Sex differences in lifespan: females homozygous for the X chromosome do not suffer the shorter lifespan predicted by the unguarded X hypothesis

Lifespan differs between the sexes in many species. Three hypotheses to explain this interesting pattern have been proposed, involving different drivers: sexual selection, asymmetrical inheritance of cytoplasmic genomes, and hemizygosity of the X(Z) chromosome (the unguarded X hypothesis). Of these, the unguarded X has received the least experimental attention. This hypothesis suggests that the heterogametic sex suffers a shortened lifespan because recessive deleterious alleles on its single X(Z) chromosome are expressed unconditionally. In Drosophila melanogaster, the X chromosome is unusually large (~20% of the genome), providing a powerful model for evaluating theories involving the X. Here, we test the unguarded X hypothesis by forcing D. melanogaster females from a laboratory population to express recessive X-linked alleles to the same degree as males, using females exclusively made homozygous for the X chromosome. We find no evidence for reduced lifespan or egg-to-adult viability due to X homozygozity. In contrast, males and females homozygous for an autosome both suffer similar, significant reductions in those traits. The logic of the unguarded X hypothesis is indisputable, but our results suggest that the degree to which recessive deleterious X-linked alleles depress performance in the heterogametic sex appears too small to explain general sex differences in lifespan.

诸多物种的两性寿命存在显著差异。针对这一有趣的演化现象，目前已提出三种基于不同驱动机制的假说：性选择、细胞质基因组的不对称遗传，以及X(Z)染色体的半合子性（未保护X假说，unguarded X hypothesis）。其中，未保护X假说得到的实验关注最少。该假说认为，异配性别个体的寿命会缩短，原因是其仅有的一条X(Z)染色体上的隐性有害等位基因会无条件表达。在黑腹果蝇（Drosophila melanogaster）中，X染色体异常庞大（约占基因组的20%），为检验涉及X染色体的相关理论提供了极具优势的实验模型。本研究通过将实验室种群的黑腹果蝇雌性个体的X染色体制备为纯合状态，使其与雄性个体同等程度地表达X连锁隐性等位基因，以此检验未保护X假说。我们未发现因X染色体纯合导致寿命缩短或卵至成虫存活率下降的证据。与之相反，常染色体纯合的雌雄个体在上述两项性状上均出现了相似且显著的下降。未保护X假说的逻辑无可辩驳，但我们的研究结果表明，隐性有害X连锁等位基因对异配性别个体相关性状表现的抑制程度，似乎不足以解释两性寿命的普遍差异。