Department of Genetics, North Carolina State University, Raleigh, North Carolina, United States of America.
PLoS Genet. 2010 Feb 5;6(2):e1000796. doi: 10.1371/journal.pgen.1000796.
Wing pattern evolution in Heliconius butterflies provides some of the most striking examples of adaptation by natural selection. The genes controlling pattern variation are classic examples of Mendelian loci of large effect, where allelic variation causes large and discrete phenotypic changes and is responsible for both convergent and highly divergent wing pattern evolution across the genus. We characterize nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium (LD), and candidate gene expression patterns across two unlinked genomic intervals that control yellow and red wing pattern variation among mimetic forms of Heliconius erato. Despite very strong natural selection on color pattern, we see neither a strong reduction in genetic diversity nor evidence for extended LD across either patterning interval. This observation highlights the extent that recombination can erase the signature of selection in natural populations and is consistent with the hypothesis that either the adaptive radiation or the alleles controlling it are quite old. However, across both patterning intervals we identified SNPs clustered in several coding regions that were strongly associated with color pattern phenotype. Interestingly, coding regions with associated SNPs were widely separated, suggesting that color pattern alleles may be composed of multiple functional sites, conforming to previous descriptions of these loci as "supergenes." Examination of gene expression levels of genes flanking these regions in both H. erato and its co-mimic, H. melpomene, implicate a gene with high sequence similarity to a kinesin as playing a key role in modulating pattern and provides convincing evidence for parallel changes in gene regulation across co-mimetic lineages. The complex genetic architecture at these color pattern loci stands in marked contrast to the single casual mutations often identified in genetic studies of adaptation, but may be more indicative of the type of genetic changes responsible for much of the adaptive variation found in natural populations.
凤蝶翅膀图案的演化提供了一些最引人注目的自然选择适应的例子。控制图案变异的基因是孟德尔效应显著的经典例子，等位基因的变异导致了大而离散的表型变化，并负责整个属的趋同和高度发散的翅膀图案演化。我们描述了两个不连锁的基因组区域的核苷酸变异、基因型-表型关联、连锁不平衡（LD）和候选基因表达模式，这些区域控制着 Heliconius erato 拟态形式的黄色和红色翅膀图案变异。尽管对颜色图案有很强的自然选择，但我们既没有看到遗传多样性的强烈减少，也没有证据表明在任何一个图案间隔中 LD 的扩展。这一观察结果突出了重组可以在自然种群中消除选择的特征，并且与假设一致，即适应性辐射或控制它的等位基因非常古老。然而，在两个图案间隔中，我们发现了几个编码区域中聚集的 SNP，这些 SNP 与颜色图案表型强烈相关。有趣的是，与 SNP 相关的编码区域广泛分离，这表明颜色图案等位基因可能由多个功能位点组成，符合以前对这些基因座作为“超级基因”的描述。对这些区域侧翼基因在 H. erato 和其共拟态种 H. melpomene 中的表达水平的检查表明，一个与驱动蛋白具有高度序列相似性的基因在调节图案方面起着关键作用，并为共拟态谱系中基因调控的平行变化提供了令人信服的证据。这些颜色图案基因座的复杂遗传结构与遗传适应性研究中经常发现的单一偶然突变形成鲜明对比，但可能更能说明导致自然种群中适应性变异的遗传变化类型。
