The genomic history and global migration of a windborne pest

Author:

Hu Qing-Ling12ORCID,Zhuo Ji-Chong1ORCID,Fang Gang-Qi34ORCID,Lu Jia-Bao1ORCID,Ye Yu-Xuan2ORCID,Li Dan-Ting2ORCID,Lou Yi-Han2ORCID,Zhang Xiao-Ya2,Chen Xuan2,Wang Si-Liang2,Wang Zhe-Chao2ORCID,Zhang Yi-Xiang34,Mazlan Norida5ORCID,OO San San6,Thet Thet6,Sharma Prem Nidhi7,Jauharlina Jauharlina8ORCID,Sukorini Ir Henik9ORCID,Ibisate Michael T.10ORCID,Rahman S.M. Mizanur11ORCID,Ansari Naved Ahmad212ORCID,Chen Ai-Dong13,Zhu Zeng-Rong214,Heong Kong Luen2,Lu Gang1ORCID,Huang Hai-Jian1ORCID,Li Jun-Min1ORCID,Chen Jian-Ping1ORCID,Zhan Shuai34ORCID,Zhang Chuan-Xi12ORCID

Affiliation:

1. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo 315211, China.

2. Institute of Insect Science, Zhejiang University, Hangzhou 310058, China.

3. Key Laboratory of Plant Design, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China.

4. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China.

5. Institute of Tropical Agriculture and Food Security, and Faculty of Agriculture, University Putra Malaysia, 43400 Serdang, Malaysia.

6. Taungoo University, Taungoo 05063, Myanmar.

7. Entomology Division, Nepal Agricultural Research Council, Khumaltar, Lalitpur, Kathmandu 44600, Nepal.

8. Department of Plant Protection, Faculty of Agriculture, Syiah Kuala University, Banda Aceh 23111, Indonesia.

9. Agrotechnology Study Program, Muhammadiyah University of Malang, Malang 65145, Indonesia.

10. College of Agriculture, Forestry and Environmental Sciences, Aklan State University, Banga, Aklan 5601, Philippines.

11. Sher-e-Bangla Agricultural University, Sher-e-Bangla Nagar, Dhaka 1207, Bangladesh.

12. Department of Zoology, Aligarh Muslim University, Aligarh, U.P. 202002, India.

13. Agriculture Environment and Resources Institute, Yunnan Academy of Agricultural Sciences, Kunming 650205, China.

14. Hainan Institute, Zhejiang University, Sanya 572025, China.

Abstract

Many insect pests, including the brown planthopper (BPH), undergo windborne migration that is challenging to observe and track. It remains controversial about their migration patterns and largely unknown regarding the underlying genetic basis. By analyzing 360 whole genomes from around the globe, we clarify the genetic sources of worldwide BPHs and illuminate a landscape of BPH migration showing that East Asian populations perform closed-circuit journeys between Indochina and the Far East, while populations of Malay Archipelago and South Asia undergo one-way migration to Indochina. We further find round-trip migration accelerates population differentiation, with highly diverged regions enriching in a gene desert chromosome that is simultaneously the speciation hotspot between BPH and related species. This study not only shows the power of applying genomic approaches to demystify the migration in windborne migrants but also enhances our understanding of how seasonal movements affect speciation and evolution in insects.

Publisher

American Association for the Advancement of Science (AAAS)

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