altruism in insect societies and beyond: voluntary or enforced?
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Altruism in insect societies and beyond: voluntary or enforced?
Tom WenseleersDepartment of Biology
University of Leuven, Belgiumtom.wenseleers@bio.kuleuven.be
advanced social behaviourapparent 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?
The origin of social behaviour
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
How can altruism evolve?
FIVE NEPHEWS
THREE BROTHERS
CLASSIC EXAMPLESOCIAL INSECTS
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
Altruism in insect societiesin 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 queenworker 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)
First case of altruism:becoming a worker
Become a queen ora worker?
QUEEN
EGOISTICOPTION
WORKER
ALTRUISTICOPTION
Bourke & Ratnieks 2001 Beh. Ecol. Sociob.; Wenseleers et al. 2003 J. Evol. Biol.
female larva
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): 14-20% 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. 2003 J. Evol. Biol.
Individuals cannot choose their own caste fate. Only 1 in 10,000 is allowed to become a queen.
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
Most stingless bees: caste fate enforced
queen cell
Individuals cannot choose their own caste fate. Only c. 1 in 5,000 is allowed to become a queen.
99.98% of all larvae forced to develop as workers even though 20% would like to
develop as queens= “enforced” altruism
Absence of social control: Melipona stingless bees
“Power” to the individual larvae, social control impossible
queens and workers are the same size
produced in identical, sealed cells
caste fate cannot be enforced
does this lead to anarchy?
(queen overproduction)
Yucatan, Mexico
São Paulo, Brazilië
Wenseleers & Ratnieks Proc. Roy. Soc. 2004
Melipona stingless bees
ca. 10% of the female larvae develop as queens
anarchistic outcome, as predicted by model
Yes, complete anarchy !
Most excess queens killed...
Wenseleers et al. Ethology 2003
...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
D.A. Alves, V.L. Imperatriz-Fonseca, T. Francoy, P. Nogueira-Neto & T. Wenseleers, unpublished
0.01% 0.10% 1.00% 10.00% 100.00%
% of females reared as queens
M. quinquefasciataM. seminigra
M. pseudocentrisM. beecheii
M. interruptaM. bicolor
M. melanoventerM. quadrifasciata
M. subnitidaM. marginataM. scutellarisM. fuliginosa
M. asilvaeM. rufiventris
M. favosaM. trinitatis
M. compressipes
Trigona amaltheaTrigona ventralisTrigona ruficrus
S. posticaS. bipunctata
Tetragonisca angustulaApis mellifera
SOCIAL CONTROLQueens reared in queen cellsOptimal # of queens reared
females forced to become workers“enforced” altruism
Effect of social control
NO SOCIAL CONTROLQueens reared in worker cells
Excess queens reared“anarchy”
D.A. Alves, V.L. Imperatriz-Fonseca, P. Santos-Filho & T. Wenseleers, unpublished
Anarchy in termites
Cryptotermes sp.
lower termites (Kalotermitidae, Termopsidae): all individuals except soldiers totipotent
when royal pair is lost:excess of individuals develop asreplacement reproductives
up to half of all individuals developas replacement reproductives
fight until only a single pair remains
photo: J. Korb
Evasion of social control
Schwarziana quadripunctata
Qq Qw
q
Evasion of social control:dwarf queens in Schwarziana bees
Wenseleers et al. 2005 Biol. Lett.; Wenseleers et al. 2004 Am. Nat.
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
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
Second case of altruism:worker sterility
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
Reproduce or remain sterile?
LAY EGGS
EGOISTICOPTION
REMAIN STERILE
ALTRUISTICOPTION
Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.
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. 2004 Am. Nat.
Queen policing
Common bumblebeeCourtesy of the BBC series “Life in the Undergrowth”
Queen policing
tree wasp Dolichovespula sylvestris
Wenseleers et al. BES 2005
red wasp Vespula rufa
Wenseleers et al. Evolution 2005
Ratnieks & Visscher Nature 1989
Worker policing
Worker policing
German wasp Vespula germanicaBonckaert et al. Beh. Ecol. 2008
Worker policing many against many
most effective
W W
W W
Queen policing one against many
less effective
Effectiveness of the “police system”
W W
W W
Q
What causes worker sterility?
Kinship Social pressure
high relatedness worker-laid eggsfavours workers are often eaten orto altruistically “policed” by queen orrefrain from laying by other workerseggs
tight social pressure causes workers not tolay eggs in first place
“voluntary altruism” “enforced altruism”
- 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
Which factor is the most important: relatedness or
social pressure?
effectiveness of the policing
deg
ree
of
altr
uis
m
1009998959080705030
0
5
10
30
% o
f eg
g-l
ayi
ng
wo
rke
rs Asian paper wasp
tree wasp
Norwegian wesp
median wesp
honeybee
red wesp
saxon wasp
hornet
German waspcommon wasp
Altruism is enforced…
shows social pressure is the cause of workers’ altruism !
Wenseleers & Ratnieks Nature 2006
0.3 0.4 0.5 0.6 0.7
0.075
0.25
0.50.75
2.5
57.5
25Polistes chinensis
Apis mellifera
Vespula germanica Vespa crabro
D. media
Vespula rufa
Dolichovespula saxonica
Vespula vulgaris
D. norwegica
D. sylvestris
0.3 0.4 0.5 0.6 0.7
genetic relatedness
0.075
0.25
0.50.75
2.5
57.5
25Asian paper wasp
honeybee
German wasp hornet
median wasp
red waspsaxon wasp
common wasp
Norwegian wasp
tree wasp
deg
ree
of
altr
uis
m
% o
f eg
g-l
ayi
ng
wo
rke
rs
…and not voluntary
opposite to Hamiltonian
scenario !
Wenseleers & Ratnieks Nature 2006
Ratnieks 1988 Am. Nat.
Why does low relatedness lead to more altruism?
• 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 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
t-test, p=0.0000000001n=90 species
RELATEDNESSLOW HIGH
Wenseleers & Ratnieks Am. Nat. 2006
werksters meest verwantmet zonen koningin→ worker policing
-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15
0
1
10
100MIERENBIJENWESPEN
-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15
0
1
10
100ANTSBEESWASPS
Workers most relatedto the sons of the queen
Workers most related tothe sons of other workers
relatedness difference between workers’ and queen’s sons
% a
dult
mal
es p
rodu
ced
by w
orke
rs
german wasp
red wasp
common wasp
hornet
median wasp
norwegian wasp
tree wasp
saxon wasp
Asian paper wasp
honeybee
genetic relatedness
deg
ree
of
altr
uis
m
in queenless colonies:no policing/enforcementHamiltonian predictionrecovered
In queenless colonies:Hamiltonian prediction recovered
% o
f eg
g-l
ayi
ng
wo
rke
rs
0
5
10
15
20
25
30
35
40
0.3 0.4 0.5 0.6 0.7Wenseleers & Ratnieks Nature 2006
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
What about the origin of eusociality?
• Richard Alexander (1974): parental manipulation theoryparents 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
Enforced cooperation in social vertebrates
Cooperatively breeding cichlid Neolamprologus pulcher:Subordinates that don’t help are evicted (Balshine-Earn et al. 1998)
Enforced cooperation in social vertebrates
Meerkats: dominant females suppress breeding by subordinates(Young et al. 2006)
Enforced cooperation in social vertebrates
Rhesus monkeys who do not share food are punished(Hauser 1992)
Enforced cooperation in mutualisms
Soybean plants sanction root nodule bacteria that do not fix nitrogen (Kiers et al. 2003)
Enforced cooperation in humans
the level of altruism displayed by 15 small-scale societies is correlated with degree to which defectors are punished
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
Acknowledgements
F.LW. Ratnieks
V.L. Imperatriz-Fonseca
D.A. Alves
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