Kaufmann Philipp, Rönn Johanna Liljestrand, Immonen Elina, Arnqvist Göran
Department of Ecology and Genetics, Evolutionary Biology, Uppsala University, 75234 Uppsala, Sweden.
Department of Ecology and Genetics, Animal Ecology, Uppsala University, 75234 Uppsala, Sweden.
Mol Biol Evol. 2024 Dec 6;41(12). doi: 10.1093/molbev/msae244.
When different alleles are favored in different environments, dominance reversal where alternate alleles are dominant in the environment in which they are favored can generate net balancing selection. The sexes represent two distinct genetic environments and sexually antagonistic (SA) selection can maintain genetic variation, especially when the alleles involved show sex-specific dominance. Sexual dimorphism in gene expression is pervasive and has been suggested to result from SA selection. Yet, whether gene-regulatory variation shows sex-specific dominance is poorly understood. We tested for sex-specific dominance in gene expression using three crosses between homozygous lines derived from a population of a seed beetle, where a previous study documented a signal of dominance reversal for fitness between the sexes. Overall, we found that the dominance effects of variants affecting gene expression were positively correlated between the sexes (r = 0.33 to 0.44). Yet, 586 transcripts showed significant differences in dominance between the sexes. Sex-specific dominance was significantly more common in transcripts with more sex-biased expression, in two of three of our crosses. Among transcripts showing sex-specific dominance, lesser sexual dimorphism in gene expression among heterozygotes was somewhat more common than greater. Gene ontology enrichment analyses showed that functional categories associated with known SA phenotypes in Callosobruchus maculatus were overrepresented among transcripts with sex-specific dominance, including genes involved in metabolic processes and the target-of-rapamycin pathway. Our results support the suggestion that sex-specific dominance of regulatory variants contributes to the maintenance of genetic variation in fitness mediated by SA selection in this species.
当不同的等位基因在不同环境中受到青睐时,优势逆转(即替代等位基因在其受青睐的环境中占主导地位)会产生净平衡选择。两性代表两种不同的遗传环境,性拮抗(SA)选择可以维持遗传变异,尤其是当所涉及的等位基因表现出性别特异性优势时。基因表达中的性别二态性普遍存在,并被认为是由SA选择导致的。然而,基因调控变异是否表现出性别特异性优势却知之甚少。我们利用来自一种种子甲虫种群的纯合品系之间的三次杂交,测试了基因表达中的性别特异性优势,之前的一项研究记录了该种群中两性之间适合度的优势逆转信号。总体而言,我们发现影响基因表达的变异的显性效应在两性之间呈正相关(r = 0.33至0.44)。然而,有586个转录本在两性之间的显性上存在显著差异。在我们的三次杂交中有两次,性别特异性优势在表达偏向性更强的转录本中显著更为常见。在表现出性别特异性优势的转录本中,杂合子中基因表达的性别二态性较小的情况比更大的情况略为常见。基因本体富集分析表明,在具有性别特异性优势的转录本中,与黄斑豆象已知SA表型相关的功能类别过度富集,包括参与代谢过程和雷帕霉素靶标途径的基因。我们的结果支持了这样一种观点,即调控变异的性别特异性优势有助于维持该物种中由SA选择介导的适合度的遗传变异。