estimates, sexual body size dimorphism did not evolve in response to female-limited selection but evolved by 30-50% under male-limited and sexually antagonistic selection. Remarkably, Y-linked variance alone could change dimorphism by 30%, despite the C. maculatus Y chromosome being small and heterochromatic. Our results demonstrate how the potential for sexual dimorphism to evolve depends on both its underlying genetic basis and the nature of sex-specific selection.
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Ivimey-Cook, E., S. Bricout, V. Candela, A.A. Maklakov, E.C. Berg. 2021. Inbreeding reduces fitness of seed beetles under thermal stress. Journal of evolutionary biology .
Abstract: Human-induced environmental change can influence populations both at the global level through climatic warming and at the local level through habitat fragmentation. As populations become more isolated, they can suffer from high levels of inbreeding, which contributes to a reduction in fitness, termed inbreeding depression. However, it is still unclear if this increase in homozygosity also results in a corresponding increase in sensitivity to stressful conditions, which could intensify the already detrimental effects of environmental warming. Here, in a fully factorial design, we assessed the life-long impact of increased inbreeding load and elevated temperature on key life history traits in the seed beetle, Callosobruchus maculatus. We found that beetles raised at higher temperatures had far reduced fitness and survival than beetles from control temperatures. Importantly, these negative effects were exacerbated in inbred beetles as a result of increased inbreeding load, with further detrimental effects manifesting on individual eclosion probability and lifetime reproductive success. These results reveal the harmful impact that increasing temperature and likelihood of habitat fragmentation due to anthropogenetic changes in environmental conditions could have on populations of organisms worldwide.
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