Ruyan Li: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen 2100, Denmark. ORCID
Xueqin Dai: Key Laboratory of Genetic Evolution & Animal Models, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China. ORCID
Jixuan Zheng: Centre for Evolutionary and Organismal Biology, Women's Hospital, & Liangzhu Laboratory, School of Medicine, Zhejiang University, Hangzhou 310058, China.
Rasmus Stenbak Larsen: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen 2100, Denmark. ORCID
Yanmei Qi: Key Laboratory of Genetic Evolution & Animal Models, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
Xiafang Zhang: Key Laboratory of Genetic Evolution & Animal Models, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China.
Joel Vizueta: Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen 2100, Denmark.
Jacobus J Boomsma: Centre for Social Evolution, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen 2100, Denmark. ORCID
Weiwei Liu: Key Laboratory of Genetic Evolution & Animal Models, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650201, China. ORCID
Guojie Zhang: Centre for Evolutionary and Organismal Biology, Women's Hospital, & Liangzhu Laboratory, School of Medicine, Zhejiang University, Hangzhou 310058, China. ORCID
Caste differentiation involves many functional traits that diverge during larval growth and metamorphosis to produce adults irreversibly adapted to reproductive division of labor. Investigating developmental differentiation is important for general biological understanding and has increasingly been explored for social phenotypes that diverge in parallel from similar genotypes. Here, we use ants to investigate the extent to which canalized worker development can be shifted toward gyne (virgin-queen) phenotypes by juvenile hormone (JH) treatment. We show that excess JH can activate gyne-biased development in workers so that wing-buds, ocelli, antennal and genital imaginal discs, flight muscles, and gyne-like fat bodies and brains emerge after pupation. However, ovary development remained unresponsive to JH treatment, indicating that JH-sensitive germline sequestration happens well before somatic differentiation. Our findings reveal important qualitative restrictions in the extent to which JH treatment can redirect larval development and that these constraints are independent of body size. Our findings corroborate that JH is a key hormone for inducing caste differentiation but show that this process can be asymmetric for higher colony-level germline somatic caste differentiation in superorganisms as defined a century ago by Wheeler. We quantified gene expression changes in response to JH treatment throughout development and identified a set of JH-sensitive genes responsible for the emergence of gyne-like somatic traits. Our study suggests that the gonadotropic role of JH in ovary maturation has shifted from the individual level in solitary insects to the colony level in an evolutionary-derived and highly polygynous superorganism like the pharaoh ant.
