Unrelated helpers in social wasps

Lead Research Organisation: University of Sussex
Department Name: Sch of Life Sciences

Abstract

The evolution of sociality is one of the major transitions in evolutionary biology. The key testing-grounds for theories concerning the origin of helping are primitively eusocial taxa in which the option of independent reproduction still exists. Social groups of Polistes paper wasps comprise groups of females in which one 'dominant' female lays most or all of the eggs while the others ( 'helpers') forage to feed the dominant's larvae. Yet despite Polistes being the best studied primitively eusocial system, it remains unclear why many females choose to become helpers rather than build their own nests and reproduce independently. Especially paradoxical are populations of P. dominulus, in which >30% of helpers are unrelated to the dominant egg-layer in the group. Unrelated helpers cannot transmit their genes indirectly by rearing offspring of the dominant (kin selection), and so must attempt to obtain direct fitness by laying eggs themselves. The proposed research will use a combination of large-scale field experiments and genetic work to investigate the reproductive strategies of unrelated females in a Spanish population of P. dominulus. The work will: (1) Estimate the reproductive success of unrelated foundresses, focussing particularly on reproduction through inheritance of the egg-laying position, a route that has been strikingly neglected in previous studies of primitively eusocial insects. (2) Separate the effects of kin selection and direct fitness benefits by comparing unrelated helpers with helpers that are sisters of the dominant in terms of: (i) helping effort; (ii) position in the queue to inherit the dominant egg-laying position; (iii) aggression in unmanipulated colonies; (iv) aggression at the critical moment when the dominant is replaced. The overall result will be the most comprehensive evaluation of the basis of helping in a primitively eusocial insect, and the first clear separation of how kin selection and direct fitness benefits influence individual behaviour.

Publications

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Description The transition to sociality has been identified as one of the major transitions in evolution. The key testing-grounds for theories concerning the origin of helping are primitively eusocial taxa, in which helpers retain the ancestral ability to reproduce independently. Co-foundress associations of Polistes paper wasps are the best studied primitively eusocial system, yet it has hitherto been unclear why many foundresses choose to become helpers. Especially paradoxical are populations of P. dominulus, in which 15-30% of helpers in three different populations are unrelated to the dominant egg-layer in the group. These unrelated helpers cannot obtain indirect fitness by helping relatives to reproduce. They thus represent a challenge to inclusive fitness theory, the dominant paradigm for understanding insect sociality.

The critical objective in the proposal was to measure the reproductive success of these unrelated helpers in comparison with the alternative strategy of nesting independently. This was achieved by monitoring >1000 individually marked foundresses on >200 natural nests in Spain, together with large-scale microsatellite genotyping of foundresses and offspring. Remarkably, we found that helpers out-reproduced independent-nesters by laying eggs of their own directly. The difference was greatest late in the nesting season, and by marking >3000 adult offspring, we further showed that only offspring produced late in the nesting season have a significant chance of reproducing themselves the following year. Genotyping showed that approximately one third of helper reproduction was through eggs laid while the dominant was still alive. But the major route was through inheriting the egg-laying position after the death of the original dominant, a route that has been strikingly neglected in previous studies. Our findings, showing that indirect fitness is not required to explain the existence of P. dominulus helpers, were published in the top international journal Science. Our results do not, however, imply that direct fitness is always the main driver of helping, because for those helpers that are relatives of the dominant, we found that indirect benefits are even larger. Rather, direct fitness benefits make helping worthwhile even when wasps are not helping their relatives. Our dataset is likely to allow tests of other major hypotheses. For example, by comparing P. dominulus nests with or without the social parasite P. semenowi, we are conducting a critical test to distinguish between general explanations for how reproduction is partitioned among the females on a nest ('reproductive skew').

Our second main objective was to test whether helpers that are unrelated to the dominant behave differently from those that are relatives. A difference might be expected: related helpers will obtain indirect fitness by working to rear the dominant's offspring, whereas working should compromise an unrelated helper's main chance of reproduction, through surviving to inherit dominance. We compared the behaviour of unrelated and related helpers on 75 field nests in a range of contexts - foraging effort, nest defence, aggression, and position in the inheritance queue - but we found no differences. A possible explanation is that wasps cannot distinguish kin from non-kin. Cuticular hydrocarbon profiles, thought to mediate recognition, were more similar on average among sisters than among non-relatives, but we found that the probability of correctly identifying relatives based on this information alone is low.

Going beyond our original objectives, we examined whether the facial markings that are thought to represent status signals in US populations of P. dominulus have the same function in our population. We found no evidence that this is the case, an unusual example of inter-population variation in the value of an intrasexual signal. We also found no evidence that wasps with apparently 'high-status' badges obtain greater reproductive success, or that the 'high-status' badge present in the social parasite P. semenowi functions to reduce aggression from P. dominulus hosts. The contrast with results from US populations may reflect environmentally induced variation in the prevalence of the badge, which is much less common in Spain.
Exploitation Route N/A The research is primarily of use for other academics in the fields of evolutionary biology/animal behaviour
 
Description Joint-funded: 50% NERC studentship (quota)/50% Sussex University
Amount £36,408 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2013 
End 03/2017
 
Description Little effect of seasonal constraints on population genetic structure in eusocial paper wasps 
Organisation University of Lausanne
Country Switzerland 
Sector Academic/University 
PI Contribution Collaboration to use data collected in a different context to that first intended
Collaborator Contribution Data analysis
Impact LENGRONNE, T., LEADBEATER, E., PATALANO, S., DREIER, S., FIELD, J., SUMNER, S. & KELLER, L. (2012) Little effect of seasonal constraints on population genetic structure in eusocial paper wasps. Ecology and Evolution 2:2615-2624
Start Year 2011