Are workers in highly eusocial insects altruistic or oppressed?

Tom Wenseleers

Why do social insects cooperate?

E.g. become a worker rather than a queen...

...or work rather than reproduce

WORKERS ARE OPPRESSED

ALTRUISM IS ENFORCED

Charles D. Michener

WORKERS ARE GENUINELY ALTRUISTIC

I.F. BENEFITS OF HELPING

William D. Hamilton

1. Why become a worker?

Inclusive fitness model

• Does kin selection theory predict that many females should develop as workers?

Or are they coerced into a working role?

• model I.F. interests of individual females?

– for swarm-founding species, e.g. honeybee

– mainly workers needed

– every female that becomes a queen rather than a worker will reduce colony productivity

– linear cost function assumed

Bourke & Ratnieks 1999 Beh. Ecol. Sociob.Wenseleers et al. 2003 J. Evol. Biol.

Results

• kinship affects % of females that like to become queens– queen polyandry / polygyny (reduces relatedness among females)– male parentage (worker reproduction increases relatedness to males reared)

• but normally far fewer queens produced

• implies females are coerced to become workers

Wenseleers et al. 2003 J. Evol. Biol.

Relatedness all males worker’s sons

all males queen’s sons

0.75 14% 20%

0.3 54% 56%

“Power” to the adult workers

Apis: worker fate enforced

Bombus terrestris Apis mellifera

Vespula vulgaris Atta cephalotes Dorylus wilverthi

Nannotrigona melanocera

Queen dimorphism allows coercion

Melipona beecheii

queen

worker

“Power” to the female larvae, coercion impossible

Exception: Melipona bees

Q

Q

Q

Q Q

Predictions supported: many become queens

Excess queens killed

Effect of kinship

• in Melipona coercion is impossible, and kinship should affect optimum

• queens singly mated (Rf=0.75)but male parentage varies

• I.F. optimum is for

14% of females to become queens when all males are W’s sons

20% of females to become queens when all males are Q’s sons

• less selfishness when cost falls on closer relatives,workers’ sons (l-f-l R=0.75) rather thanqueen’s sons (l-f-l R=0.25)

Wenseleers et al. 2003 J. Evol. Biol.; Wenseleers & Ratnieks 2004 Proc. R. Soc. B

Species M. beecheii subnitida marginata quadrifasc. favosa

% males workers’ sons

0% 36% 46% 51% 95%

% females that develop as queens

16% 7% 8% 9% 5%

refs. 1 2 3 4 5

Empirical test

1 Darchen & Delage-Darchen 1975; Moo-Valle et al 200; Paxton et al. 2001; 2; Contel & Kerr 1976; Koedam et al 1999; Kerr 1950; Hara 2001; 3 Kerr 1950; Hara 2001; Toth et al. 2002; 4 da Silva 1977; Toth et al. 2002; Kerr 1950; 5 Sommeijer et al 1999, 2003; Chinh et al. 2003

Wenseleers & Ratnieks 2004 Proc. R. Soc. B

lower optima than predicted but trend in right directionsupports role of kinship in influencing decision to become Q or W

Qq Qw

qq

Q

Evading coercion: dwarf queens Schwarziana quadripunctata89% of all queens produced are dwarf queens

strategy to evade feeding control

same weight as workers, so meant to become workers

but cost: less fecund, reduced founding success

22% of colonies headed by dwarf queens

Wenseleers, Ratnieks, Ribeiro, Alves & Imperatriz-Fonseca, submitted; Wenseleers, Hart & Ratnieks Am Nat, in press

2. Why not reproduce?

Kinship Coercionhigh relatedness worker-laid eggsfavours workers are often eaten orto be altruistic “policed” by queen or

other workers

disfavours worker reproduction

relative importance of kinship and coercion insetting the number of reproductive workers within colonies ?

assumptions

- reproductive workers don’t work

- linear cost function

Inclusive fitness model

Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press

if policing is rare or absent,fewer workers should reproduce when relatedness is high

R % workers selected to reproduce

0.75 14%

0.5 33%

0.3 54%

Effect of kinship

Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press

effective policing disfavours worker reproduction

0.5 0.6 0.7 0.8 0.9 1

5

10

15

Probability that worker-laid egg is policed

ES

S %

of l

ayin

g w

orke

rs

Effect of policing / coercion

Wenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat. in press

0

Kinship or coercion? empirical test:

correlate effectiveness of police system and relatedness with % of egg-laying workers

8 Vespidae wasps + honeybee

combination of own and literature data

% of laying workers: dissection data

Effectiveness of policing

effectiveness of policing = 1 – relative prob. that worker egg survives

rel. prob. that worker egg survives estimated in 2 ways:

from policing assays:proportion of worker eggs surviving after 1 day (ideally 3 days)proportion of queen eggs surviving after 1 day

from difference between % of male eggs (e) and adults (a) that are worker produced:

both estimates show good agreementestimates with smallest relative error used in final analysis

1.1

a ee a

Species primary form of policing

R colony size

% workerswith active ovaries

% males workers’ sons

egg stage adults

effectiveness of policing (%)

ref

A. mellifera W 0.30 10,000 0.07 7 0.1 98.5 1,2,3

P. chinensis Q 0.75 45 20 64 39 63.3 4,5

Vespa crabro W 0.68 400 3 < 5 0 98.0 6

D. media Q 0.71 100 6 60 7 94.6 7,8

D. saxonica Q+W 0.62 150 12 84 48 89.7 7,8,9

D. sylvestris Q(+W) 0.68 100 9 53 10 85.4 7,10,*

D. norwegica Q 0.71 100 8 31 3 94.0 7,*

V. vulgaris W 0.51 1,000 1 NA 0 > 98.0 11

V. rufa Q 0.58 100 9 33 11 67.9 *

Carpenter 1987, 2002

1 Ratnieks & Visscher 1989; 2 Ratnieks 1993; 3 Visscher 1989, 1996; 4 Suzuki 1998; 5 Tsuchida et al. 2002, 2003; 6 Foster et al. 1999, 2000, 2002; 7 Greene 1979; 8 Foster et al. 2001; 9 Foster & Ratnieks 2000; 10 Wenseleers, Tofilski & Ratnieks Beh. Ecol. Soc. in press; 11 Foster & Ratnieks 2001; *=Wenseleers, Badcock et al. submitted; Wenseleers, Tofilski et al. in prep.

40 50 60 70 80 90 100

0.1

1

10

-20 -10 0 10 20

-8

-4

0

4

8

V. rufa

V. vulgaris

A. mellifera

Vespa crabro

D. media

D. norwegicaD. sylvestris

D. saxonicaP. chinensis

% o

f rep

rodu

ctiv

e w

orke

rs

effectiveness of policing

Spearman rank R = -0.92, p = 0.0005

p = 0.001

0.3 0.4 0.5 0.6 0.7

0.1

1

10

-0.2 -0.1 0.0 0.1 0.2

-8

-4

0

4

8

D. sylvestrisD. norwegica

D. media

A. mellifera

V. vulgaris

Vespa crabro

V. rufa

D. saxonicaP. chinensis

% o

f rep

rodu

ctiv

e w

orke

rs

worker pedigree relatedness

Spearman rank R = 0.92, p = 0.0001

p = 0.027

Ratnieks 1988 Am. Nat.

Low relatedness favours more effective worker policing

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 favours workers to police each others’ eggs

worker policing is more effective than queen policing

• Worker policing many against many

W W

W W

Ratnieks 1988 Am. Nat.

• Queen policing one against many

Queen and worker policing

W W

W W

Q

V. vulgaris V. rufa

paternity 2 1.5

colony size 1,000 100

primary form of policing

worker policing queen policing

policing effectiveness

high

< 2% worker-eggs survive for 1 day

low

32% worker-eggs survive for 1 day

% workers that reproduce

1% 9%

% adult males workers’ sons

< 2% 11%

Foster & Ratnieks 2001; Wenseleers, Badcock et al. submitted

Low relatedness favours more effective worker policing

0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8

0

20

40

60

80

100

%

of m

ales

wor

kers

' son

s

worker relatedness

honey beesEpiponine wasps

large-colony Vespulamultiple paternity colonies

of D. saxonica

little or no adult malesworker’s sons

workers more related to queen’s sons than toother workers’ sons

stingless beesbumblebees

Augochlorella (H. bee)Dolichovespula

Vespula rufasome ants

significant % of adult malesworker’s sons

raw correlation significant = 0.28, 2-sided p = 0.01

Low relatedness favours worker policing

species in Hammond & Keller 2004+ 14 additional species- studies with low detection power

Selfish or “corrupt” policing

in D. sylvestris workers police but then

lay an egg themselves90% of all worker policing is by egg-laying workers

corrupt, but still partially effective: workers do not eat queen’s eggs (cost of killing sisters)

Summarycoercion plays a more important role than kinship in favouring cooperation in insect societies

e.g. why females develop as workers– females usually coerced to become workers– kinship only important when coercion is impossible (Melipona)– coercion selects for evasion strategies (dwarf queens)

e.g. why workers do not reproduce– coercion: policing of worker-laid eggs by queen or workers

– effective policing selects for worker sterility

– kinship only plays an indirect role:low relatedness favours more effective worker policingover less effective queen policing

We’re lucky that humans are not like social insects...

...or what a Brave New World it would be!

Thanks to Collaborators

D. Alves, V. Imperatriz-Fonseca, J. Quezada, M. Ribeiro stingless beesA. Tofilski, F. Nascimento wasp policing assaysM. Archer, N. Badcock, T. Burke, K. Erven Vespula rufa studyA. Hart, H. Helantera theoryF. Ratnieks ?

FundingINSECTS networkFWO-VlaanderenPekka Pamilo