Department of Biological and Environmental Sciences, University of Jyväskylä, Jyväskylä, 40014, Finland.
Department of Forest Science, P.O. Box 27, 00014, University of Helsinki, Finland.
Evolution. 2022 Mar;76(3):554-572. doi: 10.1111/evo.14443. Epub 2022 Feb 10.
Our understanding of how novel warning color traits evolve in natural populations is largely based on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency-dependent predation and positive assortative mating. Here, we integrate data from field surveys, predation experiments, population genomics, and phenotypic correlations to explain the origin and maintenance of geographic variation in a diet-based larval pigmentation trait in the redheaded pine sawfly (Neodiprion lecontei), a pine-feeding hymenopteran. Although our experiments confirm that N. lecontei larvae are indeed aposematic-and therefore likely to experience frequency-dependent predation-our genomic data do not support a historical demographic scenario that would have facilitated the spread of an initially deleterious allele via drift. Additionally, significantly elevated differentiation at a known color locus suggests that geographic variation in larval color is currently maintained by selection. Together, these data suggest that the novel white morph likely spread via selection. However, white body color does not enhance aposematic displays, nor is it correlated with enhanced chemical defense or immune function. Instead, the derived white-bodied morph is disproportionately abundant on a pine species with a reduced carotenoid content relative to other pine hosts, suggesting that bottom-up selection via host plants may have driven divergence among populations. Overall, our results suggest that life stage and pigment source can have a substantial impact on the evolution of novel warning signals, highlighting the need to investigate diverse aposematic taxa to develop a comprehensive understanding of color variation in nature.
我们对新的警告色特征如何在自然种群中进化的理解在很大程度上基于对生殖阶段和具有内源性色素产生的生物体的研究。在这些系统中，新等位基因需要遗传漂变才能克服来自频率依赖捕食和正交配选择的强烈净化选择。在这里，我们整合了来自野外调查、捕食实验、群体基因组学和表型相关性的数据，以解释红头松锯蝇（Neodiprion lecontei）幼虫基于饮食的色素沉着特征的地理变异的起源和维持，红头松锯蝇是一种以松为食的膜翅目昆虫。虽然我们的实验证实了 N. lecontei 幼虫确实具有警戒性——因此可能会经历频率依赖的捕食——但我们的基因组数据不支持一个历史人口情景，该情景将通过漂变促进最初有害等位基因的传播。此外，在一个已知的颜色基因座上显著升高的分化表明，幼虫颜色的地理变异目前是由选择维持的。这些数据表明，新的白色形态可能是通过选择传播的。然而，白色身体颜色不会增强警戒显示，也与增强的化学防御或免疫功能无关。相反，衍生的白色身体形态在一种相对于其他松树宿主具有降低类胡萝卜素含量的松树物种上不成比例地丰富，这表明通过宿主植物的下行选择可能导致了种群之间的分歧。总的来说，我们的结果表明，生命阶段和色素来源可以对新的警告信号的进化产生重大影响，强调需要研究不同的警戒类群，以全面了解自然界中颜色的变化。
