Models of sex‐allocation conflict are central to evolutionary biology but have mostly assumed static decisions, where resource allocation strategies are constant over colony lifespan. Here, we develop a model to study how the evolution of dynamic resource allocation strategies is affected by the queen‐worker conflict in annual eusocial insects. We demonstrate that the time of dispersal of sexuals affects the sex‐allocation ratio through sexual selection on males. Furthermore, our model provides three predictions that depart from established results of classic static allocation models. First, we find that the queen wins the sex‐allocation conflict, while the workers determine the maximum colony size and colony productivity. Second, male‐biased sex allocation and protandry evolve if sexuals disperse directly after eclosion. Third, when workers are more related to new queens, then the proportional investment into queens is expected to be lower, which results from the interacting effect of sexual selection (selecting for protandry) and sex‐allocation conflict (selecting for earlier switch to producing sexuals). Overall, we find that colony ontogeny crucially affects the outcome of sex‐allocation conflict because of the evolution of distinct colony growth phases, which decouples how queens and workers affect allocation decisions and can result in asymmetric control.
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