Abstract Eusocial insect colonies are vulnerable to exploitation by egg‐laying workers arising either as natal reproductive workers or as non‐natal reproductive ‘drifting’ workers (intraspecific social parasites). Worker egg‐laying is potentially costly to the colony, but queens and workers can counter its costs via egg eating (queen or worker policing). Bumblebee colonies exhibit egg laying by both natal and non‐natal workers: natal workers collectively lay more eggs but do so only after a specific point in the colony cycle, the ‘competition point’, whereas non‐natal workers potentially lay eggs throughout the colony cycle. These features create a special opportunity to investigate whether policing of worker‐laid eggs is context‐dependent (i.e. depends on worker origin of eggs and/or colony stage). We introduced artificial egg cells containing eggs laid by either natal or non‐natal workers into colonies of the bumblebee Bombus terrestris both before and after their competition points and observed the fate of introduced egg cells and eggs. In both colony stages, the majority of introduced egg cells and eggs were policed, demonstrating that policing was not activated only after the competition point. However, in the pre‐competition point stage alone, a smaller proportion of non‐natal workers' eggs (15%) remained after 20 h compared to the proportion of natal workers' eggs remaining (24%). More effective policing of non‐natal workers' eggs early in the colony cycle potentially represents an adaptive, context‐dependent response to the stage in the cycle when all worker‐laid eggs are normally unrelated to the natal colony.
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