Characterization of Z chromosomal inversion and lineage-specific sweeps reveal widespread local adaptation inHelicoverpa armigera

Abstract

AbstractEfficient pest management requires comprehensive knowledge of its biology, ecology, and evolution, particularly adaptation that exacerbating pest damage.Helicoverpa armigera(Hübner) is a notorious pest that attacks more than 200 species, adapts to diverse environments, and has developed resistance to almost all applied insecticides. However, local adaptation of this species especially acclimatization was less investigated. Here, we analyzed genomic variation ofHelicoverpa armigerain China and Oceania to identify adaptative loci in different lineages. Despite intensive gene flow, two differentiated Z chromosomal lineages in Central China (i.e., northern and southern lineages) were formed by chromosome inversion and local adaptation. Based on population genomic analysis, we identified genes related to circadian clock (period,cycle,cyr2anddaywake), insulin secretion (IGF2BP2) and energy metabolism (SLC25A25,CCG7766,D11DS,TSTPandCPQ) were under selection in northern lineage. These genes may have contributed to its adaptation to high latitudes. In the southern lineage however, the Z chromosome inversion harbours alleles of two clock genes (periodandcycle) introgressed from Oceanian lineage (H. a. conferta) and may have disrupted clock oscillator for acclimatization. We further conducted selective sweep analysis in lineages from Northwestern China, Central China, and Oceania, and found several insecticide resistant genes that shared among different lineages were likely contributed by introgression. Nevertheless, many candidates, including a cadherin that involved in resistance toBacillus thuringiensisprotein in Oceanian populations, are lineage-specific. Our results highlight the importance of investigating local adaptation in effective pest control under globalization of agriculture.