Unexpected worker mating and colony-founding in a superorganism

• Published in: Nature communications Vol. 14; no. 1; p. 5499
• Main Authors: Zhuang, Mingsheng, Colgan, Thomas J., Guo, Yulong, Zhang, Zhengyi, Liu, Fugang, Xia, Zhongyan, Dai, Xueyan, Zhang, Zhihao, Li, Yuanjian, Wang, Liuhao, Xu, Jin, Guo, Yueqin, Qu, Yingping, Yao, Jun, Yang, Huipeng, Yang, Fan, Li, Xiaoying, Guo, Jun, Brown, Mark J. F., Li, Jilian
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 07.09.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 45; 45/91; 631/158/856; 631/181/2469; 631/601/1466; 631/601/18; Ants; Apidae; Bees; Bombus; Caste determination; Colonies; Endangered species; Gene expression; Honey; Humanities and Social Sciences; Insects; multidisciplinary; Queens; Science; Science (multidisciplinary); Social conditions; Wildlife conservation; Workers (insect caste)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-41198-6

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. Workers in social insects such as honey bees, bumble bees, and ants are expected to spend their lives helping their mother reproduce. Here the authors show that workers of several bumble bee species can in fact mate and lead colonies of their own.