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

Abstract

Efficient pest management requires comprehensive knowledge of its biology, ecology, and evolution, particularly adaptation that exacerbating pest damage. Helicoverpa armigera (Hubner) 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 was less investigated. Here, we analyzed genomic variation of Helicoverpa armigera in 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, cyr2 and daywake), insulin secretion (IGF2BP2) and energy metabolism (SLC25A25, CCG7766, D11DS, TSTP and CPQ) 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 harboring alien alleles of two clock genes (period and cycle) and may have disrupted clock oscillator for adaptation. 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 to Bacillus thuringiensis protein in Oceanian populations, are lineage-specific. Our results highlight the importance of investigating local adaptation in effective pest control under globalization of agriculture.