Zhejiang Tiantong Forest Ecosystem National Observation and Research Station, Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration, School of Ecological and Environmental Sciences, East China Normal University, Shanghai, China.
Shanghai Institute of Pollution Control and Ecological Security, Shanghai, China.
BGI Genomics, BGI-Shenzhen, Shenzhen, China.
Agriculture and Environment Department, Harper Adams University, Newport, UK.
CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China.
Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianyang, China.
INRAE, UMR 1062 CBGP, Montferrier-sur-Lez, France.
College of Life Sciences, Northwest University, Xi'an, China.
Department of Biological and Marine Science, University of Hull, Hull, UK.
CEFE, CNRS, University of Montpellier, Paul Valéry University Montpellier, EPHE, IRD, Montpellier, France.
School of Life Sciences, East China Normal University, Shanghai, China.
Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.
School of Life Sciences, Guangzhou University, Guangzhou, China.
Department of Biology, University of Maryland, College Park, MD, USA.
Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.
Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen, China.
Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China. yuhui@scib.ac.cn.
School of Life Sciences, Qufu Normal University, Qufu, China. yuhui@scib.ac.cn.
School of Biology, University of Leeds, Leeds, UK. S.G.A.Compton@leeds.ac.uk.
Zhejiang Tiantong Forest Ecosystem National Observation and Research Station, Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration, School of Ecological and Environmental Sciences, East China Normal University, Shanghai, China. xychen@des.ecnu.edu.cn.
Shanghai Institute of Pollution Control and Ecological Security, Shanghai, China. xychen@des.ecnu.edu.cn.
Many insects metamorphose from antagonistic larvae into mutualistic adult pollinators, with reciprocal adaptation leading to specialized insect-plant associations. It remains unknown how such interactions are established at molecular level. Here we assemble high-quality genomes of a fig species, Ficus pumila var. pumila, and its specific pollinating wasp, Wiebesia pumilae. We combine multi-omics with validation experiments to reveal molecular mechanisms underlying this specialized interaction. In the plant, we identify the specific compound attracting pollinators and validate the function of several key genes regulating its biosynthesis. In the pollinator, we find a highly reduced number of odorant-binding protein genes and an odorant-binding protein mainly binding the attractant. During antagonistic interaction, we find similar chemical profiles and turnovers throughout the development of galled ovules and seeds, and a significant contraction of detoxification-related gene families in the pollinator. Our study identifies some key genes bridging coevolved mutualists, establishing expectations for more diffuse insect-pollinator systems.