QTL mapping of larval color traits in pine sawflies

Pigmentation has emerged as a premier model for understanding the genetic basis of phenotypic evolution, and a growing catalog of color loci is starting to reveal biases in the mutations, genes, and genetic architectures underlying color variation in the wild. However, existing studies have sampled a limited subset of taxa, color traits, and developmental stages. To expand the existing sample of color loci, we performed quantitative trait locus (QTL) mapping analyses on two types of larval pigmentation traits that vary among populations of the redheaded pine sawfly (Neodiprion lecontei): carotenoid-based yellow body color and melanin-based spotting pattern. For both traits, our QTL models explained a substantial proportion of phenotypic variation and suggested a genetic architecture that is neither monogenic nor highly polygenic. Additionally, we used our linkage map to anchor the current N. lecontei genome assembly. With these data, we identified promising candidate genes underlying: (1) a loss of yellow pigmentation in populations in the Mid-Atlantic/northeastern USA [C locus-associated membrane protein homologous to a mammalian HDL receptor-2 gene (Cameo2) and lipid transfer particle apolipoproteins II and I gene (apoLTP-II/I )], and (2) a pronounced reduction in black spotting in Great-Lakes populations [members of the yellow gene family, tyrosine hydroxylase gene (pale), and dopamine N-acetyltransferase gene (Dat)]. Several of these genes also contribute to color variation in other wild and domesticated taxa. Overall, our findings are consistent with the hypothesis that predictable genes of large-effect contribute to color evolution in nature.

色素沉着已成为解析表型演化遗传基础的核心模型，日益扩充的色素位点目录正逐步揭示野生种群中体色变异背后的突变、基因及遗传架构所存在的偏好性。然而，现有研究仅对有限类群、体色性状及发育阶段进行了取样。为扩充现有色素位点的样本量，本研究对红松锯蜂（Neodiprion lecontei）不同种群间存在差异的两类幼虫色素性状开展了数量性状位点（quantitative trait locus, QTL）定位分析：基于类胡萝卜素的黄色体色，以及基于黑色素的斑点模式。针对这两类性状，本研究的QTL模型均可解释表型变异的较大比例，并揭示其遗传架构既非单基因调控，亦非高度多基因调控。此外，本研究利用构建的连锁图谱对当前已公布的红松锯蜂基因组组装结果进行了锚定。基于上述数据，本研究鉴定出与以下两种表型相关的潜在候选基因：（1）美国中大西洋/东北部种群的黄色色素缺失现象[与哺乳动物高密度脂蛋白受体2同源的C位点相关膜蛋白基因（Cameo2）以及脂质转运颗粒载脂蛋白II和I基因（apoLTP-II/I）]；（2）五大湖种群的黑色斑点显著减少现象[黄色基因家族（yellow gene family）、酪氨酸羟化酶基因（pale）以及多巴胺N-乙酰转移酶基因（Dat）]。其中部分基因同样参与其他野生及驯养类群的体色变异调控。综上，本研究结果支持“自然界中体色演化由效应显著的可预测基因所驱动”这一假说。