Rand D M, Clark A G, Kann L M
Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912, USA.
Genetics. 2001 Sep;159(1):173-87. doi: 10.1093/genetics/159.1.173.
Theoretical and empirical studies have shown that selection cannot maintain a joint nuclear-cytoplasmic polymorphism within a population except under restrictive conditions of frequency-dependent or sex-specific selection. These conclusions are based on fitness interactions between a diploid autosomal locus and a haploid cytoplasmic locus. We develop a model of joint transmission of X chromosomes and cytoplasms and through simulation show that nuclear-cytoplasmic polymorphisms can be maintained by selection on X-cytoplasm interactions. We test aspects of the model with a "diallel" experiment analyzing fitness interactions between pairwise combinations of X chromosomes and cytoplasms from wild strains of Drosophila melanogaster. Contrary to earlier autosomal studies, significant fitness interactions between X chromosomes and cytoplasms are detected among strains from within populations. The experiment further demonstrates significant sex-by-genotype interactions for mtDNA haplotype, cytoplasms, and X chromosomes. These interactions are sexually antagonistic--i.e., the "good" cytoplasms in females are "bad" in males--analogous to crossing reaction norms. The presence or absence of Wolbachia did not alter the significance of the fitness effects involving X chromosomes and cytoplasms but tended to reduce the significance of mtDNA fitness effects. The negative fitness correlations between the sexes demonstrated in our empirical study are consistent with the conditions that maintain cytoplasmic polymorphism in simulations. Our results suggest that fitness interactions with the sex chromosomes may account for some proportion of cytoplasmic variation in natural populations. Sexually antagonistic selection or reciprocally matched fitness effects of nuclear-cytoplasmic genotypes may be important components of cytonuclear fitness variation and have implications for mitochondrial disease phenotypes that differ between the sexes.
理论和实证研究表明，除了在频率依赖或性别特异性选择的限制条件下，选择无法在种群中维持联合核质多态性。这些结论基于二倍体常染色体位点与单倍体细胞质位点之间的适合度相互作用。我们构建了一个X染色体和细胞质联合传递的模型，并通过模拟表明，核质多态性可以通过对X-细胞质相互作用的选择来维持。我们用一个“双列杂交”实验来测试该模型的各个方面，该实验分析了黑腹果蝇野生菌株X染色体和细胞质两两组合之间的适合度相互作用。与早期常染色体研究相反，在种群内的菌株之间检测到X染色体和细胞质之间存在显著的适合度相互作用。该实验进一步证明了线粒体DNA单倍型、细胞质和X染色体存在显著的性别-基因型相互作用。这些相互作用具有性拮抗作用——即雌性中的“好”细胞质在雄性中是“坏”的——类似于交叉反应规范。沃尔巴克氏体的存在与否并没有改变涉及X染色体和细胞质的适合度效应的显著性，但往往会降低线粒体DNA适合度效应的显著性。我们实证研究中所证明的两性之间的负适合度相关性与模拟中维持细胞质多态性的条件一致。我们的结果表明，与性染色体的适合度相互作用可能占自然种群中细胞质变异的一定比例。性拮抗选择或核质基因型的相互匹配适合度效应可能是核质适合度变异的重要组成部分，并对两性之间不同的线粒体疾病表型具有影响。
