When a queen dies, unrelated workers seize the chance to move into her nest and lay their own eggs.
The queen of a honeybee colony has a reproductive monopoly because her workers' ovaries are normally inactive and any eggs that they do lay are eaten by their fellow workers1,2,3. But if a colony becomes queenless, the workers start to lay eggs, stop policing2 and rear a last batch of males before the colony finally dies out4. Here we show that workers of the Asian dwarf red honeybee Apis florea from other colonies exploit this interval as an opportunity to move in and lay their own eggs while no policing is in force. Such parasitism of queenless colonies does not occur in the western honeybee A. mellifera and may be facilitated by the accessibility of A. florea nests, which are built out in the open.
Apis florea are small honeybees that nest by building a single comb attached to a twig (Fig. 1). We collected four wild A. florea nests (one in 2003 and three in 2004) and transported them to a different location that hosts many wild A. florea colonies, tying them on to low tree branches at least 5 m away from any other nest. After taking a sample of workers, we removed the queens from the translocated colonies and also any queen cells that subsequently developed. We sampled adult workers after one week and again after four weeks (pooled data are shown in Table 1). Samples of worker-produced eggs, larvae and pupae were collected as they appeared in the combs (but not for colonies 3 and 4, as these absconded before larvae were reared). We dissected the adult workers to determine their ovary activation3 and used analysis of DNA microsatellite loci to determine their parentage and that of worker-produced males3. (For details, see supplementary information.)
Before the queen was removed, the number of unrelated (non-natal) workers in the colony was low (averaging 2.0%; Table 1) and none of these workers had activated ovaries. After queen removal, however, the proportion of non-natal workers rose significantly (P=0.008) to 4.5%. Significantly more (P<0.001) non-natal workers (42.6%) had activated ovaries than did natal workers (17.7%), indicating that parasitic workers may actively seek out queenless colonies in order to lay eggs. Moreover, non-natal workers had significantly higher reproductive success (P<0.001) than natal workers: 3.2% of workers in colonies 1 and 2 were non-natal, but these laid 35.6% of the eggs and 22.5% of the pupae.
These results show that an important reproductive tactic of A. florea workers is actively to seek out and parasitize queenless nests with their eggs. This behaviour is not evident in the western honeybee, A. mellifera, in which the offspring of non-natal workers are rare or absent in queenless nests5. Our findings could also explain why queenless dwarf-bee colonies often abscond from their nests: these workers opt to join new, unrelated nests and parasitize them with their eggs. Even workers from A. florea colonies that have a queen may choose to parasitize queenless nests, perhaps because they favour individual reproduction in a queenless nest over contributing to the reproductive output of their own colony.
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The authors declare no competing financial interests.
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Nanork, P., Paar, J., Chapman, N. et al. Asian honeybees parasitize the future dead. Nature 437, 829 (2005). https://doi.org/10.1038/437829a
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