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

1. Stingless bees –Yucatan, Mexico

2. Stingless bees – São Paulo, Brazil

3. 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

4. Bourke and Ratnieks 1999 BES
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

5. Tragedy of the commons
Each individual gains by pursuing interests that increase returns relative to neighbours but decrease the value of the common goods. If all succumb to the temptation of free-riding, the outcome is a collective disaster William Forster Lloyd 1832

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

8. Exception: Melipona stingless beesQ

9. 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
<26.6 mg
>66.1 mg
Wenseleers et al., in prep.

11. Both castes reared from same cells

12. Mass provisioning

13. Melipona support predictions: excess queens
A piece of uncapped comb of Melipona subnitida clearly reveals that queens are produced in excess – up to 20% of all females develop as queens

14. Excess is killed
A Melipona subnitida queen ecloses from her cell

15. Excess is killed
Immediately afterwards, the workers aggress and kill the queen.

16. Excess is killed
Sometimes several workers join in on the action.

17. Excess is killed
Finally, the workers dump the dead queen corpse and leave it to decompose in the colony. The fact that queens are killed by the workers shows they are produced in excess.

18. Killing occurs quickly
Life expectancy adult workers = 48.5 days
Melipona beecheii
Colony
% of queens in brood combs % N
% of queens among adults % N
Life expectancy virgin queens 4 14
615
0.35
1131
25 hours 5 24 21
0.22
1843 8 3b 18
521
0.65
1226 35 T1 22
560
1.50
532 62 T2 23
732
0.49
612 19 T3 17
1184
0.00
1273
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 ( )
Kin selection theory

21. Costs to kin can limit exploitation
when selfishness causes cost to kin exploitation becomes less profitable
queen overproduction causes depletion of workforce and has two costs to kin: reduced ability to swarm reduced 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 sisters does 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
Rio Grande do Norte, Brazil
M. subnitida2
M. favosa4
Tobago, West Indies
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
Xunan Cab

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’ % % % % sons
predicted level HIGHEST > INTERMEDIATE > LOWEST
of queen production
3 / 1 / 2,476
10 / 12 / 8,162
Cols. / months / indiv’s.
* GLZ, p < 10-10 *
% 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
Rio Grande do Norte, Brazil
M. subnitida3
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’ % % % % 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
Rio Grande do Norte, Brazil
M. subnitida2
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 QUEENS lowers 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 production in 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 ratio in 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 high queen replacement takes 10 days in 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 remota ensures 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 fate enforced 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. Q q b c a d w
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)

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 queens produced are dwarf 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 !

48. Fig. 3. Excess dwarf queens (left) are killed by the workers.

49. Caste conflict in termites

50. Termite caste conflict
when colony loses royal pair it may be replaced by replacement reproductives (‘neotenics’)
in lower termites most individuals are totipotent
any individual would like to be a replacement reproductive
but just one pair is needed = another example of a ToC
should result in excess production of replacements

51. Termite caste conflict model
ESS is to molt into a replacement reproductive with a probability of 1-relatedness = 1 – 0.5 = 50% cf. Frank (assuming outbreeding)
predicts development of excess replacements
Wenseleers, Korb & Ratnieks, in prep.

52. Cryptotermes brevis
50% of all individuals develop as neotenics (Lenz et al. 1985)
all but one pair killed
as predicted by caste conflict theory

53. Development and killing of excess reproductives
TERMOPSIDAE
Porotermes adamsoni
Mensa-Bonsu Lenz 1985
KALOTERMITIDAE
Kalotermes flavicollis
Ruppli 1969, Lüscher 1952, 1956, 1974
Neotermes connexus
Myles & Chang 1984
Neotermes jouteli
Nagin 1972
Cryptotermes brevis
Lenz et al. 1985
RHINOTERMITIDAE
Reticulitermes lucifugus
Buchli 1956
Reticulitermes santonensis
Wenseleers, Korb & Ratnieks, in prep.

54. Summary social insect caste system provides scope for conflict
caste conflict may cause significant costs to the society (Melipona – queen overproduction)
coercion is more effective than kinship in suppressing caste conflict

55. What can we learn from all this?

56. Insight into conflict resolution
THE SAME TENSION OCCURS IN HUMAN SOCIETY !
Insight into conflict resolution
Self determination 20% queen production
stingless bees
Policing of caste fate
0.02% queen production
honey bees
Individual Freedom Causes a Cost to Society
But females prefer to become queen with probability of 56% !
Efficient Society but No Individual Freedom

57. References
Bourke A.F.G., Ratnieks F.L.W Kin conflict over caste determination in social Hymenoptera. Behavioral Ecology & Sociobiology 46:
Moo-Valle H., Quezada-Euán J.J.G., Wenseleers T The effect of food reserves on the production of sexual offspring in the stingless bee Melipona beecheii (Apidae, Meliponini). Insectes Sociaux 48:
Ratnieks F.L.W., Monnin T., Foster K.R Inclusive fitness theory: novel predictions and tests in eusocial Hymenoptera. Annales Zooogici Fennici 38:
Ratnieks F.L.W Heirs and spares: caste conflict and excess queen production in Melipona bees. Behavioral Ecology & Sociobiology 5:
Wenseleers T., Ratnieks F.L.W., Billen J Conflict over caste fate in social insects: a tragedy of the commons examined. Submitted.
Wenseleers T., Ratnieks F.L.W Tragedy of the commons in bees. Submitted.
PDF reprints and talk at

58. Acknowledgements
Collaborators V-L. Imperatriz-Fonseca, M. de F. Ribeiro, D. de A. Alves (SP, Brazil) H. Moo-Valle, J. Quezada-Euán and Luis Medina-Medina (Dept. of Apiculture, Merida, Mexico) R. Paxton (Tübingen, Germany)
Funding British Council FWO-Vlaanderen Vlaamse Leergangen EU ‘INSECTS’ and ‘Social Evolution’ Networks Marie Curie Fellowship