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