Are workers in highly eusocial insects altruistic or oppressed? Tom Wenseleers
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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
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