Actual and potential tragedies: conflicts over female caste fate in Apis and Melipona bees

1. Actual and potential tragedies: conflicts over female caste fate in Apis and Melipona bees Tom Wenseleers & Francis Ratnieks University of Sheffield, UK

2. Stingless bees –Yucatan, Mexico

3. Stingless bees – São Paulo, Brazil

4. Why become a worker? Workers Give up reproduction for the benefit of their mother queen Darwinian puzzle ‘The sterile worker caste of the social Hymenoptera poses one special difficulty, which at first appeared to me insuperable, and actually fatal to my whole theory.’ Darwin (1859) On the Origin of Species

5. E.g. honey bee • benefit of becoming a queen:ability to head daughter swarm • SO WHY DO NOT MANY FEMALES OPT TO BECOME QUEENS? • females benefit from becoming a queen, but colony would suffer if all would do so“caste fate conflict”(colony mostly needs workers for swarming) • individual benefits but collective suffers = “tragedy of the commons” Bourke and Ratnieks 1999 BES

7. Queen rearing in honey bees Socially controlled, caste fate enforced

8. Q Q Q Q Q Exception: Melipona stingless bees

9. Q Q Q Q Q Queens no larger than workers...

10. ...in fact they are slightly smaller Melipona beecheii mean = 57.1 mg F3,480=76.3, p < 1E-13 mean = 48.2 mg >66.1 mg <26.6 mg Wenseleers et al., in prep.

11. Both castes reared from same cells

12. Mass provisioning

13. Q Q Q Q Q Melipona support predictions:excess queens

14. Excess is killed

15. Excess is killed

16. Excess is killed

17. Excess is killed

18. Killing occurs quickly Life expectancy adult workers = 48.5 days Melipona beecheii Queens killed within 25 hours after eclosing

19. Summary • social insect females benefit from developing as a queen • in Melipona, females have the ability to do this (’self determination’) • results in excess queen production • why do not all females develop as a queen?what limits exploitation within the group?

20. W.D. Hamilton (1936-2000) Kin selection theory

21. Costs to kin can limit exploitation • when selfishness causescost to kin exploitationbecomesless profitable • queen overproduction causes depletion of workforce and has two costs to kin:reduced ability to swarmreduced production of males • prediction: less exploitation when group members are highly related • has never been tested

22. Factors determining kinship • multiple mating by queen: reduces relatedness among sistersdoes not occur in stingless bees • worker laying • workers can sometimes produce sons • relatedness to worker’s sons = 0.75 • relatedness to queen’s sons = 0.25 can occur in stingless bees

23. Caste conflict model • female should become a queen with a probability of (1-Rf) / (1+Rm) (self determination) with Rf = sister-sister relatedness Rm = relatedness to males = 20% under single mating, all males queen produced = 14% under single mating, all males worker produced • assuming linear cost to total colony reproduction • higher/lower ratios with other cost functions Ratnieks 2001 BES; Wenseleers & Ratnieks submitted

24. Test: interspecies comparison PREDICTION less queen overproduction when males are worker’s sons, since costs are then to closer relatives(nephews, r = 0.75, rather than brothers, r = 0.25)

25. Male parentage in Melipona % of males LOW > INTERMEDIATE> HIGH workers’ sons 4 / 604 / OBS Mean, 95% C.L. #cols. / #males / study * GLZ, p < 10-15 * % of males workers’ sons 4 / 1,338 / GEN+OBS 16/ 505 / GEN+OBS N.S. * 13 / 108 / GEN M. favosa4 Tobago, West Indies M. subnitida2 Rio Grande do Norte, Brazil M. beecheii1 Yucatan, Mexico M. quadrifasciata3 Various sites, Brazil 1 Paxton et al 2001; 2 Contel & Kerr 1976; Koedam et al 1999, 2002; 3 da Silva 1977; Toth et al 2002; 4 Sommeijer et al 1999 All species singly mated: Peters et al 1999, Contel & Kerr 1976, Paxton et al 2001, Kerr 1975, Kerr et al 1962

26. Yucatan: Melipona beecheii

27. Ah Muzencab

30. M. beecheii caste ratios Max. = 21% Average = 14.6% 95% C.L. Prop. of queens produced 10 cols.8,162 ind. Moo-Valle, Quezada-Euan and Wenseleers 2001 Insectes Sociaux

31. Test: interspecies comparison % males workers’ 0% 34% 41% 95% sons predicted level HIGHEST > INTERMEDIATE> LOWEST of queen production 3 / 1 / 2,476 10 / 12 / 8,162 * GLZ, p < 10-10 Cols. / months / indiv’s. * % of queens produced 6 / 2 / 3,989 9 / 11 / 2,806 N.S. * 78 / 10 / 13,514 Mean, 95% C.L. M. beecheii1 Yucatan, Mexico M. beecheii2 Yucatan, Mexico M. favosa5 Tobago, West Indies M. subnitida3 Rio Grande do Norte, Brazil M. quadrifasciata4 Various sites, Brazil 1 Darchen & Delage-Darchen 1975; 2 Moo-Valle et al 2001; 3 Koedam et al 1999, 2002; 4 Kerr 1950; 5 Sommeijer et al 2002

32. Test: interspecies comparison % males workers’ 0% 34% 41% 95% sons predicted level HIGHEST > INTERMEDIATE> LOWEST of queen production Data from months with maximum queen production only * * GLZ, p < 10-10 % of queens produced N.S. * Mean, 95% C.L. M. beecheii1 Yucatan, Mexico M. favosa4 Tobago, West Indies M. subnitida2 Rio Grande do Norte, Brazil M. quadrifasciata3 Various sites, Brazil 1 Moo-Valle et al 2001; 2 Koedam et al 1999, 2002; 3 Kerr 1950; 4 Sommeijer et al 2002

33. Future test: Melipona bicolor MULTIPLE MOTHER QUEENSlowers relatedness should cause even greater queen overproduction

34. Summary • Melipona females selfishly exploit colony by developing as queens • causes “tragedy of the commons”: queen overproduction • reduced exploitation when costs are to close kin (workers’ sons)

35. Alternative explanations for excess queen productionin Melipona ?

36. 1. Kerr’s theory of genetic caste determination Kerr (1950) proposed 2-locus 2-allele system for Melipona females heterozygous at both loci develop into queens results in 25% queens

37. Different levels of explanation • not an alternative hypothesis –different level of explanation (Alcock 1993) :Kerr’s hypothesis suggests HOW the observed caste ratios could come about (PROXIMATE)Caste conflict theory explains WHY the caste ratios are as observed (ULTIMATE) • cf. XY-sex determination as an efficient mechanism to attain optimal 1:1 sex ratioin mammals

38. 2. Insurance against queen loss? • queen are overproduced to ensure that continuous stock of queens is present • bet-hedging argument • queen overproduction is far too highqueen replacement takes 10 daysin this period up to 70 queens are produced • there are other ways to ensure a continuous stock of queens

39. Queen stocks kept in prisons In Trigonini stingless bees, e.g. Plebeia remotaensures that continuous stock of queens is present without having to overproduce them

40. What about other social insects? • other swarming social insects: queen-worker size dimorphism • army ants • honey bees • trigonine (non-Melipona) stingless bees • caste fateenforced via food control • results in few queens being produced • makes individuals work for the benefit of society and develop as a worker, even when not in best interests of individuals themselves

41. Policing of caste fate: food control Queen rearing in honey bees

42. Honey bee • multiply mated: Rf=0.3, Rm=0.25 • females would like to become queens with prob. of (1-Rf) / (1+Rm) = 56% • only 0.02% actually become queens • strong divergence between individual and colony optimum • females are coerced into a working role

43. Policing of caste fate: food control Queen rearing in trigonine bees

44. Evasion of caste policing:dwarf queens • observations • occur in ants and trigonine bees • same size as workers • produced in excess • can reproduce, although usually less fecund • hypothesis • selfish strategy to overcome worker feeding control? • support • overproduced relative to normal queens

45. a c a Q b q d d q Q w Q q

46. Plebeia remota dwarf queen 2 mm normal queen

47. Frequency of dwarf queens • overproduced relative to normal queens • E.g. Schwarziana quadripunctata • 1 in 85 worker cells (1.2%) yield dwarf queens • only 1 in 620 females reared as normal queens (0.16%) • i.e. 88% of all queensproduced aredwarf queens & produced in 7-fold excess relative to normal queens • excess queens are killed by workers as in Melipona • as predicted by caste conflict theory !

49. Caste conflict in termites

50. Development and killing of excess reproductives Wenseleers, Korb & Ratnieks, in prep.