Altruism in insect societies and beyond: voluntary or enforced?

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

2. The origin of social behaviour advanced social behaviourapparent 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?

3. 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

4. THREE BROTHERS FIVE NEPHEWS

5. CLASSIC EXAMPLESOCIAL INSECTS

6. 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

7. Altruism in insect societies in 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)

8. First case of altruism:becoming a worker

9. Become a queen ora worker? female larva WORKER ALTRUISTICOPTION QUEENEGOISTICOPTION Bourke & Ratnieks 2001 Beh. Ecol. Sociob.; Wenseleers et al. 2003 J. Evol. Biol.

10. 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.

11. 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 Individuals cannot choose their own caste fate. Only 1 in 10,000 is allowed to become a queen.

12. 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 Individuals cannot choose their own caste fate. Only c. 1 in 5,000 is allowed to become a queen.

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

14. Yucatan, Mexico São Paulo, Brazilië

15. Yes, complete anarchy ! Melipona stingless beesca. 10% of the female larvae develop as queens anarchistic outcome, as predicted by model Wenseleers & Ratnieks Proc. Roy. Soc. 2004

16. Most excess queens killed... Wenseleers et al. Ethology 2003

17. ...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 D.A. Alves, V.L. Imperatriz-Fonseca, T. Francoy, P. Nogueira-Neto & T. Wenseleers, unpublished

18. Effect of social control M. quinquefasciata M. seminigra M. pseudocentris M. beecheii M. interrupta M. bicolor NO SOCIAL CONTROL Queens reared in worker cellsExcess 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 cellsOptimal # of queens rearedfemales 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

19. Anarchy in termites lower termites (Kalotermitidae, Termopsidae):all individuals except soldiers totipotent when royal pair is lost:excess of individuals develop asreplacement reproductivesup to half of all individuals developas replacement reproductivesfight until only a single pair remains photo: J. Korb Cryptotermes sp.

20. Evasion of social control Schwarziana quadripunctata

21. Evasion of social control:dwarf queens in Schwarziana bees some females reared in worker cells develop as small “dwarf” queens rather than workersstrategy to evade an intended worker fate89% of all queens produced are dwarf queenssame weight as workers, so meant to become workers22% of colonies headed by these small queens w Q q Q q q Q Wenseleers et al. 2005 Biol. Lett.; Wenseleers et al. 2004 Am. Nat.

22. 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

23. Second case of altruism:worker sterility

24. 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? worker queen

25. Reproduce or remain sterile? REMAIN STERILE ALTRUISTICOPTION LAY EGGSEGOISTICOPTION Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.

26. 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 workersMore 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.

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

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

30. Worker policing Ratnieks & Visscher Nature 1989

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

32. Effectiveness of the “police system” W W Workerpolicing many against many most effective W W Queenpolicing one against many less effective W W Q W W

33. What causes worker sterility?

34. 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

35. 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 0 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

36. …and not voluntary Asian paper wasp Polistes chinensis 25 25 saxon wasp Dolichovespula saxonica tree wasp red wasp D. sylvestris Vespula rufa 7.5 7.5 Norwegian wasp D. norwegica 5 5 median wasp D. media 2.5 2.5 German wasp Vespula germanica degree of altruism hornet Vespa crabro % of egg-laying workers common wasp 0.75 0.75 Vespula vulgaris 0.5 0.5 0.25 0.25 0.075 0.075 honeybee Apis mellifera 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

37. Why does low relatedness lead to more altruism? • explanation:when relatedness is low (r < 0.5) workers are morehighly related to queen’s sons (r = 0.25) than toother 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.

38. RELATEDNESSLOW HIGH 100 100 ANTS MIEREN BEES BIJEN WESPEN WASPS Workers most related tothe sons of other workers werksters meest verwantmet zonen koningin→ worker policing % adult males producedby workers Workers most relatedto the sons of the queen 10 10 1 1 t-test, p=0.0000000001 n=90 species 0 0 - - 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

39. 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 norwegian wasp 5 0 in queenless colonies:no policing/enforcementHamiltonian predictionrecovered 0.3 0.4 0.5 0.6 0.7 Wenseleers & Ratnieks Nature 2006 genetic relatedness

40. 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

41. What about the origin of eusociality? • Richard Alexander (1974): parental manipulation theoryparents 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

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

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

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

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

46. Enforced cooperation in humans

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

48. 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