Across diverse taxa, selfing species have evolved independently from outcrossing species thousands of times. The transition from outcrossing to selfing decreases the effective population size, effective recombination rate and heterozygosity within a species. These changes lead to a reduction in genetic diversity, and therefore adaptive potential, by intensifying the effects of random genetic drift and linked selection. Within the nematode genus Caenorhabditis, selfing has evolved at least three times, and all three species, including the model organism Caenorhabditis elegans, show substantially reduced genetic diversity relative to outcrossing species. Selfing and outcrossing Caenorhabditis species are often found in the same niches, but we still do not know how selfing species with limited genetic diversity can adapt to these environments. Here, we examine the whole-genome sequences from 609 wild C. elegans strains isolated worldwide and show that genetic variation is concentrated in punctuated hyper-divergent regions that cover 20% of the C. elegans reference genome. These regions are enriched in environmental response genes that mediate sensory perception, pathogen response and xenobiotic stress response. Population genomic evidence suggests that genetic diversity in these regions has been maintained by long-term balancing selection. Using long-read genome assemblies for 15 wild strains, we show that hyper-divergent haplotypes contain unique sets of genes and show levels of divergence comparable to levels found between Caenorhabditis species that diverged millions of years ago. These results provide an example of how species can avoid the evolutionary dead end associated with selfing.

在不同的类群中，自交物种已经从异交物种中独立进化了数千次。从异型杂交到自交的转变降低了物种内的有效种群规模、有效重组率和杂合性。这些变化通过强化随机遗传漂变和连锁选择的影响，导致遗传多样性减少，从而降低适应潜力。线虫属线虫中，自交至少进化了三次，所有三个物种，包括模式生物秀丽隐杆线虫，都表现出相对于异交物种显着降低的遗传多样性。自交和异交的秀丽隐杆线虫物种经常在相同的生态位中发现，但我们仍然不知道遗传多样性有限的自交物种如何适应这些环境。在这里，我们检查了世界范围内分离的 609 个野生线虫菌株的全基因组序列，结果表明遗传变异集中在间断的高度分化区域，该区域覆盖了线虫参考基因组的 20%。这些区域富含介导感官知觉、病原体反应和外源应激反应的环境反应基因。群体基因组证据表明，这些地区的遗传多样性是通过长期平衡选择得以维持的。使用 15 个野生菌株的长读基因组组装，我们发现高度分化的单倍型包含独特的基因组，并且显示出的分化水平与数百万年前分化的秀丽隐杆线虫物种之间发现的水平相当。这些结果提供了一个例子，说明物种如何避免与自交相关的进化死胡同。