1. Altruism in insect societies and beyond: voluntary or enforced?
Tom Wenseleers
Department of Biology
University of Leuven, Belgium

2. The origin of social behaviour
advanced social behaviour apparent 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 EXAMPLE SOCIAL 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
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 or a worker?
female larva
WORKER
ALTRUISTIC OPTION
QUEEN EGOISTIC OPTION
Bourke & Ratnieks 2001 Beh. Ecol. Sociob.; Wenseleers et al 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): % 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 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
56% of all females are favoured to become queens, but only 0.01% are actually reared as queens
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
56% of all females are favoured to become queens, but only 0.01% are actually reared as queens
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 ! Wenseleers & Ratnieks Proc. Roy. Soc. 2004
Melipona stingless bees ca. 10% of the female larvae develop as queens
anarchistic outcome, as predicted by model
Queens (Q) and workers in a piece of uncapped comb of Melipona subnitida – queens are clearly produced in excess.
Wenseleers & Ratnieks Proc. Roy. Soc. 2004

16. Most excess queens killed...
Immediately afterwards, the workers aggress and kill the queen.
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
Immediately afterwards, the workers aggress and kill the queen.
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 cells Excess 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 cells Optimal # of queens reared females 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 as replacement reproductives up to half of all individuals develop as replacement reproductives fight until only a single pair remains
Immediately afterwards, the workers aggress and kill the queen.
photo: J. Korb
Cryptotermes sp.

20. Evasion of social control
Collecting a nest of S. quadripunctata – from left to right: the nest entrance hole, marking the nest entrance with flour, digging up the colony, and putting it in a box.
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 workers strategy to evade an intended worker fate 89% of all queens produced are dwarf queens same weight as workers, so meant to become workers 22% of colonies headed by these small queens w q Q Q
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) q q Q
Wenseleers et al Biol. Lett.; Wenseleers et al 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?
queen
worker

25. Reproduce or remain sterile?
ALTRUISTIC OPTION
LAY EGGS EGOISTIC OPTION
Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al 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 workers More 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 Am. Nat.

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

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

30. Worker policing
Ratnieks & Visscher Nature 1989

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

32. Effectiveness of the “police system”W W
Worker policing many against many most effective W W
The term worker policing was coined to parallel the existing term queen policing, referring to actions by the queen to prevent workers from reproducing. Queen policing has been noted in species with small colonies (several hundred or fewer workers) such as bumble bees, Polistes wasps etc.. The queen may eat eggs laid by workers or aggress workers who try to reproduce. But it is hard to see how queen policing could be effective in a large colony with tens of thousands of workers such as the honey bee. Conversely, worker policing could be effective in a large colony as it is a mutual inhibition, with many individuals policing.
Queen policing 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. effectiveness of the policing
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
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 degree of altruism genetic relatedness
Asian paper wasp
Polistes chinensis 25 25
saxon wasp
Dolichovespula saxonica
red wasp
tree wasp
D. sylvestris
Vespula rufa
7.5
7.5
Norwegian wasp
D. norwegica 5 5
median wasp
D. media
2.5
2.5
Vespula germanica
German wasp
Vespa crabro
hornet
degree of altruism
% of egg-laying workers
0.75
0.75
common wasp
Vespula vulgaris
0.5
0.5
0.25
0.25
0.075
0.075
Apis mellifera
honeybee
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 more highly related to queen’s sons (r = 0.25) than to other 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. % adult males produced by workers
RELATEDNESS LOW HIGH
100
100
ANTS
MIEREN
BIJEN
BEES
WASPS
WESPEN
Workers most related to the sons of other workers
werksters meest verwant met zonen koningin → worker policing
% adult males produced by workers
Workers most related to the sons of the queen 10 10 1 1
t-test, p=
n=90 species - -
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 recovered40
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 5
norwegian wasp
Wenseleers & Ratnieks Nature 2006
0.3
0.4
0.5
0.6
0.7
in queenless colonies: no policing/enforcement Hamiltonian prediction recovered
genetic relatedness

40. % adult males produced by workers
What about the variation in species with single-mated queens?
RELATEDNESS LOW HIGH
100
100
MIEREN
ANTS
BEES
BIJEN
WESPEN
WASPS
werksters meest verwant met zonen koningin → worker policing
% adult males produced by workers 10 10 1 1 - -
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

41. Variation in male parentage not linked to policing
e.g. stingless bees: worker reproduction usually not policed, no variation in relatedness (r = 0.75)
yet worker reproduction varies massively: 0-98% of all males workers' sons
possible explanation: colony-level cost: if workers deposit a male egg in a cell it will reduce the number of workers produced since worker-laid eggs will also compete with female eggs laid by the queen
prediction: worker reproduction should be more common if colony produces a lot of workers, i.e. if the queen lays mostly female eggs (smaller colony-level cost)

42. Prediction supported

43. 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

44. Anti-social bee-behaviour. BBC News Magazine
Egg police crack down on broody bees. New Scientist
Cops with six legs. Law and order among insects. Science News
A bug's life - Orwell style. Imprint
Bijenpolitie. Knack
Bijen leven in politiestaat. Quest Magazine
Sociale sancties werken. De Standaard
Diktatur im Bienenstock. n-tv.de (Duitsland)
(“No reproductive rights in insect police states”). Kisti (Korea)
Альтруизм общественных насекомых поддерживается полицейскими методами (“Social insect altruism is maintained by policing methods”). Elementy (Rusland)
Insectos decretan pena de muerte (“Insects declare the death penalty”). El Colombiano (Colombia)
Insectos reciben órdenes (“Insects receive orders”). TVN (Chili)

45. What about the origin of eusociality?
Richard Alexander (1974): parental manipulation theory parents 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

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

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

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

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

50. Enforced cooperation in humans

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

52. V.L. Imperatriz-Fonseca
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