Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths

Adaptive Introgression across Semipermeable Species Boundaries between Local Helicoverpa zea and Invasive Helicoverpa armigera Moths
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DOI:
10.1093/molbev/msaa108
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发表时间:
2019-12
影响因子:
10.7
通讯作者:
Wendy A. Valencia-Montoya;S. Elfekih;Henry L. North;Joana I. Meier;I. Warren;W. T. Tay;K. Gordon;A. Specht;S. Paula-Moraes;R. Rane;T. Walsh;C. Jiggins
Wendy A. Valencia-Montoya;S. Elfekih;Henry L. North;Joana I. Meier;I. Warren;W. T. Tay;K. Gordon;A. Specht;S. Paula-Moraes;R. Rane;T. Walsh;C. Jiggins
中科院分区:
生物学1区
文献类型:
--
作者:
Wendy A. Valencia-Montoya;S. Elfekih;Henry L. North;Joana I. Meier;I. Warren;W. T. Tay;K. Gordon;A. Specht;S. Paula-Moraes;R. Rane;T. Walsh;C. Jiggins

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由于气候变化、适宜农业生态系统的发展和人为扩散,物种范围转移和虫害爆发急剧增加,入侵物种与本地物种之间的杂交引起了全球关注。然而,本地物种和入侵物种亲缘间的二次接触提供了一个自然实验室来了解决定物种渗入和物种屏障维持或丧失的因素。在这里,我们描述了巴西入侵棉铃虫和玉米蚜二次接触后的早期进化结果。我们在两个时间样本中对来自巴西的Helicoverpa蛾进行了全基因组重测序:2013年棉蚜爆发期间和2017年较近的种群。有证据表明,与2013年棉蚜的扩张相吻合的是,当地玉米蚜发生了一次杂交,并广泛渗入入侵棉蚜。然而,在2013年至2017年期间,在棉铃虫中,混合比例减少,表明杂交率下降。最近的种群也显示出较短的渐渗轨迹,这表明选择反对混合。与全基因组模式相反,有惊人的证据表明,包括杀虫剂抗性等位基因在内的单个区域从入侵的棉铃虫渗入到当地的玉米玉米,这种渗入的频率随着时间的推移而增加,但定位在基因组内。综上所述,尽管二次接触后存在广泛的基因流动,但除了含有抗虫基因座的单一渐渗区域外,物种边界基本上保持不变。我们记录了一种入侵物种的最坏情况,即现在有两种害虫而不是一种,并且本地物种通过渗入和杂交获得了对拟除虫菊酯杀虫剂的抗性,这对未来种群扩展和从新的入侵棉蚜种群引入新的抗性基因的害虫管理具有重要意义。次要接触发生在地理上不重叠的亲缘物种重新结合的时候。由于物种在其原生范围之外的人为移动,导致二次接触的情况增加,通常导致入侵物种在新环境中成功传播并稳定下来。这就是棉铃虫的情况。棉铃虫是旧大陆的一种主要的农业害虫,最近入侵了美洲,在那里它与它最近的亲戚棉铃虫团聚了。虽然一些作者报道了杂交,并假设可能出现新的生态型和抗杀虫剂基因的交换,但这些结果尚未得到测试。我们通过对巴西这两个物种的个体进行测序来检验这些结果,这些个体是在2013年报告了阿米格蚜暴发后收集的,以及在2017年收集的。我们发现,尽管杂交,这些蛾子并没有崩溃成一个单一的物种,也没有形成新的生态型,而且物种的独特性是通过对大多数外来基因型的选择而保持的。然而,我们发现杂交介导了棉蚜对拟除虫菊酯抗性基因的快速获取。在本研究覆盖的时间间隔内,这两个物种的总体种群数量下降意味着我们的结果可能反映了入侵后早期杂交事件的后果,尽管可能通过南美大陆的贸易持续引入了棉铃虫的遗传多样性。我们的研究结果提供了一个罕见的入侵后变异适应性转移的例子,并阐明了玉米玉米对杀虫剂抗性进化的动力学。
Hybridization between invasive and native species has raised global concern given the dramatic increase in species range shifts and pest outbreaks due to climate change, development of suitable agroecosystems, and anthropogenic dispersal. Nevertheless, secondary contact between sister lineages of local and invasive species provides a natural laboratory to understand the factors that determine introgression and the maintenance or loss of species barriers. Here, we characterize the early evolutionary outcomes following secondary contact between invasive Helicoverpa armigera and H. zea in Brazil. We carried out whole-genome resequencing of Helicoverpa moths from Brazil in two temporal samples: during the outbreak of H. armigera in 2013, and more recent populations from 2017. There is evidence for a burst of hybridization and widespread introgression from local H. zea into invasive H. armigera coinciding with H. armigera expansion in 2013. However, in H. armigera, admixture proportions were reduced between 2013 and 2017, indicating a decline in hybridization rates. Recent populations also showed shorter introgressed tracks suggesting selection against admixture. In contrast to the genome-wide pattern, there was striking evidence for introgression of a single region including an insecticide-resistance allele from the invasive H. armigera into local H. zea, which increased in frequency over time but was localized within the genome. In summary, despite extensive gene-flow after secondary contact, the species boundaries are largely maintained except for the single introgressed region containing the insecticide-resistant locus. We document the worst-case scenario for an invasive species, in which there are now two pest species instead of one, and the native species has acquired resistance to pyrethroid insecticides through introgression and hybridization, with significant implications for pest management in future population expansions and introductions of novel resistance genes from new invasive H. armigera populations. Author summary Secondary contact occurs when related species with non-overlapping ranges are geographically reunited. Scenarios of secondary contact have increased due to anthropogenic movement of species outside of their native range, often resulting in invasive species that successfully spread and stabilised in the new environment. This is the case for Helicoverpa armigera, a major agricultural pest in the Old World that has recently invaded the Americas, where it reunited with its closest relative, H. zea. While some authors reported hybridisation, and hypothesised about the potential emergence of novel ecotypes and the exchange of pesticide-resistant genes, these outcomes have not been tested yet. We examine these outcomes by sequencing individuals from both species in Brazil, collected in 2013 after outbreaks of H. armigera were reported, and individuals collected during 2017. We discovered that despite hybridisation, these moths have not collapsed into a single species nor formed new ecotypes, and that the species distinctiveness is maintained through selection against most of the foreign genotypes that cross species boundaries. However, we found that hybridisation mediated the rapid acquisition of a H. armigera gene conferring resistance to pyrethroids by H. zea. The overall decline in populations of both species during the interval covered by this study means that our results are likely to reflect the consequences of hybridization events early after invasion, despite the likely ongoing introduction of H. armigera genetic diversity through trade across the South American continent. Our results provide a rare example of adaptive transferral of variation right after invasion and elucidate the dynamics of insecticide resistance evolution in H. zea.