Divergence of chemosensing during the early stages of speciation

Divergence of chemosensing during the early stages of speciation
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DOI:
10.1073/pnas.1921318117
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发表时间:
2020-06
影响因子:
11.1
通讯作者:
Bas van Schooten;Bas van Schooten;Jesyka Meléndez-Rosa;S. M. Belleghem;C. Jiggins;J. D. Tan;W. McMillan;Riccardo Papa;Riccardo Papa
Bas van Schooten;Bas van Schooten;Jesyka Meléndez-Rosa;S. M. Belleghem;C. Jiggins;J. D. Tan;W. McMillan;Riccardo Papa;Riccardo Papa
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Bas van Schooten;Bas van Schooten;Jesyka Meléndez-Rosa;S. M. Belleghem;C. Jiggins;J. D. Tan;W. McMillan;Riccardo Papa;Riccardo Papa

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昆虫依靠嗅觉来完成诸如觅食、产卵和择偶等生物过程。虽然大量的实验证据支持化学线索在这些过程中的重要性,但涉及复杂行为反应的化学感觉整合的基因在很大程度上仍然未知。利用差异基因表达和基因流的全基因组信号,我们描述了一对蝴蝶感觉组织的化学感觉表达谱,并鉴定了配偶和寄主植物识别的候选基因。我们发现候选化学感觉基因与颜色模式基因在物理上没有联系。我们的研究结果表明,与Heliconius化学感觉系统和视觉系统相关的基因座的独立进化,都可能介导促进生殖隔离和下游物种形成的行为。化学感觉交流在昆虫生物学中是必不可少的,在寻找配偶、觅食和产卵行为中起着不可或缺的作用。这些特征在物种形成过程中尤为重要,在此过程中,化学感知可能有助于建立物种屏障。然而,识别与这些复杂行为特征相关的基因仍然是一个重大挑战。通过转录组学和基因组学方法的结合,我们对Heliconius melpomene和Heliconius cydno这对幼种蝴蝶的化学感知的遗传结构和化学感知在物种形成过程中的作用进行了表征。我们提供了化学感觉基因表达谱的详细描述,因为它们与感觉组织(触角、腿和口器)、性别(雄性和雌性)和生命阶段(未交配和交配的雌性蝴蝶)有关。我们的研究结果揭示了化学通讯在物种形成过程中建立屏障的潜在作用,并确定了配偶和寄主植物选择行为的强候选基因。在252个化学感觉基因中,HmOBP20(参与挥发性物质检测)和HmGr56(一种假定的辛弗林相关受体)分别成为信息素检测和寄主植物识别的强有力候选基因。这两个基因与翅膀颜色模式位点或其他与视觉配偶偏好相关的基因组区域没有物理联系。总之,我们的研究结果为两种很少杂交的蝴蝶(具有不同的配偶和寄主植物偏好)之间的化学感觉差异提供了证据,这一发现支持了物种边界的多基因结构。
Significance Insects are dependent on olfactory cues to complete biological processes, such as foraging, oviposition, and mate choice. While extensive experimental evidence supports the importance of chemical cues in these processes, genes involved in chemosensory integration of complex behavioral responses remain largely unknown. Using a combination of differential gene expression and genome-wide signals of gene flow, we describe the chemosensory expression profiles of sensory tissues and identify candidate genes for mate and host plant recognition in a pair of Heliconius butterflies. We find that candidate chemosensory genes are physically unlinked from color-pattern genes. Our results suggest the independent evolution of loci associated with the chemosensory and visual systems of Heliconius, both potentially mediating behaviors that promote reproductive isolation and downstream speciation. Chemosensory communication is essential to insect biology, playing indispensable roles during mate-finding, foraging, and oviposition behaviors. These traits are particularly important during speciation, where chemical perception may serve to establish species barriers. However, identifying genes associated with such complex behavioral traits remains a significant challenge. Through a combination of transcriptomic and genomic approaches, we characterize the genetic architecture of chemoperception and the role of chemosensing during speciation for a young species pair of Heliconius butterflies, Heliconius melpomene and Heliconius cydno. We provide a detailed description of chemosensory gene-expression profiles as they relate to sensory tissue (antennae, legs, and mouthparts), sex (male and female), and life stage (unmated and mated female butterflies). Our results untangle the potential role of chemical communication in establishing barriers during speciation and identify strong candidate genes for mate and host plant choice behaviors. Of the 252 chemosensory genes, HmOBP20 (involved in volatile detection) and HmGr56 (a putative synephrine-related receptor) emerge as strong candidates for divergence in pheromone detection and host plant discrimination, respectively. These two genes are not physically linked to wing-color pattern loci or other genomic regions associated with visual mate preference. Altogether, our results provide evidence for chemosensory divergence between H. melpomene and H. cydno, two rarely hybridizing butterflies with distinct mate and host plant preferences, a finding that supports a polygenic architecture of species boundaries.