Subfamily‐dependent alternative reproductive strategies in worker honeybees

Abstract

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.

Rebel honeybee workers have a tendency to become intraspecific reproductive parasites

“…In contrast to the previously mentioned study (Yagound et al, ), we did not find more ovarioles and more activated ovaries in normal workers that drifted to foreign colonies compared to those that stayed in native colonies, but this result is easy to explain. Previous studies examined large numbers of normal workers and their tendency to migrate, while the total number of normal bees that drifted to other colonies was very low in our experiment (a maximum of 10 individuals in every colony), and this number was probably not sufficiently large to statistically determine the reproductive differences between bees in native and foreign nests, even if this tendency does exist in honeybee colonies.…”

“…Additionally, some studies showed that ovary activation is related to the number of ovarioles (Makert, Paxton, & Hartfelder, ). Thus, the ovary activation in rebel workers collected from foreign colonies might have been higher because these individuals had more ovarioles in the ovary and spend life in alien colony, but we have no evidence to exclude the alternative scenario that rebel workers with more activated ovaries are more likely to drift to other colonies, as suggested by Yagound et al ().…”

“…The same tendency was not found among normal workers collected from different types of colonies. Higher ovary activation in a foreign colony was not surprising results because workers typically have a greater likelihood of ovary activation in a foreign as well as queenless colony (Miller & Ratnieks, ; Yagound et al, ). Additionally, some studies showed that ovary activation is related to the number of ovarioles (Makert, Paxton, & Hartfelder, ).…”

“…The same research also showed that drifting workers had no preference between queenless or queenright colonies (Chapman et al, ), confirming that drift to foreign colonies is the result of mistakes in orientation. However, a different study showed that some individuals with activated ovaries tend to migrate to foreign colonies, with a preference for hopelessly queenless colonies (Yagound, Duncan, Chapman, & Oldroyd, ). Yagound et al () found that the probability to drift depends on both the subfamily of the worker (genetic aspect) and on the social environment, which directly influences the reproductive state of workers.…”

“…However, a different study showed that some individuals with activated ovaries tend to migrate to foreign colonies, with a preference for hopelessly queenless colonies (Yagound, Duncan, Chapman, & Oldroyd, ). Yagound et al () found that the probability to drift depends on both the subfamily of the worker (genetic aspect) and on the social environment, which directly influences the reproductive state of workers. Their study indicates that reproductive parasitism in honeybee workers is fairly common and that individuals with the opportunity to enter an unrelated colony often take advantage of it.…”