On the evolution of acquiescence or why consent to social oppression T. Wenseleers, University of Sheffield

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

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)

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

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

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)

Policing in the honey bee Workers lay male eggs… r own sons > r queen’s sons …but these are eaten by other workers r other workers’ sons < r queen’s sons “worker policing”

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

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

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%) Early queen replacement Nonproductive ‘Lag period’ length L

Productivity cost of early replacement L 0%10%20%30%40%50% 20% 40% 60% 80% 100% ESS age of replacement All males queen’s sons All males workers’ sons 50% INDIVIDUAL OPTIMUM COLLECTIVE OPTIMUM  PREVENT EARLY OVERTHROW Single mating Double mating Conflict over queen replacement = L(1+R m )/(1-R f ) = 0.1x1.25/0.25

Imprisonment of virgin queens to prevent early overthrow In Trigonini stingless bees, e.g. Plebeia remota prevents 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

Policing and acquiescence Conflict overIt is selfishPolicing viaAcquiescence Male parentageFor a worker to lay eggs Cannibalization of w/laid eggs Worker sterility Caste fateTo become a queen Food controlAccept worker caste fate Queen replacement To replace current queen Aggression or imprisonment Not attempt to replace queen ?

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 Conflict over male parentage

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

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

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

Efficiency of policing (P) ESS fraction of laying workers Worker sterility as acquiescence honey bee, polyandrous queen single monandrous queen

Empirical data : honey bees and vespine wasps Vespa crabro Dolichovespula media Dolichovespula sylvestris Dolichovespula saxonica Vespula vulgaris Apis mellifera Apis cerana efficiency of policing (% of worker eggs eaten) % of laying workers  = -0.8, p < 0.01

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) R f = 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 laying e.g. with P = 0.99 only 1 in 10,000 laying workers predicted Fits observed data very well

Theoretically predicted values Vespa crabro Dolichovespula media Dolichovespula sylvestris Dolichovespula saxonica Vespula vulgaris Apis mellifera Apis cerana theoretically predicted % of laying workers observed % of laying workers % of laying workers colony productivity honey bees k = 5.7 vespine wasps k = 1.5 Using best-fit colony-level cost function y = (1-x) k  = 0.8, p < 0.01

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

dwarf queen normal queen 2 mm Stingless bee Plebeia remota

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

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

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

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

ESS fraction of resisting workers Effectiveness of pretender punishment (P) All males gamergate’s sons All males workers’ sons

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

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