Data from: Unexpected high genetic diversity in small populations suggests maintenance by associative overdominance

The effective population size (Ne) is a central factor in determining maintenance of genetic variation. The neutral theory predicts that loss of variation depends on Ne, with less genetic drift in larger populations. We monitored genetic drift in 42 Drosophila melanogaster populations of different adult census population sizes (10, 50 or 500) using pooled RAD sequencing. In small populations, variation was lost at a substantially lower rate than expected. This observation was consistent across two ecological relevant thermal regimes, one stable and one with a stressful increase in temperature across generations. Estimated ratios between Ne and adult census size were consistently higher in small than in larger populations. The finding provides evidence for a slower than expected loss of genetic diversity and consequently a higher than expected long-term evolutionary potential in small fragmented populations. More genetic diversity was retained in areas of low recombination, suggesting that associative overdominance, driven by disfavored homozygosity of recessive deleterious alleles, is responsible for the maintenance of genetic diversity in smaller populations. Consistent with this hypothesis, the X-chromosome, which is largely free of recessive deleterious alleles due to hemizygosity in males, fits neutral expectations even in small populations. Our experiments provide experimental answers to a range of unexpected patterns in natural populations, ranging from variable diversity on X-chromosomes and autosomes to surprisingly high levels of nucleotide diversity in small populations.有效种群大小（effective population size, Nₑ）是决定遗传变异维持的核心要素。中性理论（neutral theory）预测，遗传变异的丢失取决于有效种群大小，种群规模越大，遗传漂变（genetic drift）的作用越弱。本研究采用混合RAD测序（pooled RAD sequencing）技术，对42个不同成虫计数种群规模（10、50或500）的黑腹果蝇（Drosophila melanogaster）种群的遗传漂变进行了监测。结果显示，小型种群的遗传变异丢失速率远低于预期。这一观测结果在两种生态相关的热环境模式下均保持一致：其一为恒温稳定环境，其二为跨世代经历温度胁迫升高的环境。有效种群大小与成虫计数种群规模的估算比值，在小型种群中始终高于大型种群。该研究结果为小型生境破碎化种群中遗传多样性丢失速率慢于预期、进而长期进化潜力高于预期的现象提供了实验依据。低重组区域保留了更多的遗传多样性，这表明由隐性有害等位基因纯合性遭受选择排斥所驱动的联合超显性（associative overdominance），是小型种群维持遗传多样性的关键机制。与该假说一致的是，由于雄性的半合子状态（hemizygosity），X染色体几乎不含隐性有害等位基因，因此即便在小型种群中，其遗传变异模式也符合中性理论预期。本研究通过实验解答了自然种群中一系列令人意外的模式：涵盖X染色体与常染色体（autosomes）间的多样性差异，以及小型种群中核苷酸多样性（nucleotide diversity）水平异常高等一系列现象。