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

qQ

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