Unexpected worker mating and colony-founding in a superorganism

Mingsheng Zhuang, Thomas J. Colgan, Yulong Guo, Zhengyi Zhang, Fugang Liu, Zhongyan Xia, Xueyan Dai, Zhihao Zhang, Yuanjian Li, Liuhao Wang, Jin Xu, Yueqin Guo, Yingping Qu, Jun Yao, Huipeng Yang, Fan Yang, Xiaoying Li, Jun Guo, Mark J. F. Brown () and Jilian Li ()
Additional contact information
Mingsheng Zhuang: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Thomas J. Colgan: Johannes Gutenberg University Mainz
Yulong Guo: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Zhengyi Zhang: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Fugang Liu: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Zhongyan Xia: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Xueyan Dai: Shanghai Suosheng Biotechnology Co., Ltd
Zhihao Zhang: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Yuanjian Li: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Liuhao Wang: Henan Institute of Science and Technology
Jin Xu: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Yueqin Guo: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Yingping Qu: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Jun Yao: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Huipeng Yang: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Fan Yang: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Xiaoying Li: Institute of Apicultural Research, Chinese Academy of Agricultural Science
Jun Guo: Kunming University of Science and Technology
Mark J. F. Brown: Royal Holloway University of London
Jilian Li: Institute of Apicultural Research, Chinese Academy of Agricultural Science

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract The emergence of caste-differentiated colonies, which have been defined as ‘superorganisms’, in ants, bees, and wasps represents a major transition in evolution. Lifetime mating commitment by queens, pre-imaginal caste determination and lifetime unmatedness of workers are key features of these animal societies. Workers in superorganismal species like honey bees and many ants have consequently lost, or retain only vestigial spermathecal structures. However, bumble bee workers retain complete spermathecae despite 25-40 million years since their origin of superorganismality, which remains an evolutionary mystery. Here, we show (i) that bumble bee workers retain queen-like reproductive traits, being able to mate and produce colonies, underlain by queen-like gene expression, (ii) the social conditions required for worker mating, and (iii) that these abilities may be selected for by early queen-loss in these annual species. These results challenge the idea of lifetime worker unmatedness in superorganisms, and provide an exciting new tool for the conservation of endangered bumble bee species.

Date: 2023
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DOI: 10.1038/s41467-023-41198-6

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