On the evolution of acquiescence

or why consent to social oppression

T. Wenseleers, University of Sheffield

Conflict & cooperation

conflicts occur in most societies

how are conflicts resolved?

Kin selection

Recriprocity (tit-for-tat)

Reputation (humans)

Policing

PunishmentCOERCIVE

NON-COERCIVE

Policing in social insects

occurs in three contexts :

conflict over male parentage

(eating of worker laid eggs by queen or workers)

conflict over caste fate in societies with morph. castes

(caste fate policing by food control)

conflict over queen replacement

(prevention of queen overthrow)

Hypothesis

policing reduces benefit of attempted selfishness

could this favour individuals not even to attempt to behave selfishly ?

idea of “self policing” or “acquiescence” = to agree without protest to a system of policing

Aims

formally investigate the likelihood for the evolution of acquiescence

models specific for social insects, where several types of policing occur

Policing in social insects

occurs in three contexts :

conflict over male parentage

(eating of worker laid eggs by queen or workers)

conflict over caste fate in societies with morph. castes

(caste fate policing by food control)

conflict over queen replacement

(prevention of queen overthrow)

Policing in the honey bee

Workers laymale eggs…

rown sons > rqueen’s sons

…but these are eaten byother workers

rother workers’ sons < rqueen’s sons

“worker policing”

Caste fate policing in the honey bee

But workers only provision a few “royal cells” with sufficient food to allow queen development

Females in other cells are forced to develop as workers

Bourke & Ratnieks BES 1999, Wenseleers, Ratnieks & Billen J. Evol. Biol. in press

Females would generally benefit from becoming a queen rather than a worker

“caste fate conflict”

Selfish antattempts to overthrow current breeder

Policed by fellow workers

“pretender punishment”

Monnin & Ratnieks BES 2001, Monnin et al. Nature 2002

Conflict over queen replacement in Dinoponera ants

Conflict over queen replacement

Benefit of early replacement:no risk of queen being replaced by sister at later time

Cost of early replacement:drop in average colony productivity, since it takes time for new queen to reestablish

Selects for workers to police ‘early replacers’

Normal queen lifespan (100%)

Early queen replacement

Nonproductive‘Lag period’

length L

Productivity cost of early replacement L

0% 10% 20% 30% 40% 50%

20%

40%

60%

80%

100%

ES

S a

ge

of

rep

lace

men

t

All males queen’s sons

All males workers’ sons

50% INDIVIDUALOPTIMUM

COLLECTIVE OPTIMUM PREVENT EARLY OVERTHROW

Singlemating

Doublemating

Conflict over queen replacement

= L(1+Rm)/(1-Rf) = 0.1x1.25/0.25

Imprisonment of virgin queens to prevent early overthrow

In Trigonini stingless bees, e.g. Plebeia remota

prevents virgin queens from selfishly overthrowing mother queen - “preemptive policing”

Workers force virgin queens to build their own prison and queens that escape from their prison are executed

Policing and acquiescence

Conflict over It is selfish Policing via Acquiescence

Male parentage For a worker to lay eggs

Cannibalization of w/laid eggs

Worker sterility

Caste fate To become a queen

Food control Accept worker caste fate

Queen replacement

To replace current queen

Aggression or imprisonment

Not attempt to replace queen

?

If workers reproduce, but their eggs are policed, could it favour workers not to lay eggs in the first place

i.e. could policing secondarily select for worker sterility?

NEW THEORY: YES

Conflict over male parentage

Worker sterility as acquiescence

single worker selected to lay when

shows that benefit of worker laying reduces as the efficiency of policing P goes up

policing can potentially make it unprofitable for any worker to lay

1 1 1.( ) . . 0son brother brother sister

PR R R R

q n n

ESS fraction of laying workers

Function of colony size (n), relative queen fecundity (q), sister-sister relatedness (Rf) and probability that worker-laid eggs are policed (P)

2 4*

2

B B ACz

A

2 2with 2 (1 ) (1 )

2 (1 )( (1 )(1 ) (1 4 ))

( (1 ) (1 4 ))

f

f f

f

A n P R

B n P n P R q R

C q n P q R

Conflict over male parentage

when there is no policing (P=0) and for large n,ESS is for colony to have ratio of

Rson-Rnephew laying workers

to Rnephew+Rsister sterile workers

i.e. z* =(1-Rsister)/(1+Rsister) =14% under single mating

but fewer workers selected to lay when there is a high chance that their eggs are policed

Worker sterility as acquiescence

0.2 0.4 0.6 0.8 1

0.1

0.2

0.3

0.4

0.5

Efficiency of policing (P)

ES

S f

ract

ion

of

layi

ng

wo

rker

sWorker sterility as acquiescence

honey bee, polyandrous queen

single monandrous queen

Empirical data : honey bees and vespine wasps

Vespa crabro

Dolichovespula media

Dolichovespula sylvestris

Dolichovespula saxonica

Vespula vulgaris

Apis mellifera

Apis cerana

84 86 88 90 92 94 96 98 100

0.05

0.50

5.00

efficiency of policing(% of worker eggs eaten)

% o

f la

yin

g w

ork

ers

= -0.8, p < 0.01

Empirical data : honey bee

Only 1 in 10,000 workers lay eggs

Model’s predictions n = 35,000 workers

q = 25 (counting only queen’s male eggs)

Rf = 0.3 (multiple mating)

If policing were absent : 54% of all workers should lay

But as a result of highly effective policing there is less to gain from layinge.g. with P = 0.99 only 1 in 10,000 laying workers predicted

Fits observed data very well

Theoretically predicted values

Vespa crabro

Dolichovespula media

Dolichovespula sylvestris

Dolichovespula saxonica

Vespula vulgaris

Apis mellifera

Apis cerana

0 2 4 6 8 10 12 14 16

theoretically predicted % of laying workers

0

2

4

6

8

10

12

14o

bse

rve

d %

of l

ayin

g w

ork

ers

0 0.5 1

% of laying workers

0

0.5

1

colo

ny

pro

du

ctiv

ityhoney bees

k = 5.7

vespine waspsk = 1.5

Using best-fit colony-levelcost function y = (1-x)k

= 0.8, p < 0.01

Caste fate policing

Given that there are individuals benefits of developing as as queen, why do females accept their worker caste fate?

Even when females are only given little food they could potentially evade their caste fate by becoming a dwarf queen

Occurs in stingless bees and some ants

dwarf queen

normal queen2 mm

Stingless beePlebeia remota

Acquiescence to caste fate

dwarf queens may have lower fecundity than normal queens

producing 100% of sister’s offspring (r = 0.375) is as good as producing 75% own offspring (r = 0.5) !

favours acquiescence

Favouritism for large queens

Schwarziana quadripunctata

89% of all queens produced are

dwarf queens

Yet only 31% of all colonies are

headed by dwarf queens

Seems to be the result of favouritism:

workers selectively kill dwarf queens

and prefer to swarm with normal queens

This also reduces the benefit of

becoming a dwarf queen

0.2 0.4 0.6 0.8 1

0.05

0.1

0.15

0.2E

SS

pro

b.

of

bec

om

ing

dw

arf

qu

een

Worker preference for normal queens (P)

single mating, all males workers’ sons

single mating, all males queen’s sons

Schwarziana quadripunctata

Parameters: 1 in a 100 cells are normal sized queen cells

Resolution of conflict over queen replacement

Dinoponera ants:workers are selected to overthrow mother at 50% her normal lifespan, but attempted overthrow is punished

Does punishment of “pretenders” reduce the conflict?

YES, it reduces the benefit of becoming a dominant “resisting” worker

0.2 0.4 0.6 0.8 1

0.05

0.1

0.15

0.2E

SS

fra

ctio

n o

f re

sist

ing

wo

rker

s

Effectiveness of pretender punishment (P)

All males gamergate’s sons

All males workers’ sons

Conclusion

Varied mechanisms of policing in social insects - aggression, imprisonment, punishment, etc…

Policing does not just repress individual selfishness, it also makes it unprofitable for individuals to act selfishly in the first place

Can explain why workers in many species are sterile

females usually accept worker caste fate

breeder isn’t always challenged in totipotent societies

Acknowledgements

Collaborators

Steve Frank, Adam Hart, Heikki Helanterä, Thibaud Monnin, Francis Ratnieks

Funding

INSECTS network

EC Marie Curie Fellowship