Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade.

Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade.
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DOI:
10.1371/journal.pgen.1000794
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发表时间:
2010-02-05
期刊:
影响因子:
4.5
通讯作者:
Jiggins CD
Jiggins CD
中科院分区:
生物学2区
文献类型:
--
作者:
Baxter SW;Nadeau NJ;Maroja LS;Wilkinson P;Counterman BA;Dawson A;Beltran M;Perez-Espona S;Chamberlain N;Ferguson L;Clark R;Davidson C;Glithero R;Mallet J;McMillan WO;Kronforst M;Joron M;Ffrench-Constant RH;Jiggins CD

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蝴蝶的翅膀图案是一个长期存在的<s:1>勒勒模仿和强自然选择下的表型辐射的例子。控制这些模式的位点是适应性进化的“热点”,在属中不同物种之间具有巨大的等位基因多样性。研究人员分析了Heliconius melpomene及其近亲的核苷酸变异、基因型-表型关联、连锁不平衡以及两个位点和多个杂交带的候选基因表达。HmB的等位基因控制红色前翼带的存在与否,而HmYb的等位基因控制黄色后翼带的存在与否。在HmYb中,相隔约100 kb的两个区域显示出显着的基因型-表型关联,这些关联在独立的杂交区中被复制。相比之下,在HmB中,单个关联峰表示三个基因的功能位点可能的位置,编码一个激酶、一个g蛋白偶联受体和一个mRNA剪接因子。在HmYb和HmB中,有证据表明,在相隔高达14 kb的相关位点之间,连锁不平衡(LD)增强,这表明多个位点正在进行选择。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性扫描,与这些等位基因相对古老一致。在显示与HmB位点相关的三个基因中,运动蛋白显示了在共同模仿者(Heliconius erato)中复制的种族之间翼盘表达的差异,这为<s:1>勒氏共模仿者(lererian co-mimics)之间基因表达的平行变化提供了显著证据。因此,Heliconius melpomene的翅膀图案位点显示了一种通过选择维持的单倍型结构,但没有证据表明最近的选择性扫描。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,但可能为数百万年而不是几十年出现的自然种群中的大多数适应性提供更好的模型。蝴蝶翅膀图案的多样性是一个长期存在的<s:1>勒勒模仿和适应性辐射的例子。控制这种模式的遗传区域是适应性进化的“热点”,基因组的小区域控制着翅膀模式的主要变化。在多个杂交带中,我们没有发现较强的种群近期选择信号。尽管如此,我们在多个位点发现了遗传变异和翼型之间的显著关联。这表明模式等位基因是相对古老的,与最近人类诱导的选择(如农药抗性)的简单遗传基础相比,它可能是大多数自然适应的更好模型。引人注目的是,在控制红色前翼带的区域,与表型的强烈关联暗示有三个基因可能参与控制翅膀的模式。其中一种运动蛋白基因,在两种模拟物种的不同形式之间表现出平行的表达水平差异,使其成为控制翅膀图案的强有力的候选者。这些结果表明,模仿涉及基因表达的平行变化,并强烈提示该基因在控制翅膀图案中的作用。
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 ∼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. The diversity of wing patterns in Heliconius butterflies is a longstanding example of both Müllerian mimicry and adaptive radiation. The genetic regions controlling such patterns are “hotspots” for adaptive evolution, with small regions of the genome controlling major changes in wing pattern. Across multiple hybrid zones in Heliconius melpomene and related species, we no find no strong population signal of recent selection. Nonetheless, we find significant associations between genetic variation and wing pattern at multiple sites. This suggests patterning alleles are relatively old, and might be a better model for most natural adaptation, in contrast to the simple genetic basis of recent human-induced selection such as pesticide resistance. Strikingly, across the region controlling the red forewing band, a very strong association with phenotype implicates three genes as potentially being involved in control of wing pattern. One of these, a kinesin gene, shows parallel differences in expression levels between divergent forms in the two mimetic species, making it a strong candidate for control of wing pattern. These results show that mimicry involves parallel changes in gene expression and strongly suggest a role for this gene in control of wing pattern.
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