Abstract

During social evolution, life-history traits not only diverged, with social insect queens becoming highly fecund and long-lived compared to their sterile workers, but also individual traits lost their importance compared to colony-level traits. In solitary animals, fecundity is largely influenced by female size, whereas in eusocial insects, colony size and queen number can affect the egg-laying rate. Here we focussed on the ant Temnothorax rugatulus, which exhibits two queen morphs varying in size and reproductive strategy, correlating with their colony's social organization. We experimentally tested the influence of social structure, colony and body size on queen fecundity and investigated links between body size, metabolic rate and survival under paraquat-induced oxidative stress. To gain insights into the molecular physiology underlying the alternative reproductive strategies, we analysed fat body transcriptomes. Per-queen egg production was lower in polygynous colonies when fecundity was limited by worker care. Colony size was a determinant of fecundity rather than body size or queen number, highlighting the super-organismal properties of these societies. The smaller microgynes were more frequently fed by workers and exhibited an increase in metabolic activity, yet they were similarly resistant to oxidative stress. Small queens differentially expressed metabolic genes in the fat body indicating that shifts in molecular physiology and resource availability allow microgyne queens to compensate their small size with a more active metabolism without paying increased mortality costs. We provide novel insights into how life-history traits and their associations were modified during social evolution and adapted to queen reproductive strategies.