Adaptive evolution to the natural and anthropogenic environment in a global invasive crop pest, the cotton bollworm

Jin, Minghui and North, Henry L. and Peng, Yan and Liu, Hangwei and liu, Bo and Pan, Ruiqing and Zhou, Yan and Zheng, Weigang and Liu, Kaiyu and Yang, Bo and Zhang, Lei and Xu, Qi and Elfekih, Samia and Montoya, Wendy Valencia and Walsh, Tom and Cui, Peng and Zhou, Yongfeng and Wilson, Kenneth and Jiggins, Chris and Wu, Kongming and Xiao, Yutao (2023) Adaptive evolution to the natural and anthropogenic environment in a global invasive crop pest, the cotton bollworm. The Innovation, 4 (4): 100454. ISSN 2666-6758

Abstract

The cotton bollworm, Helicoverpa armigera, is set to become the most economically devastating crop pest in the world, threatening food security and bio-safety as its range expands across the globe. Key to understanding the eco-evolutionary dynamics of H. armigera, and thus its management, is an understanding of population connectivity and the adaptations that allow the pest to establish in unique environments. We assembled a chromosome-scale reference genome and re-sequenced 503 individuals spanning the species range to delineate global patterns of connectivity, uncovering previously cryptic population structure. Using GWAS and cell line expression of major effect loci, we show that adaptive changes in a temperature- and light-sensitive developmental pathway enable facultative diapause, and that adaptation of trehalose synthesis and transport underlies cold tolerance in extreme environments. Incorporating extensive pesticide resistance monitoring, we also characterize a suite of novel pesticide and Bt resistance alleles under selection in East China. These findings offer avenues for more effective management strategies and provide insight into how insects adapt to variable climatic conditions and newly colonized environments.