INRA, UMR 1349, Institute of Genetics, Environment and Plant Protection, Domaine de la Motte, Le Rheu, France.
PLoS Genet. 2013;9(8):e1003690. doi: 10.1371/journal.pgen.1003690. Epub 2013 Aug 8.
Evolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative modes of inheritance of sex chromosomes offer interesting opportunities for studying sexual conflicts and their resolution, because expectations for the preferred genomic location of sexually antagonistic alleles may differ from standard systems. Aphids display an XX/X0 system and combine an unusual inheritance of the X chromosome with the alternation of sexual and asexual reproduction. In this study, we first investigated theoretically the accumulation of sexually antagonistic mutations on the aphid X chromosome. Our results show that i) the X is always more favourable to the spread of male-beneficial alleles than autosomes, and should thus be enriched in sexually antagonistic alleles beneficial for males, ii) sexually antagonistic mutations beneficial for asexual females accumulate preferentially on autosomes, iii) in contrast to predictions for standard systems, these qualitative results are not affected by the dominance of mutations. Under the assumption that sex-biased gene expression evolves to solve conflicts raised by the spread of sexually antagonistic alleles, one expects that male-biased genes should be enriched on the X while asexual female-biased genes should be enriched on autosomes. Using gene expression data (RNA-Seq) in males, sexual females and asexual females of the pea aphid, we confirm these theoretical predictions. Although other mechanisms than the resolution of sexual antagonism may lead to sex-biased gene expression, we argue that they could hardly explain the observed difference between X and autosomes. On top of reporting a strong masculinization of the aphid X chromosome, our study highlights the relevance of organisms displaying an alternative mode of sex chromosome inheritance to understanding the forces shaping chromosome evolution.
进化理论预测，在具有 XY 性别决定系统的物种中，性拮抗突变会在 X 染色体和常染色体上积累，其影响（X 的雄性化或雌性化）取决于突变的显性。具有性染色体替代遗传模式的生物为研究性冲突及其解决提供了有趣的机会，因为对性拮抗等位基因优选基因组位置的期望可能与标准系统不同。蚜虫表现出 XX/X0 系统，并结合了 X 染色体的不寻常遗传与有性和无性繁殖的交替。在这项研究中，我们首先从理论上研究了性拮抗突变在蚜虫 X 染色体上的积累。我们的结果表明：i）X 染色体总是比常染色体更有利于雄性有益等位基因的传播，因此应该富含对雄性有益的性拮抗等位基因，ii）对无性雌性有益的性拮抗突变优先在常染色体上积累，iii）与标准系统的预测相反，这些定性结果不受突变显性的影响。假设性别偏向基因表达的进化是为了解决由性拮抗等位基因传播引起的冲突，人们期望雄性偏向基因应该在 X 染色体上富集，而无性雌性偏向基因应该在常染色体上富集。利用豌豆蚜雄性、有性雌性和无性雌性的基因表达数据（RNA-Seq），我们证实了这些理论预测。尽管除了解决性拮抗作用之外的其他机制可能导致性别偏向基因表达，但我们认为它们很难解释 X 染色体和常染色体之间的观察到的差异。除了报告蚜虫 X 染色体的强烈雄性化之外，我们的研究还强调了具有替代性染色体遗传模式的生物对于理解塑造染色体进化的力量具有重要意义。
