Are workers in highly eusocial insects altruistic or oppressed? Tom Wenseleers

1. Are workers in highly eusocial insects altruistic or oppressed?Tom Wenseleers

2. Why do social insects cooperate?

3. E.g. become a worker rather than a queen...

4. ...or work rather than reproduce

5. Charles D. Michener William D. Hamilton WORKERS ARE OPPRESSEDALTRUISM IS ENFORCED WORKERS ARE GENUINELY ALTRUISTIC I.F. BENEFITS OF HELPING

6. 1. Why become a worker?

7. Inclusive fitness model • Does kin selection theory predict that many females should develop as workers? Or are they coerced into a working role? • model I.F. interests of individual females? • for swarm-founding species, e.g. honeybee • mainly workers needed • every female that becomes a queen rather than a worker will reduce colony productivity • linear cost function assumed Bourke & Ratnieks 1999 Beh. Ecol. Sociob. Wenseleers et al. 2003 J. Evol. Biol.

8. Results • kinship affects % of females that like to become queens • queen polyandry / polygyny (reduces relatedness among females) • male parentage (worker reproduction increases relatedness to males reared) • but normally far fewer queens produced • implies females are coerced to become workers Wenseleers et al. 2003 J. Evol. Biol.

9. Apis: worker fate enforced “Power” to the adult workers

10. Queen dimorphism allows coercion Bombus terrestris Apis mellifera Nannotrigona melanocera Vespula vulgaris Atta cephalotes Dorylus wilverthi

11. Exception: Melipona bees Melipona beecheii queen worker “Power” to the female larvae, coercion impossible

12. Predictions supported: many become queens Q Q Q Q Q

13. Excess queens killed

14. Effect of kinship • in Meliponacoercion is impossible, and kinship should affect optimum • queens singly mated (Rf=0.75)but male parentage varies • I.F. optimum is for14% of females to become queens when all males are W’s sons20% of females to become queens when all males are Q’s sons • less selfishness when cost falls on closer relatives,workers’ sons (l-f-l R=0.75) rather thanqueen’s sons (l-f-l R=0.25) Wenseleers et al. 2003 J. Evol. Biol.; Wenseleers & Ratnieks 2004 Proc. R. Soc. B

15. Empirical test lower optima than predicted but trend in right directionsupports role of kinship in influencing decision to become Q or W Wenseleers & Ratnieks 2004 Proc. R. Soc. B 1 Darchen & Delage-Darchen 1975; Moo-Valle et al 200; Paxton et al. 2001; 2; Contel & Kerr 1976; Koedam et al 1999; Kerr 1950; Hara 2001; 3 Kerr 1950; Hara 2001; Toth et al. 2002; 4 da Silva 1977; Toth et al. 2002; Kerr 1950; 5 Sommeijer et al 1999, 2003; Chinh et al. 2003

16. Evading coercion: dwarf queens Schwarziana quadripunctata89% of all queens produced are dwarf queens strategy to evade feeding control same weight as workers, so meant to become workers but cost: less fecund, reduced founding success 22% of colonies headed by dwarf queens w Q q Q q q Q Wenseleers, Ratnieks, Ribeiro, Alves & Imperatriz-Fonseca, submitted; Wenseleers, Hart & Ratnieks Am Nat, in press

17. 2. Why not reproduce?

18. Kinship Coercion high relatedness worker-laid eggs favours workers are often eaten or to be altruistic “policed” by queen or other workers disfavours worker reproduction

19. Inclusive fitness model • relative importance of kinship and coercion insetting the number of reproductive workers within colonies ? • assumptions - reproductive workers don’t work - linear cost function Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press

20. Effect of kinship if policing is rare or absent,fewer workers should reproduce when relatedness is high Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press

21. Effect of policing / coercion effective policing disfavours worker reproduction 15 10 ESS % of laying workers 5 0 0.5 0.6 0.7 0.8 0.9 1 Probability that worker-laid egg is policed Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press

22. Kinship or coercion? • empirical test: correlate effectiveness of police system and relatedness with % of egg-laying workers • 8 Vespidae wasps + honeybee • combination of own and literature data • % of laying workers: dissection data

23. effectiveness of policing = 1 – relative prob. that worker egg survives • rel. prob. that worker egg survives estimated in 2 ways: • from policing assays:proportion of worker eggs surviving after 1 day (ideally 3 days)proportion of queen eggs surviving after 1 day • from difference between % of male eggs (e) and adults (a) that are worker produced: • both estimates show good agreementestimates with smallest relative error used in final analysis Effectiveness of policing

24. 1 Ratnieks & Visscher 1989; 2 Ratnieks 1993; 3 Visscher 1989, 1996; 4 Suzuki 1998; 5 Tsuchida et al. 2002, 2003; 6 Foster et al. 1999, 2000, 2002; 7 Greene 1979; 8 Foster et al. 2001; 9 Foster & Ratnieks 2000; 10 Wenseleers, Tofilski & Ratnieks Beh. Ecol. Soc. in press; 11 Foster & Ratnieks 2001; *=Wenseleers, Badcock et al. submitted; Wenseleers, Tofilski et al. in prep. Carpenter 1987, 2002

25. Spearman rank R = -0.92, p = 0.0005 p = 0.001

26. Spearman rank R = 0.92, p = 0.0001 p = 0.027

27. Low relatedness favours more effective worker policing • 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 favours workers to police each others’ eggs • worker policing is more effective than queen policing Ratnieks 1988 Am. Nat.

28. Queen and worker policing W W • Worker policing many against many W W • Queen policing one against many W W Q W W Ratnieks 1988 Am. Nat.

29. Low relatedness favours more effective worker policing Foster & Ratnieks 2001; Wenseleers, Badcock et al. submitted

31. Low relatedness favours worker policing raw correlation significant = 0.28, 2-sided p = 0.01 stingless bees bumblebees Augochlorella (H. bee) Dolichovespula Vespula rufa some ants significant % of adult males worker’s sons species in Hammond & Keller 2004+ 14 additional species- studies with low detection power honey bees Epiponine wasps large-colony Vespula multiple paternity colonies of D. saxonica little or no adult males worker’s sonsworkers more related to queen’s sons than toother workers’ sons

32. Selfish or “corrupt” policing • inD. sylvestris • workers police but then lay an egg themselves90% of all worker policing is by egg-laying workers • corrupt, but still partially effective: workers do not eat queen’s eggs (cost of killing sisters)

34. Summary coercion plays a more important role thankinship in favouring cooperation in insect societies e.g. why females develop as workers • females usually coerced to become workers • kinship only important when coercion is impossible (Melipona) • coercion selects for evasion strategies (dwarf queens) e.g. why workers do not reproduce • coercion: policing of worker-laid eggs by queen or workers • effective policing selects for worker sterility • kinship only plays an indirect role:low relatedness favours more effective worker policingover less effective queen policing

35. We’re lucky that humans are not like social insects... ...or what a Brave New World it would be!

36. Thanks to • CollaboratorsD. Alves, V. Imperatriz-Fonseca, J. Quezada, M. Ribeiro stingless beesA. Tofilski, F. Nascimento wasp policing assaysM. Archer, N. Badcock, T. Burke, K. Erven Vespula rufa studyA. Hart, H. Helantera theoryF. Ratnieks ? • FundingINSECTS networkFWO-VlaanderenPekka Pamilo