Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry

Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry
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DOI:
10.1073/pnas.1907068116
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发表时间:
2019-11-26
影响因子:
11.1
通讯作者:
Reed, Robert D.
Reed, Robert D.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Lewis, James J.;Geltman, Rachel C.;Reed, Robert D.

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蝴蝶的颜色模式模仿是通过对几个大效应基因的选择来进行复杂特征适应的经典案例。关联研究已经将颜色模式变异与少数非编码区联系起来,然而控制颜色模式的假定顺式调控元件(CRE)仍然未知。在这里,我们结合染色质分析、DNA序列关联和基因组编辑来从功能上表征颜色模式基因Optix的5个顺式调节元件。我们惊讶地发现Optix的顺式调节结构具有多效性和调节脆弱性,其中单个顺式调节元件的缺失对颜色模式和翼静脉发育都有广泛的影响。值得注意的是,我们发现同源顺式调控元件与远亲漫画的翅膀图案趋同有关,这表明祖先元素的平行共同进化促进了图案模仿。我们的结果支持赫利诺斯的颜色模式演化模型,其中古老的、多功能顺式调节元件的变化是适应性辐射的基础。
Color pattern mimicry in Heliconius butterflies is a classic case study of complex trait adaptation via selection on a few large effect genes. Association studies have linked color pattern variation to a handful of noncoding regions, yet the presumptive cis-regulatory elements (CREs) that control color patterning remain unknown. Here we combine chromatin assays, DNA sequence associations, and genome editing to functionally characterize 5 cis-regulatory elements of the color pattern gene optix. We were surprised to find that the cis-regulatory architecture of optix is characterized by pleiotropy and regulatory fragility, where deletion of individual cis-regulatory elements has broad effects on both color pattern and wing vein development. Remarkably, we found orthologous cis-regulatory elements associate with wing pattern convergence of distantly related comimics, suggesting that parallel coevolution of ancestral elements facilitated pattern mimicry. Our results support a model of color pattern evolution in Heliconius where changes to ancient, multifunctional cis-regulatory elements underlie adaptive radiation.