On the evolution of acquiescence

1. On the evolution of acquiescence or why consent to social oppressionT. Wenseleers, University of Sheffield

2. Conflict & cooperation • conflicts occur in most societies • how are conflicts resolved? • Kin selection • Recriprocity (tit-for-tat) • Reputation (humans) • Policing • Punishment NON-COERCIVE COERCIVE

3. Policing in social insects • occurs in three contexts : • conflict over male parentage(eating of worker laid eggs by queen or workers) • conflict over caste fate in societies with morph. castes (caste fate policing by food control) • conflict over queen replacement(prevention of queen overthrow)

4. Hypothesis • policing reduces benefit of attempted selfishness • could this favour individuals not even to attempt to behave selfishly ? • idea of “self policing” or “acquiescence” = to agree without protest to a system of policing

5. Aims • formally investigate the likelihood for the evolution of acquiescence • models specific for social insects, where several types of policing occur

6. Policing in social insects • occurs in three contexts : • conflict over male parentage(eating of worker laid eggs by queen or workers) • conflict over caste fate in societies with morph. castes (caste fate policing by food control) • conflict over queen replacement(prevention of queen overthrow)

7. Policing in the honey bee Workers lay male eggs…rown sons > rqueen’s sons …but these are eaten byother workersrother workers’ sons < rqueen’s sons“worker policing”

8. Caste fate policing in the honey bee Females would generally benefit from becoming a queen rather than a worker“caste fate conflict” But workers only provision a few “royal cells” with sufficient food to allow queen developmentFemales in other cells are forced to develop as workers Bourke & Ratnieks BES 1999, Wenseleers, Ratnieks & Billen J. Evol. Biol. in press

9. Conflict over queen replacement in Dinoponera ants Policed by fellow workers“pretender punishment” Selfish antattempts to overthrow current breeder Monnin & Ratnieks BES 2001, Monnin et al. Nature 2002

10. Conflict over queen replacement • Benefit of early replacement:no risk of queen being replaced by sister at later time • Cost of early replacement:drop in average colony productivity, since it takes time for new queen to reestablish • Selects for workers to police ‘early replacers’ Normal queen lifespan (100%) Nonproductive‘Lag period’ length L Early queen replacement

11. Conflict over queen replacement COLLECTIVE OPTIMUM  PREVENT EARLY OVERTHROW 100% Singlemating Doublemating 80% 60% ESS age of replacement INDIVIDUALOPTIMUM 50% = L(1+Rm)/(1-Rf) = 0.1x1.25/0.25 40% All males queen’s sons 20% All males workers’ sons 0% 10% 20% 30% 40% 50% Productivity cost of early replacement L

12. Imprisonment of virgin queens to prevent early overthrow In Trigonini stingless bees, e.g. Plebeia remotaprevents virgin queens from selfishly overthrowing mother queen - “preemptive policing” Workers force virgin queens to build their own prison and queens that escape from their prison are executed

13. Policing and acquiescence ?

14. Conflict over male parentage • If workers reproduce, but their eggs are policed, could it favour workers not to lay eggs in the first place • i.e. could policing secondarily select for worker sterility? NEW THEORY: YES

15. Worker sterility as acquiescence • single worker selected to lay when • shows that benefit of worker laying reduces as the efficiency of policing P goes up • policing can potentially make it unprofitable for any worker to lay

16. Conflict over male parentage • ESS fraction of laying workers • Function of colony size (n), relative queen fecundity (q), sister-sister relatedness (Rf) and probability that worker-laid eggs are policed (P)

17. Worker sterility as acquiescence • when there is no policing (P=0) and for large n,ESS is for colony to have ratio ofRson-Rnephew laying workers to Rnephew+Rsister sterile workers i.e. z*=(1-Rsister)/(1+Rsister) =14% under single mating • but fewer workers selected to lay when there is a high chance that their eggs are policed

18. Worker sterility as acquiescence honey bee, polyandrous queen 0.5 0.4 0.3 ESS fraction of laying workers 0.2 single monandrous queen 0.1 0.2 0.4 0.6 0.8 1 Efficiency of policing (P)

19. Empirical data : honey bees and vespine wasps Dolichovespula saxonica Dolichovespula sylvestris 5.00 Dolichovespula media Apis cerana Vespa crabro % of laying workers 0.50 Vespula vulgaris 0.05 Apis mellifera  = -0.8, p < 0.01 84 86 88 90 92 94 96 98 100 efficiency of policing(% of worker eggs eaten)

20. Empirical data : honey bee • Only 1 in 10,000 workers lay eggs • Model’s predictions • n = 35,000 workers • q = 25 (counting only queen’s male eggs) • Rf = 0.3 (multiple mating) • If policing were absent : 54% of all workers should lay • But as a result of highly effective policing there is less to gain from layinge.g. with P = 0.99 only 1 in 10,000 laying workers predicted • Fits observed data very well

21. Using best-fit colony-levelcost function y = (1-x)k 1 vespine waspsk = 1.5 colony productivity 0.5 honey beesk = 5.7 0 0 0.5 1 % of laying workers Theoretically predicted values 14  = 0.8, p < 0.01 Dolichovespula saxonica 12 10 8 Dolichovespula sylvestris observed % of laying workers 6 Dolichovespula media 4 Apis cerana 2 Vespa crabro Vespula vulgaris 0 Apis mellifera 0 2 4 6 8 10 12 14 16 theoretically predicted % of laying workers

22. Caste fate policing • Given that there are individuals benefits of developing as as queen, why do females accept their worker caste fate? • Even when females are only given little food they could potentially evade their caste fate by becoming a dwarf queen • Occurs in stingless bees and some ants

23. Stingless beePlebeia remota dwarf queen 2 mm normal queen

24. Acquiescence to caste fate • dwarf queens may have lower fecundity than normal queens • producing 100% of sister’s offspring (r = 0.375) is as good as producing 75% own offspring (r = 0.5) ! • favours acquiescence

25. Favouritism for large queens Schwarziana quadripunctata • 89% of all queens produced are dwarf queens • Yet only 31% of all colonies are headed by dwarf queens • Seems to be the result of favouritism:workers selectively kill dwarf queens and prefer to swarm with normal queens • This also reduces the benefit of becoming a dwarf queen

26. single mating, all males queen’s sons 0.2 0.15 single mating, all males workers’ sons ESS prob. of becoming dwarf queen 0.1 Schwarziana quadripunctata 0.05 0.2 0.4 0.6 0.8 1 Worker preference for normal queens (P) Parameters: 1 in a 100 cells are normal sized queen cells

27. Resolution of conflict over queen replacement • Dinoponera ants:workers are selected to overthrow mother at 50% her normal lifespan, but attempted overthrow is punished • Does punishment of “pretenders” reduce the conflict? • YES, it reduces the benefit of becoming a dominant “resisting” worker

28. 0.2 0.15 ESS fraction of resisting workers 0.1 0.05 All males gamergate’s sons All males workers’ sons 0.2 0.4 0.6 0.8 1 Effectiveness of pretender punishment (P)

29. Conclusion • Varied mechanisms of policing in social insects - aggression, imprisonment, punishment, etc… • Policing does not just repress individual selfishness, it also makes it unprofitable for individuals to act selfishly in the first place • Can explain why • workers in many species are sterile • females usually accept worker caste fate • breeder isn’t always challenged in totipotent societies

30. Acknowledgements • Collaborators • Steve Frank, Adam Hart, Heikki Helanterä, Thibaud Monnin, Francis Ratnieks • Funding • INSECTS network • EC Marie Curie Fellowship