The Innovation (Jul 2023)
Adaptive evolution to the natural and anthropogenic environment in a global invasive crop pest, the cotton bollworm
- Minghui Jin,
- Henry L. North,
- Yan Peng,
- Hangwei Liu,
- Bo Liu,
- Ruiqing Pan,
- Yan Zhou,
- Weigang Zheng,
- Kaiyu Liu,
- Bo Yang,
- Lei Zhang,
- Qi Xu,
- Samia Elfekih,
- Wendy A. Valencia-Montoya,
- Tom Walsh,
- Peng Cui,
- Yongfeng Zhou,
- Kenneth Wilson,
- Chris Jiggins,
- Kongming Wu,
- Yutao Xiao
Affiliations
- Minghui Jin
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China; The State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, West Yuanmingyuan Road, Beijing 100193, China
- Henry L. North
- Department of Zoology, University of Cambridge, Cambridge CB2 1SZ, UK
- Yan Peng
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China; College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China
- Hangwei Liu
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Bo Liu
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Ruiqing Pan
- Berry Genomics Corporation, Beijing 102200, China
- Yan Zhou
- The State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, West Yuanmingyuan Road, Beijing 100193, China
- Weigang Zheng
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Kaiyu Liu
- Institute of Entomology, School of Life Sciences, Central China Normal University, Wuhan 430079, China
- Bo Yang
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Lei Zhang
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Qi Xu
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Samia Elfekih
- Australian Centre for Disease Preparedness (ACDP), CSIRO Health & Biosecurity, East Geelong, VIC 3169, Australia; Bio21 Institute and the School of Biosciences, The University of Melbourne, Melbourne, VIC 3010, Australia
- Wendy A. Valencia-Montoya
- Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA
- Tom Walsh
- CSIRO Land and Water, Black Mountain Laboratories, Canberra, ACT 2601, Australia
- Peng Cui
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Yongfeng Zhou
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China
- Kenneth Wilson
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China; Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YW, UK
- Chris Jiggins
- Department of Zoology, University of Cambridge, Cambridge CB2 1SZ, UK; Corresponding author
- Kongming Wu
- The State Key Laboratory for Biology of Plant Disease and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, West Yuanmingyuan Road, Beijing 100193, China; Corresponding author
- Yutao Xiao
- Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Gene Editing Technologies (Hainan), Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518116, China; Corresponding author
- Journal volume & issue
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Vol. 4,
no. 4
p. 100454
Abstract
The cotton bollworm, Helicoverpa armigera, is set to become the most economically devastating crop pest in the world, threatening food security and biosafety 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 a previously cryptic population structure. Using a genome-wide association study (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.