Data from: Population genomics of divergence within an obligate pollination mutualism: selection maintains differences between Joshua tree species

PREMISE OF THE STUDY: Speciation is a complex process that can be shaped by many factors, from geographic isolation to interspecific interactions. In Joshua trees, selection from pollinators on style length has been hypothesized to contribute to the maintenance of differentiation between two hybridizing sister species. We used population genomics approaches to measure the extent of genetic differentiation between these species, test whether selection maintains differences between them, and determine whether genetic variants associated with style length show signatures of selection.

METHODS: Using restriction-site-associated DNA (RAD)-sequencing, we identified 9516 single nucleotide polymorphisms (SNPs) across the Joshua tree genome. We characterized the genomic composition of trees in a narrow hybrid zone and used genomic scans to search for signatures of selection acting on these SNPs. We used a genome-wide association study to identify SNPs associated with variation in phenotypic traits, including style length, and asked whether those SNPs were overrepresented among the group under selection.

KEY RESULTS: The two species were highly genetically differentiated (FST = 0.25), and hybrids were relatively rare in the hybrid zone. Approximately 20% of SNPs showed evidence of selection maintaining divergence. While SNPs associated with style length were overrepresented among those under selection (P << 0.0001), the same was true for SNPs associated with highly differentiated vegetative traits.

CONCLUSIONS: The two species of Joshua tree are clearly genetically distinct, and selection is maintaining differences between them. We found that loci associated with differentiated traits were likely to be under selection. However, many traits other than style length appeared to be under selection. Together with the dearth of intermediate hybrids, these findings reveal that these taxa are more strongly diverged than previously suspected and that selection, likely on many targets, is maintaining separation where the two species meet and hybridize.

研究背景：物种形成是一个复杂的过程，可由多种因素塑造，从地理隔离到种间相互作用均会对其进程产生影响。针对约书亚树（Joshua tree），已有假说提出：传粉者对花柱长度的选择作用，有助于维持两个杂交姊妹种之间的遗传分化。本研究采用群体基因组学方法，量化这两个物种间的遗传分化程度，验证选择是否维持了二者的遗传差异，并探究与花柱长度相关的遗传变异是否存在选择信号。

研究方法：通过限制性位点相关DNA（restriction-site-associated DNA, RAD）测序技术，我们在约书亚树全基因组中鉴定出9516个单核苷酸多态性（single nucleotide polymorphisms, SNPs）。我们对狭窄杂交带内的约书亚树个体进行基因组组成分析，并通过基因组扫描法搜寻这些SNPs所受选择的信号。此外，我们开展全基因组关联分析，鉴定出与包括花柱长度在内的表型性状变异相关的SNPs，并探究这些SNPs在受选择位点集合中是否存在富集现象。

主要结果：两个物种间的遗传分化程度极高（FST=0.25），且杂交带内的杂交个体相对稀少。约20%的SNPs呈现出维持物种分化的选择信号。尽管与花柱长度相关的SNPs在受选择位点中显著富集（P << 0.0001），但与分化程度极高的营养性状相关的SNPs亦呈现相同的富集趋势。

研究结论：两种约书亚树在遗传层面存在明确的分化，且选择作用维持了二者的遗传差异。我们发现，与分化性状相关的基因座大概率受到选择作用的调控。然而，除花柱长度外，诸多其他性状似乎也处于选择压力之下。结合杂交带内缺乏中间型杂交个体的现象，本研究结果表明：这两个类群的分化程度远超此前预期，且很可能通过作用于多个靶标的选择作用，维持了二者在杂交接触区的物种隔离与分化。