Data from: What causes mating system shifts in plants? Arabidopsis lyrata as a case study

The genetic breakdown of self-incompatibility (SI) and subsequent mating system shifts to inbreeding has intrigued evolutionary geneticists for decades. Most of our knowledge is derived from interspecific comparisons between inbreeding species and their outcrossing relatives, where inferences may be confounded by secondary mutations that arose after the initial loss of SI. Here, we study an intraspecific breakdown of SI and its consequences in North American Arabidopsis lyrata to test whether: (1) particular S-locus haplotypes are associated with the loss of SI and/or the shift to inbreeding; (2) a population bottleneck may have played a role in driving the transition to inbreeding; and (3) the mutation(s) underlying the loss of SI are likely to have occurred at the S-locus. Combining multiple approaches for genotyping, we found that outcrossing populations on average harbour 5 to 9 S-locus receptor kinase (SRK) alleles, but only two, S1 and S19, are shared by most inbreeding populations. Self-compatibility (SC) behaved genetically as a recessive trait, as expected from a loss-of-function mutation. Bulked segregant analysis in SC × SI F2 individuals using deep sequencing confirmed that all SC plants were S1 homozygotes but not all S1 homozygotes were SC. This was also revealed in population surveys, where only a few S1 homozygotes were SC. Together with crossing data, this suggests that there is a recessive factor that causes SC that is physically unlinked to the S-locus. Overall, our results emphasise the value of combining classical genetics with advanced sequencing approaches to resolve long outstanding questions in evolutionary biology.

自交不亲和性（self-incompatibility, SI）的遗传瓦解以及随后向近交交配系统的转变，数十年来一直令进化遗传学家们深感着迷。目前学界的绝大多数认知均来自近交物种与其远交近缘类群之间的种间比较，但这类研究中的推论可能会受到初始自交不亲和性丧失后出现的次生突变的干扰。本研究以北美拟南芥（Arabidopsis lyrata）为研究对象，对其种内的自交不亲和性瓦解及其演化后果展开探究，以验证以下三个核心假说：（1）特定的S位点（S-locus）单倍型是否与自交不亲和性的丧失和/或向近交的转变存在关联；（2）种群瓶颈是否可能在推动向近交的过渡中发挥了作用；（3）导致自交不亲和性丧失的突变是否极有可能发生在S位点上。本研究结合多种基因分型手段，结果显示远交种群平均携带5至9个S位点受体激酶（S-locus receptor kinase, SRK）等位基因，但仅有S1和S19这两种等位基因被多数近交种群共享。自交亲和性（self-compatibility, SC）在遗传上表现为隐性性状，这与功能丧失型突变的预期结果相符。通过对自交亲和 × 自交不亲和F₂个体进行深度测序的集群分离分析（bulked segregant analysis），本研究证实所有自交亲和植株均为S1纯合子，但并非所有S1纯合子均表现出自交亲和性。这一结论在种群调查中也得到了验证：仅少数S1纯合子为自交亲和植株。结合杂交实验数据，该结果表明存在一个与S位点物理上不连锁的隐性因子，该因子可导致自交亲和性。总体而言，本研究结果凸显了将经典遗传学研究方法与先进测序技术相结合的重要价值，可为解决进化生物学中长期悬而未决的科学问题提供有效的研究路径。