Ruling the unruly: Larval passiveness enabled size inequality between ant queens and workers

Building differences between genetically equivalent units is a fundamental challenge for every (super)organism with reproductive division of labor. In ants, reproductive or worker fate is typically determined during the larval stage. However, the methods by which adults feed their larvae, thus controlling their development, vary widely across ant species. Similarly, the body size gap between queen and worker is highly heterogeneous, ranging from species with similar-sized individuals to species with queens over 300 times larger than their smallest workers. To investigate the role of alloparental feeding control in caste dimorphism and the evolution of social complexity, we assembled data for queen:worker dimorphism, alloparental care, and larval morphology for a phylogenetically comprehensive sample of several hundred species, along with ecological and life-history traits. Using comparative phylogenetic methods, we analyzed the macroevolution of ant larvae and queen:worker dimorphism on a large scale. Our findings indicate that both extended alloparental feeding care and dimorphism are associated with the evolution of passive larval morphologies. Furthermore, greater queen:worker dimorphism co-evolved with several traits indicative of social complexity, including larger colony sizes, distinct worker subcastes, and the loss of full reproductive potential in workers. In sum, change in larval feeding habits were promoted by dietary shifts from prey to foods necessitating individualized distribution. These innovations granted adults greater capacity to manipulate larval nutrition, and consequently, caste size inequality, with significant implications for social complexity. Significance statementAnts are among the rare organisms to have extended reproductive division labor beyond the cells of a multicellular organism. However, the degree of specialization between reproductive and worker castes varies considerably between ant lineages. In this study, we demonstrate that strong caste dimorphism in ants co-evolved with complex eusociality traits, and this strong caste dimorphism was achieved by asserting adult control over larvae development. We conclude that this enhanced control over larval caste fate was a critical junction in the major evolutionary transition of ants toward caste specialization. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=125 SRC="FIGDIR/small/519655v2_ufig1.gif" ALT="Figure 1"> View larger version (21K): org.highwire.dtl.DTLVardef@9347dborg.highwire.dtl.DTLVardef@1528464org.highwire.dtl.DTLVardef@71c2f0org.highwire.dtl.DTLVardef@b52a2d_HPS_FORMAT_FIGEXP M_FIG C_FIG