Tom Wenseleers Department of Biology University of Leuven, Belgium [email protected]

The evolution of conflict and cooperation in insect societies: towards greater realism in

inclusive fitness modelsTom Wenseleers

Department of BiologyUniversity of Leuven, Belgium

[email protected]

Conflict & cooperation• insect societies: highly

cooperative• but conflicts over reproduction

can occur• these conflicts can be

understood on the basis of Hamilton's inclusive fitness theory

Ratnieks, Foster & Wenseleers Ann. Rev. Entomol. 2006

William D. Hamilton : inclusive fitness theory "The Genetical Evolution of Social Behaviour" (1964, J. Theor. Biol.)

Robert Trivers & Hope Hare “Haplodiploidy and the Evolution of Social Insects" (1976, Science)

The evolutionary basisof conflict

Various relatedness asymmetries (e.g.between sisters and brothers) within insectsocieties are a source of conflict

Inclusive fitness theoryIndividuals selected to help relatives, potentiallyat a cost of more distant relatives

Success stories of IF theory• sex-ratios• (nepotistic queen rearing)• variation in male parentage and

patterns of queen and worker policing (mostly)

• but there are also some putative "exceptions" where empirical data do not fit basic relatedness predictions so well, and this has led to a certain amount of skepticism about IF theory

Ratnieks, Foster & Wenseleers Ann. Rev. Entomol. 2006

Skepticism about IF theory"It is often said in research reports on social insects that

some particular set of empirical data is “consistent with kin selection theory.” But the same can be said of almost any other imaginable result, and the particular connection of data to the theory remains unclear. Hence, kin selection theory is not wrong. It is instead constructed to arrive at almost any imaginable result, and as a result is largely empty of content. Its abstract parameters can be jury-rigged to fit any set of empirical data, but not built to predict them in any detail, nor have they been able to guide,with a few exceptions, research in profitable new directions."

"the theory has contributed little or nothing not already understood from field and experimental studies"

(E.O. Wilson BioScience 2008)

Large variation in male parentage found which is not caused by variation in relatedness. E.g. stingless bees: all species have single mated queens, yet worker reproduction varies massively, with 0-98% of all males being workers' sons in different species. Why the variation?

Costs & benefits• how can these so-called "exceptions" of kin selection

theory be explained?• usually they stem from naive application of the theory,

taking into account only relatedness, and not the costs & the benefits

• the aim of my studies was to develop more realistic IF models that modelled costs & benefits in much more detail, allowing me to obtain much more accurate quantitative predictions

• approach: Frank (1997): costs & benefits are not taken to be simple constants but are calculated by differentiating fitness functions

First series of models:caste determination

Queens are usually larger than workers. This allows nestmates to force females to develop as workers by rationing their food intake.(trophic caste determination)

Bourke & Ratnieks 2001 Beh. Ecol. Sociob.; Wenseleers et al. 2003 J. Evol. Biol.

Honey bee Stingless bees(trigonines)

Army ants

Caste determination

Individuals cannot choose their own caste fate. Only 1 in 10,000 is allowed to become a queen.

Honeybee: trophic caste determination

Most stingless bees: trophic caste determination

queen cell

Individuals cannot choose their own caste fate. Only c. 1 in 5,000 is allowed to become a queen.

Exception: Melipona stingless bees

“Power” to the individual larvae, social control impossible

queens and workers same size

produced in identical, sealed cells

caste fate cannot be enforced, and instead is expected to be determined by individual genotype

caste fate conflict theory: larvae better of if they become queens

leads to many larvae "selfishly" developing as queens(queen overproduction)

Ratnieks & Wenseleers Science 2006

Melipona stingless beesca. 10% of the female larvae develop as queens

represents a queen overproduction, since queens are needed only sparingly, to swarm or replace a failing mother queen

consistent with the idea that larvae control their own caste development and that many selfishly develop as queens

Queen overproduction

Dry weight (mg)

No

of o

bs

7 8 9 10 11 12 13 14 150

20

40

60

80

100

120

140

Melipona beecheii queensworkers

meansqueens: 11.4 mgworkers: 11.6 mg

GLM, F1=1.06, p=0.4

Evidence for self determination (1)

Wenseleers et al. Ethology 2003

Evidence for self determination (2)

No

of o

bs

M. scu te lla ris

-0 .5 -0.4 -0 .3 -0.2 -0 .1 0.0 0 .1 0.2 0 .3 0.4 0 .5 0.60

20

40

60

80

10 0

12 0

14 0

M. b ico lo r

-0 .5 -0 .4 -0 .3 -0 .2 -0 .1 0 .0 0 .1 0.2 0.3 0.4 0 .5 0.6

M. ru five n tris

-0 .5 -0 .4 -0 .3 -0 .2 -0 .1 0 .0 0 .1 0.2 0 .3 0.4 0 .5 0 .6

M. a silva i

-0 .5 -0.4 -0 .3 -0.2 -0 .1 0.0 0 .1 0.2 0 .3 0.4 0 .5 0.60

20

40

60

80

10 0

12 0

14 0

M sub n itida

-0 .5 -0 .4 -0 .3 -0 .2 -0 .1 0 .0 0 .1 0.2 0.3 0.4 0 .5 0.6

M. favo sa

-0 .5 -0 .4 -0 .3 -0 .2 -0 .1 0 .0 0 .1 0.2 0 .3 0.4 0 .5 0 .6

M. b ee che i i

-0 .5 -0.4 -0 .3 -0.2 -0 .1 0.0 0 .1 0.2 0 .3 0.4 0 .5 0.60

20

40

60

80

10 0

12 0

14 0

M. m arg ina ta

-0 .5 -0 .4 -0 .3 -0 .2 -0 .1 0 .0 0 .1 0.2 0.3 0.4 0 .5 0.6

• data from 413 combs from 8 different species: gynes are randomly distributed in combs

D.A. Alves, V.L. Imperatriz-Fonseca, P. Santos-Filho & T. Wenseleers, unpublished data

Most excess queens killed...

Wenseleers et al. Ethology 2003

...a minority escapes being killed by parasitizing queenless colonies

• Melipona scutellaris: some virgin queens escape being killed by leaving the colony and parasitizing unrelated queenless hives

• if the mother queen dies in 25% (6/24) of the cases it is replaced by an unrelated queen coming from other queenright colony

T. Wenseleers, D.A. Alves, T. Francoy, J. Billen & V.L. Imperatriz-Fonseca, unpublished data

0.01% 0.10% 1.00% 10.00% 100.00%

% of females reared as queens

M. quinquefasciataM. seminigra

M. pseudocentrisM. beecheii

M. interruptaM. bicolor

M. melanoventerM. quadrifasciata

M. subnitidaM. marginataM. scutellarisM. fuliginosa

M. asilvaeM. rufiventris

M. favosaM. trinitatis

M. compressipes

Trigona amaltheaTrigona ventralisTrigona ruficrus

S. posticaS. bipunctata

Tetragonisca angustulaApis mellifera

TROPHIC CASTE DETERMINATIONQueens reared in queen cellsOptimal # of queens reared

Levels of queen production

SELF DETERMINATIONQueens reared in worker cells

Excess queens reared“anarchy”


Can we predict the absolute levels of queen production?

Various mechanistic explanations (1)

Kerr (1950) proposed a 2-locus 2-allele system for Melipona

females heterozygous at both loci develop into queens

would result in 25% queens

system could be generalized to 3 or 4 loci, resulting in 12% or 6% of queens

yet the Kerr hypothesis does not explain why only Melipona would have this caste determination mechanism, nor why queen production should be so high, or why it should be 6%, 12% or 25%.(proximate, not an ultimate explanation)

develop as workers develop as queens

Various mechanistic explanations (2)

S. Jarau & M. Ayasse (Sunday)

larvae in cells that contain a high amount of geraniol develop as queens

interesting, as it provides a theory about what cue larvae could use to decide to develop as either a queen or a worker

but does not explain why larvae would put their threshold at a certain level

again, provides a proximate, but not an ultimate explanation

Geraniol content of a given cell

Freq

uenc

y di

strib

utio

n

threshold

9-25% develop as queens

Inclusive fitness model• assume larvae can control their own caste

fate, and develop with a genetically determined probability into either a queen or a worker

• assume that relative colony productivity (swarm and male production) decreases linearly with queen overproduction (mean prob. that larvae develop as queens)

• what is the evolutionarily stable probability of developing as a queen?

• result model: single mating (stingless bees): 14-20% of all larvae selected to

develop as queens depending on male parentage

Wenseleers et al. 2003 J. Evol. Biol.

Quantitative fit

1.00% 10.00% 100.00%









M. compressipes

1.00% 10.00% 100.00%









M. compressipes

Kerr model

model Wenseleers et al.

In terms of absolute quantitativefit neither the model of W. Kerrnor my model is fully satisfactory

Observed levels of queenproduction generally below 14% or 20%


More detailed model original model assumed that colony productivity drops to zero when

all females develop as queens

more detailed model: colony is unable to grow and produce new swarms when the rate at which new workers are produced equals the rate at which they die

this results in swarm production dropping to zero when c. 40% of all females develop as queens (based on literature data on worker mortality, the % of eggs laid that are female and the number of new cells provisioned per day per worker)

depending on parameters, this results in an ESS whereby 5-20% of all females should develop as queens: excellent quantitative fit to observed data

only if worker mortality is close to zero does the ESS reduce to that obtained in the original, simpler model

T. Wenseleers, unpublished

Conclusion

• inclusive fitness models can be developed to make very concrete predictions, in this case about what % of female larvae should develop as queens in different bee species

• the quantitative fit to empirical data increases as the model is made more realistic, e.g. implementing the details of how colonies grow and reproduce, etc...

Second series of models:worker reproduction

Worker reproduction

Workers can lay unfertilised male eggs and would be expected to benefit from doing so since they are always more related to sons than to brothers. Causes a queen-worker conflict over male parentage.

queen worker

Queen policing

Common bumblebeeCourtesy of the BBC series “Life in the Undergrowth”

Queen selected to prevent workers from reproducing since she is more related to sons than grandsons.

Ratnieks & Visscher Nature 1989

Worker policing

Workers can also prevent each other from reproducing by eating each others eggs, and are selected to do so particularly when they are collectively most related to the queen's sons (i.e. under multiple mating) or when suppressing worker reproduction increases colony productivity or makes the colony sex-ratio more female biased

Worker policing

German wasp Vespula germanicaBonckaert et al. Beh. Ecol. 2008

Inclusive fitness model• assume that workers in a colony become egg-layers with

a genetically set probability • assume that relative colony productivity decreases as

the % of egg-laying workers goes up (due to a shortage of foragers) and that worker reproduction does not change the sex-ratio

• what is the evolutionary stable probability to become an egg-laying worker?

• if there is no policing: low relatedness should result in greater selfishness, and a greater % of workers laying eggs

• presence of policing: reduces the benefit of laying eggsWenseleers, Helantera & Ratnieks 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.

Theoretical prediction: queenright cololonies

0.5 0.6 0.7 0.8 0.9 1

5

10

15

Effectiveness of policing (P)

ESS

% o

f lay

ing

wor

kers % of laying workers set mainly

by effectiveness of policing not by relatedness

Wenseleers et al. J. Evol. Biol. 2003

Theoretical prediction: queenless colonies

0.4 0.5 0.6 0.7

10

20

30

40

50

0

60

Relatedness among workers

ESS

% o

f lay

ing

wor

kers

% of laying workers higherwhen relatedness is lower

linear cost function

concave cost function

Wenseleers et al. J. Evol. Biol. 2003

- comparative study of 10 species (9 wasps+honeybee) with variable % of egg laying-workers

- correlate worker egg-laying with relatedness and the effectiveness of the policing system

Explaining variation in the % of egg laying workers

effectiveness of the policing

leve

l of s

elfis

hnes

s

10099989590807050300

5

10

30

% o

f egg

-layi

ng w

orke

rs Asian paper wasp

tree wasp

Norwegian wespmedian wesp

honeybee

red wesp

saxon wasp

hornet

German waspcommon wasp

Effect of policing

policing reduces the incentive to selfishly lay eggs

Wenseleers & Ratnieks Nature 2006

0.3 0.4 0.5 0.6 0.7

0.075

0.25

0.50.75

2.5

57.5

25Polistes chinensis

Apis mellifera

Vespula germanica Vespa crabro

D. media

Vespula rufa

Dolichovespula saxonica

Vespula vulgaris

D. norwegica

D. sylvestris

0.3 0.4 0.5 0.6 0.7

genetic relatedness

0.075

0.25

0.50.75

2.5

57.5

25Asian paper wasp

honeybee

German wasp hornet

median wasp

red waspsaxon wasp

common wasp

Norwegian wasp

tree wasp

leve

l of s

elfis

hnes

s

% o

f egg

-layi

ng w

orke

rs

Effect of relatedness

opposite to basic relatedness prediction but in line with species with low relatedness having more policing (red)

Wenseleers & Ratnieks Nature 2006

t-test, p=0.0000000001n=90 species

RELATEDNESSLOW HIGH

Wenseleers & Ratnieks Am. Nat. 2006

werksters meest verwantmet zonen koningin→ worker policing

-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15

0

1

10

100 MIERENBIJENWESPEN

-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15

0

1

10

100 ANTSBEESWASPS

Workers most relatedto the sons of the queen

Workers most related tothe sons of other workers

relatedness difference between workers’ and queen’s sons

% a

dult

mal

es p

rodu

ced

by w

orke

rs

german wasp

red wasp

common wasp

hornet

median wasp

norwegian wasp

tree wasp

saxon wasp

Asian paper wasp

honeybee

genetic relatedness

in queenless colonies:no policing and the basic relatedness prediction is recovered

In queenless colonies: basic relatedness prediction recovered

% o

f egg

-layi

ng w

orke

rs

0

5

10

15

20

25

30

35

40

0.3 0.4 0.5 0.6 0.7Wenseleers & Ratnieks Nature 2006

leve

l of s

elfis

hnes

s

Supports worker control

0.3 0.4 0.5 0.6 0.70

5

10

15

20

25

30

35

% o

f egg

-layi

ng w

orke

rs

queenrightqueenless

relatedness among workers

Large difference between % of egg laying workers in QR and QL colonies for species with worker policing (red, where in presence of the queen workers are selected not to lay eggs); small difference for the other species (green).

Supports the idea that workers respond to the queen signal in their own best interests ("worker control") and that they are not coerced by the queen.

RELATEDNESSLOW HIGH

werksters meest verwantmet zonen koningin→ worker policing

-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15

0

1

10

100 MIERENBIJENWESPEN

-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15

0

1

10

100 ANTSBEESWASPS

relatedness difference between workers’ and queen’s sons

% a

dult

mal

es p

rodu

ced

by w

orke

rsWhat about the variation in specieswith single-matedqueens?

Variation in male parentage not linked to policing

• e.g. stingless bees: worker reproduction usually not policed, no variation in relatedness (r = 0.75)

• yet worker reproduction varies massively: 0-98% of all males workers' sons

• possible explanation: colony-level cost: if workers deposit a male egg in a cell it will reduce the number of workers produced since worker-laid eggs will also compete with female eggs laid by the queen

Inclusive fitness model

• assume workers replace a random queen-laid egg with an own egg with a genetically set probability

• since they will end up replacing some female worker-destined eggs with male eggs this will result in a reduced colony productivity (differential equation model)

• determine the ESS probability for a worker to replace a random queen-laid egg with an own egg

• prediction: worker reproduction should be more common if colony produces a lot of workers, i.e. if the queen lays mostly female eggs (smaller colony-level cost)

M. beecheii

M. asilvai

M. scutellaris

M. bicolorM. subnitida

M. marginata

M. quadrifasciata

M. favosa

70 75 80 85 90 95 100

% female eggs laid by queen

0

20

40

60

80

100%

mal

es w

orke

rs' s

ons

n=8 speciesSpearman R=0.95, p=0.0003

Parameters:0.04 new cells built/day/worker (n=8 sp.)worker life expectancy: 46.5 days (n=4 sp.)

ESS

Prediction supported

Conclusion

• inclusive fitness models can be developed to make very concrete and accurate predictions, such as about what % of female larvae should develop as queens in different bee species, what % of the workers should lay eggs or what % of the males should be workers' sons

• the quantitative fit to empirical data increases as the model is made more realistic, e.g. by implementing the details of how colonies grow and reproduce, etc...

• Wilson's critique is not warranted!

wasp work: F.L.W. Ratnieks, F. Nascimento, A. Tofilski, M. Archer, N. Badcock, W. Bonckaert, T. Burke,

K. Erven, H. Helantera, L. Holman, K. Vuerinckx

stingless bee work: V.L. Imperatriz-Fonseca, D. Alves, T. Francoy, M. Ribeiro, J. Quezada

Acknowledgements

F.LW. Ratnieks

V.L. Imperatriz-Fonseca

D.A. Alves

Tom Wenseleers Department of Biology University of Leuven, Belgium [email protected]

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