actual and potential tragedies: conflicts over female caste fate in apis and melipona bees
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Actual and potential tragedies: conflicts over female caste fate in Apis and Melipona bees. Tom Wenseleers & Francis Ratnieks University of Sheffield, UK. Stingless bees –Yucatan, Mexico. Stingless bees – S ão Paulo, Brazil. Why become a worker?. Worker s - PowerPoint PPT PresentationTRANSCRIPT
Actual and potential tragedies: conflicts over female caste fate in Apis and
Melipona beesTom Wenseleers & Francis Ratnieks
University of Sheffield, UK
Stingless bees –Yucatan, Mexico
Stingless bees – São Paulo, Brazil
Workers
Give up reproduction for the benefit of their mother queen
Darwinian puzzle
‘The sterile worker caste of the social Hymenoptera poses one special difficulty, which at first appeared to me insuperable, and actually fatal to my whole
theory.’
Darwin (1859) On the Origin of
Species
Why become a worker?
E.g. honey bee benefit of becoming a queen:
ability to head daughter swarm
SO WHY DO NOT MANY FEMALES OPT TO BECOME QUEENS?
females benefit from becoming a queen, but colony would suffer if all would do so “caste fate conflict”(colony mostly needs workers for swarming)
individual benefits but collective suffers = “tragedy of the commons”
Bourke and Ratnieks 1999 BES
Socially controlled, caste fate enforced
Queen rearing in honey bees
Exception: Melipona stingless bees
Q
Q
Q
Q Q
Queens no larger than workers...
Q
Q
Q
Q Q
...in fact they are slightly smaller
0
10
20
30
40
50
60
70
Queens
Workers
<26
.6 m
g
>66
.1 m
g
mean = 48.2 mg
mean = 57.1 mg
F3,480=76.3, p < 1E-13
Melipona beecheii
Wenseleers et al., in prep.
Both castes reared from same cells
Mass provisioning
Melipona support predictions:excess queens
Q
Q
Q
Q Q
Excess is killed
Excess is killed
Excess is killed
Excess is killed
Killing occurs quickly
Colony % of queens in brood combs
% N
% of queens among adults
% N
Life expectancy virgin queens
4 14 615 0.35 1131 25 hours
5 24 21 0.22 1843 8
3b 18 521 0.65 1226 35
T1 22 560 1.50 532 62
T2 23 732 0.49 612 19
T3 17 1184 0.00 1273 0
Queens killed within 25 hours after eclosing
Life expectancy adult workers = 48.5 daysMelipona beecheii
Summary
social insect females benefit from developing as a queen
in Melipona, females have the ability to do this (’self determination’)
results in excess queen production
why do not all females develop as a queen?
what limits exploitation within the group?
W.D. Hamilton (1936-2000)
Kin selection theory
Costs to kin can limit exploitation
when selfishness causes cost to kin exploitation becomes less profitable
queen overproduction causes depletion of workforce and has two costs to kin:
reduced ability to swarmreduced production of males
prediction: less exploitation when group members are highly related
has never been tested
Factors determining kinship
multiple mating by queen: reduces relatedness among sisters
does not occur in stingless bees
worker laying
– workers can sometimes produce sons
– relatedness to worker’s sons = 0.75
– relatedness to queen’s sons = 0.25
can occur in stingless bees
Caste conflict model
female should become a queen with a probability of (1-Rf) / (1+Rm) (self determination)
with Rf = sister-sister relatedness
Rm = relatedness to males
= 20% under single mating, all males queen produced
= 14% under single mating, all males worker produced
assuming linear cost to total colony reproduction
higher/lower ratios with other cost functions
Ratnieks 2001 BES; Wenseleers & Ratnieks submitted
Test: interspecies comparison
PREDICTION
less queen overproduction when males are worker’s sons, since costs are then to closer relatives
(nephews, r = 0.75, rather than brothers, r = 0.25)
0
20
40
60
80
100
% o
f m
ale
s w
ork
ers
’ so
ns
0
20
40
60
80
100
M. q
uadrif
asci
ata
3
Vario
us si
tes,
Bra
zil
M. s
ubnitida
2
Rio G
rande
do Norte
, Bra
zil
M. b
eech
eii1
Yucata
n, Mex
ico
M. f
avosa
4
Tobago, W
est I
ndies
*
*
4 / 604 / OBS
4 / 1,338 / GEN+OBS16 / 505 / GEN+OBS
13 / 108 / GEN
#cols. / #males / study
* GLZ, p < 10-
15
N.S
.
Male parentage in Melipona% of males LOW > INTERMEDIATE > HIGHworkers’ sons
1 Paxton et al 2001; 2 Contel & Kerr 1976; Koedam et al 1999, 2002; 3 da Silva 1977; Toth et al 2002; 4 Sommeijer et al 1999 All species singly mated: Peters et al 1999, Contel & Kerr 1976, Paxton et al 2001, Kerr 1975, Kerr et al 1962
Mean, 95% C.L.
Yucatan: Melipona beecheii
Ah Muzencab
M. beecheii caste ratios
0
0.05
0.1
0.15
0.2
0.25
J F M A M J J A S O N D
Pro
p.
of
qu
een
s p
rod
uced Max. = 21% Average = 14.6%
10 cols.8,162 ind.
95% C.L.
Moo-Valle, Quezada-Euan and Wenseleers 2001 Insectes Sociaux
0
5
10
15
20
25%
of
qu
ee
ns
pro
du
ce
d
0
5
10
15
20
25
% males workers’ 0% 34% 41% 95% sons
predicted level HIGHEST > INTERMEDIATE > LOWESTof queen production
M. b
eech
eii1
Yucata
n, Mex
ico
M. q
uadrif
asci
ata
4
Vario
us si
tes,
Bra
zil
M. s
ubnitida
3
Rio G
rande
do Norte
, Bra
zil
M. b
eech
eii2
Yucata
n, Mex
ico
M. f
avosa
5
Tobago, W
est I
ndies
*
*78 / 10 / 13,514
9 / 11 / 2,8066 / 2 / 3,989
10 / 12 / 8,162
3 / 1 / 2,476
Cols. / months / indiv’s.
* GLZ, p < 10-
10N.S
.
Test: interspecies comparison
1 Darchen & Delage-Darchen 1975; 2 Moo-Valle et al 2001; 3 Koedam et al 1999, 2002; 4 Kerr 1950; 5 Sommeijer et al 2002
Mean, 95% C.L.
0
5
10
15
20
25
% o
f q
ue
en
s p
rod
uc
ed
0
5
10
15
20
25
N.S
.
*
*
Data from months with maximum queen production only
M. q
uadrif
asci
ata
3
Vario
us si
tes,
Bra
zil
M. s
ubnitida
2
Rio G
rande
do Norte
, Bra
zil
M. b
eech
eii1
Yucata
n, Mex
ico
M. f
avosa
4
Tobago, W
est I
ndies
1 Moo-Valle et al 2001; 2 Koedam et al 1999, 2002; 3 Kerr 1950; 4 Sommeijer et al 2002
% males workers’ 0% 34% 41% 95% sons
predicted level HIGHEST > INTERMEDIATE > LOWESTof queen production
Mean, 95% C.L.
* GLZ, p < 10-
10
Test: interspecies comparison
MULTIPLE MOTHER QUEENSlowers relatedness
should cause even greater queen overproduction
Future test: Melipona bicolor
Summary
Melipona females selfishly exploit colony by developing as queens
causes “tragedy of the commons”: queen overproduction
reduced exploitation when costs are to close kin (workers’ sons)
Alternative explanations for excess queen production
in Melipona ?
1. Kerr’s theory of genetic caste determination
♀♀ ♀
♀
♀♀ ♀♀
Kerr (1950) proposed2-locus 2-allele systemfor Melipona
females heterozygous at both loci develop into queens
results in 25% queens
Different levels of explanation
not an alternative hypothesis –different level of explanation (Alcock 1993) :
Kerr’s hypothesis suggests HOW the observed caste ratios could come about (PROXIMATE)
Caste conflict theory explains WHY the caste ratios are as observed (ULTIMATE)
cf. XY-sex determination as an efficient mechanism to attain optimal 1:1 sex ratioin mammals
2. Insurance against queen loss?
queen are overproduced to ensure that continuous stock of queens is present
bet-hedging argument
queen overproduction is far too high
queen replacement takes 10 daysin this period up to 70 queens are produced
there are other ways to ensure a continuous stock of queens
Queen stocks kept in prisonsIn Trigonini stingless bees, e.g. Plebeia remota
ensures that continuous stock of queens is present without having to overproduce them
What about other social insects?
other swarming social insects: queen-worker size dimorphism– army ants– honey bees– trigonine (non-Melipona) stingless bees
caste fate enforced via food control
results in few queens being produced
makes individuals work for the benefit of society and develop as a worker, even when not in best interests of individuals themselves
Queen rearing in honey bees
Policing of caste fate: food control
Honey bee
multiply mated: Rf=0.3, Rm=0.25
females would like to become queens with prob. of (1-Rf) / (1+Rm) = 56%
only 0.02% actually become queens
strong divergence between individual and colony optimum
females are coerced into a working role
Queen rearing in trigonine bees
Policing of caste fate: food control
Evasion of caste policing:dwarf queens
observations– occur in ants and trigonine bees– same size as workers– produced in excess– can reproduce, although usually less
fecund
hypothesis– selfish strategy to overcome worker
feeding control?
support– overproduced relative to normal queens
46
Q
q
q
Q
b
caa
ddq Qw
Plebeia remota
dwarf queen
normal queen2 mm
Frequency of dwarf queens
overproduced relative to normal queens– E.g. Schwarziana quadripunctata– 1 in 85 worker cells (1.2%) yield dwarf queens– only 1 in 620 females reared as normal queens (0.16%)– i.e. 88% of all queens produced are dwarf queens &
produced in 7-fold excess relative to normal queens
excess queens are killed by workers as in Melipona
as predicted by caste conflict theory !
49
Caste conflict in termites
Development and killing of excess reproductives
TERMOPSIDAE Porotermes adamsoni Mensa-Bonsu 1976Lenz 1985
KALOTERMITIDAE Kalotermes flavicollis Ruppli 1969, Lüscher 1952, 1956, 1974
Neotermes connexus Myles & Chang 1984
Neotermes jouteli Nagin 1972
Cryptotermes brevis Lenz et al. 1985
RHINOTERMITIDAE Reticulitermes lucifugus Buchli 1956
Reticulitermes santonensis
Wenseleers, Korb & Ratnieks, in prep.
Summary
social insect caste system provides scope for conflict
caste conflict may cause significant costs to the society
(Melipona – queen overproduction)
coercion is more effective than kinship in suppressing caste conflict
What can we learn from all this?
Insight into conflict resolution
Self determination20% queen production
stingless bees
Policing of caste fate0.02% queen production
honey bees
Individual Freedom Causes a Cost to Society
But females prefer to become
queen with probability
of 56% !
Efficient Society but
No Individual Freedom
THE SAME TENSION OCCURS IN HUMAN SOCIETY !
Bourke A.F.G., Ratnieks F.L.W. 1999. Kin conflict over caste determination in social Hymenoptera. Behavioral Ecology & Sociobiology 46: 287-297.
Moo-Valle H., Quezada-Euán J.J.G., Wenseleers T. 2001. The effect of food reserves on the production of sexual offspring in the stingless bee Melipona beecheii (Apidae, Meliponini). Insectes Sociaux 48: 398-403.
Ratnieks F.L.W., Monnin T., Foster K.R. 2001. Inclusive fitness theory: novel predictions and tests in eusocial Hymenoptera. Annales Zooogici Fennici 38: 201-214.
Ratnieks F.L.W. 2001. Heirs and spares: caste conflict and excess queen production in Melipona bees. Behavioral Ecology & Sociobiology 5: 467-473.
Wenseleers T., Ratnieks F.L.W., Billen J. 2002. Conflict over caste fate in social insects: a tragedy of the commons examined. Submitted.
Wenseleers T., Ratnieks F.L.W. 2002. Tragedy of the commons in bees. Submitted.
PDF reprints and talk at www.shef.ac.uk/projects/taplab/twpub.html
References
Acknowledgements
Collaborators
V-L. Imperatriz-Fonseca, M. de F. Ribeiro, D. de A. Alves (SP, Brazil)
H. Moo-Valle, J. Quezada-Euán and Luis Medina-Medina (Dept. of Apiculture, Merida, Mexico)R. Paxton (Tübingen, Germany)
Funding
British CouncilFWO-VlaanderenVlaamse LeergangenEU ‘INSECTS’ and ‘Social Evolution’ NetworksMarie Curie Fellowship