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

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. Relatednessall males worker’s sons all males queen’s sons 0.7514%20% 0.354%56%

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

10. Bombus terrestrisApis mellifera Vespula vulgarisAtta cephalotesDorylus wilverthi Nannotrigona melanocera Queen dimorphism allows coercion

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

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

13. Excess queens killed

14. Effect of kinship in Melipona coercion is impossible, and kinship should affect optimum queens singly mated (R f =0.75) but male parentage varies I.F. optimum is for 14% of females to become queens when all males are W’s sons 20% 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 than queen’s sons (l-f-l R=0.25) Wenseleers et al. 2003 J. Evol. Biol.; Wenseleers & Ratnieks 2004 Proc. R. Soc. B

15. Species M.beecheiisubnitidamarginataquadrifasc.favosa % males workers’ sons 0%36%46%51%95% % females that develop as queens 16%7%8%9%5% refs.12345 Empirical test 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 Wenseleers & Ratnieks 2004 Proc. R. Soc. B lower optima than predicted but trend in right direction supports role of kinship in influencing decision to become Q or W

16. Q q Qw q q Q Evading coercion: dwarf queens Schwarziana quadripunctata 89% 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 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 workersare often eaten or to be altruistic“policed” by queen or other workers disfavours worker reproduction

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

20. if policing is rare or absent, fewer workers should reproduce when relatedness is high R% workers selected to reproduce 0.7514% 0.533% 0.354% Effect of kinship Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press

21. effective policing disfavours worker reproduction 0.50.60.70.80.91 5 10 15 Probability that worker-laid egg is policed ESS % of laying workers Effect of policing / coercion Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press 0

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 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 agreement estimates with smallest relative error used in final analysis

24. Speciesprimary form of policing Rcolony size % workers with active ovaries % males workers’ sons egg stage adults effectiveness of policing (%) ref A. melliferaW0.3010,0000.07 70.198.51,2,3 P. chinensisQ0.754520 643963.34,5 Vespa crabroW0.684003 < 5098.06 D. mediaQ0.711006 60794.67,8 D. saxonicaQ+W0.6215012 844889.77,8,9 D. sylvestrisQ(+W)0.681009 531085.47,10,* D. norwegicaQ0.711008 31394.07,* V. vulgarisW0.511,0001 NA0> 98.011 V. rufa Q0.581009 331167.9* Carpenter 1987, 2002 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.

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

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

29. V. vulgarisV. rufa paternity21.5 colony size1,000100 primary form of policing worker policingqueen policing policing effectiveness high < 2% worker-eggs survive for 1 day low 32% worker-eggs survive for 1 day % workers that reproduce 1%9% % adult males workers’ sons < 2%11% Foster & Ratnieks 2001; Wenseleers, Badcock et al. submitted Low relatedness favours more effective worker policing

31. Augochlorella striataDNA-FINGERPRINTING Apis dorsata Apis florea Apis melliferaPHENOT.MARKER Apis cerana Bombus terrestrisMICROSAT Bombus hypnorum Bombus melanopygusPHENOT.MARKER Plebeia saiqui Plebeia remota Plebeia droryana Schwarziana quadripunctata Melipona scutellaris Melipona quadrifasciata Melipona marginata Melipona favosaBEHAVIOURAL Melipona beecheiiMICROSAT Paratrigona subnuda Scaptotrigona postica Austroplebeia australis Austroplebeia symei Tetragona clavipes Trigona clypearis Trigona hockingsi Trigona mellipes Trigona carbonara Polistes gallicus Polistes chinensisMICROSAT Polistes dorsalis Polistes bellicosus Polybioides tabidus Parachartergus colobopterus Brachygastra mellifica Vespa crabro gribodi Vespa crabro flavofasciataMICROSAT Vespa ducalisMICROSAT Vespa mandariniaMICROSAT Dolichovespula maculata Dolichovespula media Dolichovespula arenariaALLOZYME Dolichovespula norwegica Dolichovespula sylvestris Dolichovespula saxonica (S) Dolichovespula saxonica (M) Vespula vulgaris Vespula maculifronsALLOZYME Vespula germanica Vespula rufaMICROSAT Vespula squamosaALLOZYME Nothomyrmecia macrops Formica exsecta Lasius niger Crematogaster smithi Protomognathus americanus Leptothorax acervorum Leptothorax nylanderi Epimyrma ravouxi Leptothorax unifasciatus Myrmica punctiventris Myrmica tahoensis Cyphomyrmex costatus Cyphomyrmex longiscapus Sericomyrmex amabilis Trachymyrmex cf zeteki Trachymyrmex cornetzi sp1 Acromyrmex echinatiorMICROSAT

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

33. 51 PICs Pearson R=0.52 p=0.00009 D. saxonica S vs M paternity V. rufa vs V. squamosa Dolichovespula vs Vespula Polistini vs Epiponini Bombini+Meliponini vs Apis Low relatedness favours more effective policing

34. many species with single mating but few worker-produced males many possible explanations: 1. (colony-level costs) 2. effective queen policing occurs in ants, bumblebees, halictid bees, Polistine and Vespine wasps e.g. D. norwegica (Wenseleers, Tofilski, et al., in prep.) 31% male eggs worker-laid but queen removes 94% of them 3. queen matricide (Bourke 1994) 4. sex-ratio costs (Foster & Ratnieks 2001; Wenseleers et al. in prep.) worker reproduction may results in non-optimal male-biased sex-ratio can favour worker policing and even self-restraint under single mating 5. selfish policing selfish motives drive worker policing But trend not perfect

36. Selfish or “corrupt” policing in D. sylvestris workers police but then lay an egg themselves 90% 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)

38. queenworker EGG-LAYINGQG50G81G78G20W93total Q190000000 G5018101001113 G811363100010 G7831100002 G2030110002 G1632100003 W6720101002 W9310010001 total62198311133 Q eggs W eggs 19 43 POLICING COLONY 5 29/6/2003

39. Summary coercion plays a more important role than kinship 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 policing over less effective queen policing

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

41. Thanks to Collaborators D. Alves, V. Imperatriz-Fonseca, J. Quezada, M. Ribeirostingless bees A. Tofilski, F. Nascimentowasp policing assays M. Archer, N. Badcock, T. Burke, K. ErvenVespula rufa study A. Hart, H. Helantera theory F. Ratnieks? Funding INSECTS network FWO-Vlaanderen Pekka Pamilo