Sweat bee workers that could start their own nests – but don’t

Miriam Richards, Associate Editor, Insectes Sociaux

In a recent issue of Insectes Sociaux, we described a rather surprising example of behavioural flexibility in an obligately eusocial sweat bee, Halictus ligatus (Rehan et al. 2013). This is a particularly well studied species that has been the subject of hundreds and hundreds of hours of behavioural observations. As in many eusocial sweat bees, there is considerable evidence in H. ligatus for queen-worker conflict over oviposition rights in Brood 2, a conflict that often results in queen domination, if not monopolization, of Brood 2 egg-laying. Many H. ligatus queens appear to be multiply mated, so relatedness of workers to queen-produced brood is low enough to suggest that workers might often achieve higher fitness through personal reproduction rather than by raising siblings (Richards et al. 1995). Why don’t workers that are bullied by queens and which can’t lay eggs in the natal nest simply leave and raise their own brood somewhere? The lack of any evidence that H. ligatus workers ever start their own nests suggested that they were not capable of doing so, although the reasons why not remained mysterious.[1]

We now know that H. ligatus workers can found their own nests, but only under very specific circumstances (Rehan et al. 2013). This was an unexpected discovery during the course of a summer’s fieldwork on several species of social sweat bees nesting in a huge dirt pile created in the course of university landscaping activities. Knowing the dirt pile was likely to be disturbed again as soil was added and removed by the gardeners, we observed and excavated sweat bee nests throughout the summer. In early July, around the time that workers first emerge from their nests to provision Brood 2, little black wasps in the genus Astata, suddenly began nesting activities right amongst the H. ligatus nests. Their digging activities so severely disrupted sweat bee burrows that newly emerged workers returning from their first foraging trips were unable to find relocate their nests. Some of these workers responded to the loss of their natal burrows by founding new burrows. In so doing, their behaviour perfectly recapitulated the behaviour of spring foundresses – they dug tunnels, excavated brood cells, then provisioned them and laid eggs. In a separate paper, we also discovered evidence for queen renesting in the face of the wasp disruptions: one or two nests appeared to have been so damaged by the wasps, that the queens lost contact with their workers and were forced to provision Brood 2 themselves (Richards et al. 2015). Years ago, I saw the same thing happen when H. ligatus queens nesting in excessively wet soil lost their worker broods to rot.

So, these observations demonstrate that H. ligatus workers can found their own nests and raise their own brood, and yet, they only do so in response to complete loss of contact with their natal nests and nestmates. That workers can establish their own nests reinforces the conclusion that workers are totipotent, potentially capable of expressing both normal worker behaviour and behaviour more typical of queens. On the other hand, it suggests that there are limits to behavioural flexibility, as mid-summer nest-founding would seem to be possible only in response to orphaning, but not as a means of evading aggression and manipulation by queens. Similarly, queens only forage in mid-summer if none of their workers survive to adulthood – the emergence of even a single worker results in queen behaviour by the foundress (sometimes with the result that the queen works her single helper to death in a very short time).

Halictus ligatus is not the only eusocial sweat bee in which nests are founded in mid-summer, but the phenomenon seems to be quite rare. To date, only in one study of Lasioglossum baleicum, has there been a comparison of rates of brood production in spring vs, summer-founded nests. As it turns out, workers that founded their own nests and raised brood solitarily had lower inclusive fitness than those that remained as helpers in the natal nest (Yagi and Hasegawa 2012). However, the high frequency of worker nest-founding in the L. baleicum study suggests that even if worker altruism in the natal nest is a better strategy for workers than founding their own nests, the latter could still be adaptive as a conditional response environmental insult that deprives workers of opportunities to increase inclusive fitness through helping.

Mid-summer nest-founding in H. ligatus and other social species reflects a previously unappreciated ability of female sweat bees to renest in the face of devastating and unpredictable damage to their nests. With the advantage of hindsight, perhaps renesting ability should not be surprising – sweat bees are well known for their preference for nesting in disturbed habitats where their nests are likely often to be trampled by animals or damaged by rain or erosion. In fact, the nesting aggregation where we did this work was colonized soon after the soil was dumped and lasted only a few years until grass and thistles covered the ground, discouraging bees from establishing new nests. Perhaps our surprise just reflects the fact that even those of us who spend a lot of time with these interesting little bees tend to under-estimate their ability to adapt to an unpredictable environment.

[1] Indeed, this question was asked repeatedly at my PhD defense by an eminent insect physiologist who was apparently quite irritated by my suggestion that sweat bee queens aggressively force workers to remain in the natal nest as helpers, preventing them from laying their own eggs. He asked rather pointedly (and repeatedly) why the bullied workers didn’t just leave the nest. Eventually, the social psychologist on the examining committee got quite annoyed and pointed out the similarity between bullied workers and abused women who also don’t leave aggressive spouses – not to mention the similar attitudes of onlookers who wonder why the women don’t just leave.   The argument between my examiners continued to escalate until George Eickwort, also an eminent entomologist and expert on social sweat bees, intervened and agreed with me. The eminent physiologist remained highly skeptical (and rather grumpy), but at least my thesis defense was not completely derailed!

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