Adaptive introgression across semipermeable species boundaries between localHelicoverpa zeaand invasiveHelicoverpa armigeramoths

AbstractHybridization 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 invasiveHelicoverpa armigeraandH. zeain Brazil. We carried out whole-genome resequencing ofHelicoverpamoths from Brazil in two temporal samples: during the outbreak ofH. armigerain 2013, and more recent populations from 2017. There is evidence for a burst of hybridization and widespread introgression from localH. zeainto invasiveH. armigeracoinciding withH. armigeraexpansion in 2013. However, inH. 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 invasiveH. armigerainto localH. 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 invasiveH. armigerapopulations.Author summarySecondary 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 forHelicoverpa 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 ofH. armigerawere 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 aH. armigeragene conferring resistance to pyrethroids byH. 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 ofH. armigeragenetic 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 inH. zea.