Data from: Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies

Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in Heliconius, a clade of neotropical butterflies that have undergone an adaptive radiation for wing-pattern mimicry and are influenced by distinct selection regimes. Using crosses between natural wing-pattern variants, we used genome-wide restriction site-associated DNA (RAD) genotyping, traditional linkage mapping and multivariate image analysis to study the evolution of the architecture of adaptive variation in two closely related species: Heliconius hecale and H. ismenius. We implemented a new morphometric procedure for the analysis of whole-wing pattern variation, which allows visualising spatial heatmaps of genotype-to-phenotype association for each quantitative trait locus separately. We used the H. melpomene reference genome to fine-map variation for each major wing-patterning region uncovered, evaluated the role of candidate genes and compared genetic architectures across the genus. Our results show that, although the loci responding to mimicry selection are highly conserved between species, their effect size and phenotypic action vary throughout the clade. Multilocus architecture is ancestral and maintained across species under directional selection, whereas the single-locus (supergene) inheritance controlling polymorphism in H. numata appears to have evolved only once. Nevertheless, the conservatism in the wing-patterning toolkit found throughout the genus does not appear to constrain phenotypic evolution towards local adaptive optima.

自费希尔（Fisher）以来，解析适应性性状的遗传架构便始终是现代进化生物学的核心议题；然而，由于实证数据匮乏，学界对生态重要性状的遗传架构如何影响这些性状的多样化的评估始终受阻。如今，高通量基因组学技术为深入探究近缘类群的基因组-表型映射变异提供了可能。本研究聚焦釉蛱蝶属（Heliconius）翅纹多样性的演化历程：该类群为新热带界蝴蝶，其翅纹拟态经历了适应性辐射，并受到不同选择压力的调控。本研究通过自然翅纹变异个体间的杂交实验，结合全基因组限制性酶切位点相关DNA（restriction site-associated DNA, RAD）分型、传统连锁作图与多变量图像分析，对两个近缘物种——赫氏釉蛱蝶（Heliconius hecale）与伊斯曼釉蛱蝶（H. ismenius）的适应性变异架构演化展开研究。我们开发了一套全新的形态测量流程，用于分析全翅纹变异，该方法可分别可视化每个数量性状位点的基因型-表型关联空间热图。我们以红带袖蝶（H. melpomene）参考基因组为模板，对已鉴定的各主要翅纹区域变异进行精细定位，评估候选基因的功能，并比较该属内不同类群的遗传架构差异。研究结果表明，尽管响应拟态选择的基因位点在物种间高度保守，但其效应量与表型调控方式在该属类群中存在显著差异。多基因座架构为祖先性状，并在定向选择下被多个物种保留；而控制夜神釉蛱蝶（H. numata）多态性的单基因座（超基因）遗传模式似乎仅演化出现一次。尽管如此，该属翅纹调控工具包的保守性并未限制物种向本地适应性最优表型方向的演化。