Conflict resolution and direct benefits in kin-selected conflicts in social groups

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences


Kin selection theory is the leading theory for explaining the evolution of social behaviour in organisms. The theory is based on the application of natural selection theory to the genes that influence social behaviour, where social behaviour includes both cooperation and conflict. It proposes that individuals value one another in proportion to their genetic relatedness, since relatedness measures the chance they share the genes influencing the social behaviour. Because of its fundamental basis, and the need to explain the complexity of animal sociality, investigating kin selection is of major interest to evolutionary ecologists. The theory has proved very successful in explaining social phenomena in some respects, but not in others. Two general reasons for the failures of the theory have been proposed. The first is that social interactions are resolved by as-yet poorly-investigated aspects of the theory, namely, in social conflicts, the relative power held by different sets of individuals, and/or the overall costs to the social group of conflict behaviour. The second explanation is that individuals' social behaviour is driven by direct benefits (gains from personal reproduction), not kin-selected benefits. We propose to test both these ideas using the bumble bee Bombus terrestris as our study organism. In the social Hymenoptera (ants, bees and wasps), kin selection predicts that either queens or workers (which, if reproductive, produce only sons) should monopolise the production of adult male offspring, depending on the relatedness structure of the colony. But the actual level of worker reproduction is often far lower than that predicted. This is the case in B. terrestris. In this species, the theory predicts that workers should produce most of the adult males, but our data show that in fact they produce only c. 5%. We propose to test two hypotheses for the lack of fit between male parentage data and predictions of kin selection theory in B. terrestris. The hypotheses stem, respectively, from the ideas of conflict resolution (through the unequal distribution of power) and direct benefits. They are: (1) most worker-laid eggs are selectively destroyed by the queen or by other workers, with which power over male parentage largely lies; and (2) worker reproduction is not determined by the relatedness of workers to nestmates, as kin selection theory proposes, but is instead a by-product of workers' capacity for intraspecific social parasitism. These hypotheses arise from two sets of observations. The first is that worker-laid eggs in B. terrestris are frequently eaten by the queen or other workers, although the extent of this has never been quantified. The second is our recent discovery that B. terrestris workers enter other colonies of their own species in which they then produce sons as reproductive 'drifters' (intraspecific social parasites). We will test Hypothesis 1 by using observations, experimentation and genetic parentage analyses (based on microsatellite markers) to determine whether the major consumers of worker-laid eggs in B. terrestris are the queen, reproductive workers, or workers as a whole. We will test Hypothesis 2 by using the same techniques to determine whether colonies with the most reproduction by resident workers are those exporting the most reproductive drifter workers, and/or whether reproductive drifters are losers in dominance battles with resident workers. We will also measure the frequency of reproductive drifter workers in field colonies and effects of nest aggregation on drifting behaviour. Our planned work is novel because it addresses new phenomena and unanswered research questions. Its impact will be broad because of the fundamental nature of the research, widespread interest in social evolution, and the possibility that the results will cause a reassessment of long-standing concepts. It should advance considerably our understanding of the evolutionary ecology of social behaviour.


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ZANETTE L (2014) Bumble bee workers drift to conspecific nests at field scales in Ecological Entomology

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Zanette LR (2012) Reproductive conflict in bumblebees and the evolution of worker policing. in Evolution; international journal of organic evolution

Description The aims of the research were to test aspects of kin selection theory, which is the leading theory for explaining the evolution of social behaviour in organisms. The theory proposes that individuals act towards one another as if they valued them according to their genetic relatedness (level of kinship). Kin selection theory has been successful in explaining many aspects of the biology of social species, including the social Hymenoptera (ants, bees and wasps). However, in the bumble bee Bombus terrestris, the theory predicts that workers, being more closely related to worker-produced males than to queen-produced ones, should produce most of the colony's males, which is not found. Our research was designed to investigate why not, so potentially expanding our understanding of social evolution in general.

We tested two hypotheses. The first was that workers fail to produce as many adult sons as expected because they are prevented from doing so ('policed') by the colony queen or other workers. The second was that workers are less reproductive in their natal colony than expected because some workers take the option of entering other colonies of the same species (as so-called 'drifter' workers) and producing their own offspring inside them. We tested the two hypotheses using a mixture of observation and experiment in the laboratory and field, along with genetic parentage analyses using microsatellite DNA markers.

The results confirmed the first hypothesis. We found that, once workers had started laying eggs, they collectively accounted for almost 70% of them. But most worker-laid eggs (93%) were then eaten, even though we showed experimentally that they had the same viability as the queen's eggs. This caused the expected frequency of adult worker-produced males to be low (13%), matching the frequency measured by our genetic analyses of the study colonies (14%) very closely. Workers' eggs were eaten by the queen (49% of eggs), reproductive workers (23%) and non- reproductive workers (28%). Overall, therefore, B. terrestris exhibits a mixture of queen policing, 'corrupt' policing (i.e. policing by reproductive workers) and collective worker policing (i.e. by the mass of non-reproductive workers), resolving the conflict over worker egg-laying largely in favour of queens. However, while queens are more related to their sons than to the workers', it is not clear why workers do not eat the queen's eggs or why non-reproductive workers eat eggs laid by other workers, and these findings need investigating in future.

The results also confirmed the second hypothesis. In eight wild-caught B. terrestris colonies collected from the field, our genetic analyses showed that a small fraction (3%) of workers originated from colonies other than those in which they were found. In an experiment with nests of marked workers placed outside, we found that workers flew up to 60m to enter other nests. Therefore, as expected if workers can act as intraspecific social parasites, workers occurred in foreign nests in nature and were shown to visit and enter them over field scales. Although we did not find evidence that drifted workers in wild nests had produced sons, suggesting drifter B. terrestris workers do so only rarely, this has recently been reported by another group of researchers in a different bumble bee species from Japan.

As well as confirming our two hypotheses, our findings have two broader implications. One is to suggest a pathway whereby collective worker policing, a major mechanism for resolving conflicts over reproduction in social evolution, may have arisen. The other, given that workers in wild populations almost certainly fly large distances to enter other nests, is to alter our view of how bees transport key materials (pollen, pathogens) around landscapes, with important consequences for understanding pollination and the spread of diseases in wild bees.
Exploitation Route The results regarding worker movement should inform pollinator conservation efforts.
Sectors Environment