Data from: History, geography, and host use shape genome-wide patterns of genetic variation in the redheaded pine sawfly (Neodiprion lecontei)

Divergent host use has long been suspected to drive population differentiation and speciation in plant-feeding insects. Evaluating the contribution of divergent host use to genetic differentiation can be difficult, however, as dispersal limitation and population structure may also influence patterns of genetic variation. In this study, we use double-digest restriction-associated DNA (ddRAD) sequencing to test the hypothesis that divergent host use contributes to genetic differentiation among populations of the redheaded pine sawfly (Neodiprion lecontei), a widespread pest that uses multiple Pinus hosts throughout its range in eastern North America. Because this species has a broad range and specializes on host plants known to have migrated extensively during the Pleistocene, we first assess overall genetic structure using model-based and model-free clustering methods, and identify three geographically distinct genetic clusters. Next, using a composite-likelihood approach based on the site frequency spectrum and a novel strategy for maximizing the utility of linked RAD markers, we infer the population topology and date divergence to the Pleistocene. Based on existing knowledge of Pinus refugia, estimated demographic parameters, and patterns of diversity among sawfly populations, we propose a Pleistocene divergence scenario for N. lecontei. Finally, using Mantel and partial Mantel tests, we identify a significant relationship between genetic distance and geography in all clusters, and between genetic distance and host use in two of three clusters. Overall, our results indicate that Pleistocene isolation, dispersal limitation, and ecological divergence all contribute to genome-wide differentiation in this species, and support the hypothesis that host use is a common driver of population divergence in host-specialized insects.

长期以来，学界普遍推测寄主利用分化是驱动植食性昆虫种群分化与物种形成的核心驱动力。然而，评估寄主利用分化对遗传分化的贡献并非易事，因为扩散限制与种群结构同样可能影响遗传变异的分布格局。本研究采用双酶切限制性位点关联DNA（double-digest restriction-associated DNA, ddRAD）测序技术，针对红头松叶蜂（Neodiprion lecontei）开展种群遗传分化的假说验证。红头松叶蜂是一种分布广泛的林业害虫，在北美东部的分布范围内可利用多种松属（Pinus）植物作为专性寄主。鉴于该物种分布范围广泛，且其专性寄主植物在更新世时期曾发生过大规模迁移，本研究首先采用基于模型与无模型两类聚类方法，对其整体遗传结构进行解析，共鉴定出3个地理分化显著的遗传聚类群。随后，本研究基于位点频率谱（site frequency spectrum）构建复合似然分析框架，并开发了一种最大化连锁RAD标记利用效率的全新策略，以此推断种群拓扑结构并将分化时间校准至更新世时期。结合现有松属避难所的相关研究成果、估算得到的种群历史参数以及叶蜂种群的遗传多样性分布格局，本研究提出了红头松叶蜂的更新世分化演化情景。最后，本研究通过曼特尔（Mantel）检验与偏曼特尔检验，发现所有聚类群中遗传距离与地理距离均存在显著相关性，且在3个聚类群中的2个聚类群内，遗传距离与寄主利用模式同样存在显著关联。综合来看，本研究结果表明，更新世隔离、扩散限制以及生态分化共同塑造了该物种的全基因组遗传分化格局，同时验证了"寄主利用分化是寄主专化昆虫种群分化的普遍驱动力"这一假说。