Altruism in insect societies and beyond: voluntary or enforced? Tom Wenseleers Department of Biology University of Leuven, Belgium tom.wenseleers@bio.kuleuven.be

The origin of social behaviour advanced social behaviour apparent in many animals, e.g. social insects, some birds and mammals, and in humans most advanced form of social behaviour: altruism helping another at a cost to oneself puzzle: how can behaviour that is individually costly evolve under a regime of natural selection?

How can altruism evolve? William D. Hamilton (1964) close family ties are essential helping relatives results in the propagation of copies of the altruist’s own genes in this way the gene for the altruistic behaviour can spread high relatedness should cause greater altruism

THREE BROTHERS FIVE NEPHEWS

CLASSIC EXAMPLE SOCIAL INSECTS

Could the textbooks be wrong? due to haplodiploidy, relatedness is indeed very high in insect societies (¾) but is it high enough to explain the workers’ altruism? no, based on theoretical models I will show that the levels of altruism observed in many contemporaneous species can only be explained as having evolved in response to social coercion altruism is not voluntary, but enforced

Altruism in insect societies the context of the origin of social behaviour decision for a female to become a worker rather than breed solitarily in advanced social species becoming a worker rather than a queen worker sterility (not lay eggs) I compared level of altruism you should get in these last 2 contexts if individuals could behave free from social coercion (voluntary altruism) versus when coercion is present (enforced altruism)

First case of altruism: becoming a worker

Become a queen or a worker? female larva WORKER ALTRUISTIC OPTION QUEEN EGOISTIC OPTION Bourke & Ratnieks 2001 Beh. Ecol. Sociob.; Wenseleers et al. 2003 J. Evol. Biol.

Theoretical model if every individual is able to control its own caste development you should get “anarchy” in the colony: excess queens single mating (stingless bees): 14-20% of all larvae selected to develop as queens 10 matings (honey bees): 56% of all larvae selected to develop as queens bees do not require so many queens, since mainly workers are needed for colony multiplication via swarming adult workers are selected to try to prevent excess queens from developing via social control Wenseleers et al. 2003 J. Evol. Biol.

Honeybee: caste fate enforced 99.99% of all larvae forced to develop as workers even though 56% would like to develop as queens = “enforced” altruism 56% of all females are favoured to become queens, but only 0.01% are actually reared as queens Individuals cannot choose their own caste fate. Only 1 in 10,000 is allowed to become a queen.

Most stingless bees: caste fate enforced 99.98% of all larvae forced to develop as workers even though 20% would like to develop as queens = “enforced” altruism queen cell 56% of all females are favoured to become queens, but only 0.01% are actually reared as queens Individuals cannot choose their own caste fate. Only c. 1 in 5,000 is allowed to become a queen.

Absence of social control: Melipona stingless bees (queen overproduction) “Power” to the individual larvae, social control impossible

Yucatan, Mexico São Paulo, Brazilië

Yes, complete anarchy ! Wenseleers & Ratnieks Proc. Roy. Soc. 2004 Melipona stingless bees ca. 10% of the female larvae develop as queens anarchistic outcome, as predicted by model Queens (Q) and workers in a piece of uncapped comb of Melipona subnitida – queens are clearly produced in excess. Wenseleers & Ratnieks Proc. Roy. Soc. 2004

Most excess queens killed... Immediately afterwards, the workers aggress and kill the queen. Wenseleers et al. Ethology 2003

...or escape being killed by parasitizing queenless colonies Melipona scutellaris: some virgin queens escape being killed by leaving the colony and parasitizing unrelated queenless hives if the mother queen dies in 30% (7/24) of the cases it is replaced by an unrelated queen coming from other queenright colony Immediately afterwards, the workers aggress and kill the queen. D.A. Alves, V.L. Imperatriz-Fonseca, T. Francoy, P. Nogueira-Neto & T. Wenseleers, unpublished

Effect of social control M. quinquefasciata M. seminigra M. pseudocentris M. beecheii M. interrupta M. bicolor NO SOCIAL CONTROL Queens reared in worker cells Excess queens reared “anarchy” M. melanoventer M. quadrifasciata M. subnitida M. marginata M. scutellaris M. fuliginosa M. asilvae M. rufiventris M. favosa M. trinitatis M. compressipes SOCIAL CONTROL Queens reared in queen cells Optimal # of queens reared females forced to become workers “enforced” altruism Trigona amalthea Trigona ventralis Trigona ruficrus S. postica S. bipunctata Tetragonisca angustula Apis mellifera 0.01% 0.10% 1.00% 10.00% 100.00% % of females reared as queens D.A. Alves, V.L. Imperatriz-Fonseca, P. Santos-Filho & T. Wenseleers, unpublished

Anarchy in termites lower termites (Kalotermitidae, Termopsidae): all individuals except soldiers totipotent when royal pair is lost: excess of individuals develop as replacement reproductives up to half of all individuals develop as replacement reproductives fight until only a single pair remains Immediately afterwards, the workers aggress and kill the queen. photo: J. Korb Cryptotermes sp.

Evasion of social control Collecting a nest of S. quadripunctata – from left to right: the nest entrance hole, marking the nest entrance with flour, digging up the colony, and putting it in a box. Schwarziana quadripunctata

Evasion of social control: dwarf queens in Schwarziana bees some females reared in worker cells develop as small “dwarf” queens rather than workers strategy to evade an intended worker fate 89% of all queens produced are dwarf queens same weight as workers, so meant to become workers 22% of colonies headed by these small queens w q Q Q Fig. 1. (a) In the trigonine stingless bees, queens are normally reared from special royal cells constructed near the periphery of the comb (Q). The other, smaller cells yield males and workers. (b) However, in the stingless bee Schwarziana quadripunctata, approx. 1% of all females in small cells cheat on their intended caste fate and become miniature queens (q) rather than sterile workers. The female in the larger royal cell (Q) is a normal queen. (c) Just like normal queens (c), these dwarf queens can succesfully reproduce and head colonies (d). (scale bars = 5mm, a and b and c and d are the same scale) q q Q Wenseleers et al. 2005 Biol. Lett.; Wenseleers et al. 2004 Am. Nat.

Conclusion caste development generally under tight social control females usually forced to become workers against their own evolutionary interests altruism is not voluntary, but enforced absence of social control causes anarchy

Second case of altruism: worker sterility

Workers can reproduce but often they don’t Workers can lay unfertilised male eggs but usually only few do so. Why are workers so altruistic? queen worker

Reproduce or remain sterile? ALTRUISTIC OPTION LAY EGGS EGOISTIC OPTION Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.

Theoretical model Hamiltonian prediction: high relatedness should favour greater voluntary altruism (fewer egg laying workers) But also an influence of sociale pressure: in many species, eggs laid by workers are cannibalized or “policed” by the queen or by other workers More effective policing selects for fewer workers to lay eggs in the first place “enforced altruism” Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.

Queen policing Common bumblebee Courtesy of the BBC series “Life in the Undergrowth”

Queen policing red wasp Vespula rufa Wenseleers et al. Evolution 2005 tree wasp Dolichovespula sylvestris Wenseleers et al. BES 2005

Worker policing Ratnieks & Visscher Nature 1989

Worker policing Bonckaert et al. Beh. Ecol. 2008 German wasp Vespula germanica

Effectiveness of the “police system” W W Worker policing many against many most effective W W The term worker policing was coined to parallel the existing term queen policing, referring to actions by the queen to prevent workers from reproducing. Queen policing has been noted in species with small colonies (several hundred or fewer workers) such as bumble bees, Polistes wasps etc.. The queen may eat eggs laid by workers or aggress workers who try to reproduce. But it is hard to see how queen policing could be effective in a large colony with tens of thousands of workers such as the honey bee. Conversely, worker policing could be effective in a large colony as it is a mutual inhibition, with many individuals policing. Queen policing one against many less effective W W Q W W

What causes worker sterility?

Which factor is the most important: relatedness or social pressure? comparative study of 10 species (9 wasps+honeybee) effectiveness of the policing and % of reproductive workers determined mother queen mates with a variable # of males → variation in relatedness

effectiveness of the policing Altruism is enforced… Asian paper wasp 30 saxon wasp degree of altruism red wesp % of egg-laying workers 10 tree wasp Norwegian wesp median wesp 5 hornet German wasp common wasp honeybee shows social pressure is the cause of workers’ altruism ! Wenseleers & Ratnieks Nature 2006 30 50 70 80 90 95 98 99 100 effectiveness of the policing

…and not voluntary degree of altruism genetic relatedness Asian paper wasp Polistes chinensis 25 25 saxon wasp Dolichovespula saxonica red wasp tree wasp D. sylvestris Vespula rufa 7.5 7.5 Norwegian wasp D. norwegica 5 5 median wasp D. media 2.5 2.5 Vespula germanica German wasp Vespa crabro hornet degree of altruism % of egg-laying workers 0.75 0.75 common wasp Vespula vulgaris 0.5 0.5 0.25 0.25 0.075 0.075 Apis mellifera honeybee opposite to Hamiltonian scenario ! Wenseleers & Ratnieks Nature 2006 0.3 0.3 0.4 0.4 0.5 0.5 0.6 0.6 0.7 0.7 genetic relatedness

Why does low relatedness lead to more altruism? explanation: when relatedness is low (r < 0.5) workers are more highly related to queen’s sons (r = 0.25) than to other workers’ sons (r < 0.25) this selects for workers to police each others’ eggs worker policing is more effective than queen policing meta-analysis of 90 species also shows that worker reproduction is more effectively inhibited in species with low relatedness Ratnieks 1988 Am. Nat.

% adult males produced by workers RELATEDNESS LOW HIGH 100 100 ANTS MIEREN BIJEN BEES WASPS WESPEN Workers most related to the sons of other workers werksters meest verwant met zonen koningin → worker policing % adult males produced by workers Workers most related to the sons of the queen 10 10 1 1 t-test, p=0.0000000001 n=90 species - - 0.15 0.15 - - 0.10 0.10 - - 0.05 0.05 0.00 0.00 0.05 0.05 0.10 0.10 0.15 0.15 relatedness difference between workers’ and queen’s sons Wenseleers & Ratnieks Am. Nat. 2006

In queenless colonies: Hamiltonian prediction recovered 40 honeybee 35 german wasp 30 common wasp Asian paper wasp 25 degree of altruism % of egg-laying workers red wasp 20 tree wasp 15 median wasp saxon wasp 10 hornet 5 norwegian wasp Wenseleers & Ratnieks Nature 2006 0.3 0.4 0.5 0.6 0.7 in queenless colonies: no policing/enforcement Hamiltonian prediction recovered genetic relatedness

% adult males produced by workers What about the variation in species with single-mated queens? RELATEDNESS LOW HIGH 100 100 MIEREN ANTS BEES BIJEN WESPEN WASPS werksters meest verwant met zonen koningin → worker policing % adult males produced by workers 10 10 1 1 - - 0.15 0.15 - - 0.10 0.10 - - 0.05 0.05 0.00 0.00 0.05 0.05 0.10 0.10 0.15 0.15 relatedness difference between workers’ and queen’s sons

Variation in male parentage not linked to policing e.g. stingless bees: worker reproduction usually not policed, no variation in relatedness (r = 0.75) yet worker reproduction varies massively: 0-98% of all males workers' sons possible explanation: colony-level cost: if workers deposit a male egg in a cell it will reduce the number of workers produced since worker-laid eggs will also compete with female eggs laid by the queen prediction: worker reproduction should be more common if colony produces a lot of workers, i.e. if the queen lays mostly female eggs (smaller colony-level cost)

Prediction supported

Conclusion social pressure is often the true cause of the workers’ altruism (worker sterility), and close family ties usually not required altruism is usually not voluntary, but enforced low relatedness actually correlated with greater cooperation because it is associated with tighter social control

Anti-social bee-behaviour. BBC News Magazine Egg police crack down on broody bees. New Scientist Cops with six legs. Law and order among insects. Science News A bug's life - Orwell style. Imprint Bijenpolitie. Knack Bijen leven in politiestaat. Quest Magazine Sociale sancties werken. De Standaard Diktatur im Bienenstock. n-tv.de (Duitsland) (“No reproductive rights in insect police states”). Kisti (Korea) Альтруизм общественных насекомых поддерживается полицейскими методами (“Social insect altruism is maintained by policing methods”). Elementy (Rusland) Insectos decretan pena de muerte (“Insects declare the death penalty”). El Colombiano (Colombia) Insectos reciben órdenes (“Insects receive orders”). TVN (Chili)

What about the origin of eusociality? Richard Alexander (1974): parental manipulation theory parents force offspring to take on a worker role, e.g. by unferfeeding them But little supporting evidence, e.g. in Polistes annularis even the smallest females can leave the nest and become a foundress the next year Eusociality should be more common if it had evolved via a route of parental manipulation

Enforced cooperation in social vertebrates Cooperatively breeding cichlid Neolamprologus pulcher: Subordinates that don’t help are evicted (Balshine-Earn et al. 1998)

Enforced cooperation in social vertebrates Meerkats: dominant females suppress breeding by subordinates (Young et al. 2006)

Enforced cooperation in social vertebrates Rhesus monkeys who do not share food are punished (Hauser 1992)

Enforced cooperation in mutualisms Soybean plants sanction root nodule bacteria that do not fix nitrogen (Kiers et al. 2003)

Enforced cooperation in humans

the level of altruism displayed by 15 small-scale societies is correlated with degree to which defectors are punished

V.L. Imperatriz-Fonseca Acknowledgements F.LW. Ratnieks D.A. Alves V.L. Imperatriz-Fonseca wasp work: F.L.W. Ratnieks, F. Nascimento, A. Tofilski, M. Archer, N. Badcock, W. Bonckaert, T. Burke, K. Erven, H. Helantera, L. Holman, K. Vuerinckx stingless bee work: V.L. Imperatriz-Fonseca, D. Alves, T. Francoy, M. Ribeiro, J. Quezada