Department of Zoology, University of Cambridge, Cambridge, United Kingdom.
PLoS Genet. 2010 Feb 5;6(2):e1000794. doi: 10.1371/journal.pgen.1000794.
Wing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are "hotspots" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by approximately 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.
凤蝶翅膀的斑纹是缪勒拟态和强烈自然选择下表型辐射的长期范例。控制这些模式的基因座是适应进化的“热点”，在该属的不同物种中具有很大的等位基因多样性。我们在 Heliconius melpomene 和相关物种的两个基因座和多个杂交区描述了核苷酸变异、基因型-表型关联、连锁不平衡和候选基因表达。HmB 等位基因控制红色前翅带的存在或不存在，而 HmYb 等位基因控制黄色后翅条。在 HmYb 的两个区域，大约相隔 100 kb，显示出显著的基因型-表型关联，这种关联在独立的杂交区中得到了复制。相比之下，在 HmB 中，一个单一的关联峰表明三个基因的功能位点的可能位置，这些基因编码一种肌球蛋白、一种 G 蛋白偶联受体和一种 mRNA 剪接因子。在 HmYb 和 HmB 都有证据表明，与关联位点之间的连锁不平衡（LD）增强，这些关联位点相隔 14 kb，表明多个位点受到选择。然而，没有证据表明变异减少或偏离中性，这可能表明最近的选择清除，这与这些等位基因相对古老一致。在与 HmB 基因座相关的三个基因中，肌球蛋白在种族之间的翅膀盘表达中存在差异，在共同拟态的 Heliconius erato 中得到了复制，这为缪勒共同拟态的基因表达平行变化提供了引人注目的证据。因此，Heliconius melpomene 的翅膀图案基因座显示出由选择维持的单倍型结构，但没有最近选择清除的证据。这种复杂的遗传模式与之前研究的许多适应性特征的简单遗传基础形成对比，但可能为在自然种群中已经发生的、经过数百万年而不是几十年的大多数适应性提供了更好的模型。
