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The evolution of conflict and cooperation in insect societies: towards greater realism in inclusive fitness models. Tom Wenseleers Department of Biology University of Leuven, Belgium tom.wenseleers@bio.kuleuven.be. Conflict & cooperation. insect societies: highly cooperative

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slide1

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

Tom Wenseleers

Department of Biology

University of Leuven, Belgium

tom.wenseleers@bio.kuleuven.be

conflict cooperation
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

the evolutionary basis of conflict
The evolutionary basisof conflict

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)

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

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

success stories of if theory
Success stories of IF theory

sex-ratios

(nepotistic queen rearing)

variation in male parentage andpatterns 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
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)

slide6

Large variation in male parentage found which is not causedby 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
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 accuratequantitative predictions
  • approach: Frank (1997): costs & benefits are not taken to be simple constants but are calculated by differentiating fitness functions
caste determination
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)

Honey bee

Stingless bees(trigonines)

Army ants

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

slide10

Honeybee: trophic caste determination

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

slide11

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
Exception: Melipona stingless bees

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)

“Power” to the individual larvae, social control impossible

slide13

Queen overproduction

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

Ratnieks & Wenseleers Science 2006

slide14

Evidence for self determination (1)

Melipona beecheii

queens

workers

meansqueens: 11.4 mg

workers: 11.6 mgGLM, F1=1.06, p=0.4

Wenseleers et al. Ethology 2003

slide15

Evidence for self determination (2)

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

slide16

Most excess queens killed...

Wenseleers et al. Ethology 2003

slide17

...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

slide18

Levels of queen production

M. quinquefasciata

M. seminigra

M. pseudocentris

M. beecheii

M. interrupta

M. bicolor

SELF DETERMINATION

Queens reared in worker cellsExcess queens reared

“anarchy”

M. melanoventer

M. quadrifasciata

M. subnitida

M. marginata

M. scutellaris

M. fuliginosa

M. asilvae

M. rufiventris

M. favosa

M. trinitatis

M. compressipes

Trigona amalthea

TROPHIC CASTE DETERMINATION

Queens reared in queen cellsOptimal # of queens reared

Trigona ventralis

Trigona ruficrus

S. postica

S. bipunctata

Tetragonisca angustula

Apis mellifera

0.01%

0.10%

1.00%

10.00%

100.00%

% of females reared as queens

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

various mechanistic explanations 1
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)

various mechanistic explanations 2
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

develop as workers develop as queens

threshold

Frequency distribution

9-25% develop as queens

Geraniol content of a given cell

inclusive fitness model
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 withqueen 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.

slide23

Quantitative fit

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%

Kerr model

model Wenseleers et al.

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

more detailed model
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
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...

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.

worker

queen

queen policing
Queen policing

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

Common bumblebee

Courtesy of the BBC series “Life in the Undergrowth”

worker policing
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

Ratnieks & Visscher Nature 1989

worker policing1
Worker policing

German wasp Vespula germanica

Bonckaert et al. Beh. Ecol. 2008

inclusive fitness model1
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 eggs

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

theoretical prediction queenright cololonies
Theoretical prediction: queenright cololonies

15

% of laying workers set mainly

by effectiveness of policing

not by relatedness

10

ESS % of laying workers

5

0.5

0.6

0.7

0.8

0.9

1

Effectiveness of policing (P)

Wenseleers et al. J. Evol. Biol. 2003

theoretical prediction queenless colonies
Theoretical prediction: queenless colonies

60

% of laying workers higher

when relatedness is lower

50

linear cost function

40

ESS % of laying workers

30

20

concave cost function

10

0

0.4

0.5

0.6

0.7

Relatedness among workers

Wenseleers et al. J. Evol. Biol. 2003

explaining variation in the of egg laying workers
Explaining variation in the % of egg laying workers
  • 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
effect of policing
Effect of policing

Asian paper wasp

30

saxon wasp

level of selfishness

red wesp

% of egg-laying workers

10

tree wasp

Norwegian wesp

median wesp

5

hornet

German wasp

common wasp

honeybee

0

Wenseleers & Ratnieks Nature 2006

policing reduces the incentive to selfishly lay eggs

30

50

70

80

90

95

98

99

100

effectiveness of the policing

effect of relatedness
Effect of relatedness

Asian paper wasp

Polistes chinensis

25

25

saxon wasp

Dolichovespula saxonica

tree wasp

red wasp

D. sylvestris

Vespula rufa

7.5

7.5

Norwegian wasp

D. norwegica

5

5

median wasp

D. media

2.5

2.5

German wasp

Vespula germanica

level of selfishness

hornet

Vespa crabro

% of egg-laying workers

common wasp

0.75

0.75

Vespula vulgaris

0.5

0.5

0.25

0.25

0.075

0.075

honeybee

Apis mellifera

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

Wenseleers & Ratnieks Nature 2006

0.3

0.3

0.4

0.4

0.5

0.5

0.6

0.6

0.7

0.7

genetic relatedness

slide38

RELATEDNESSLOW HIGH

100

100

ANTS

MIEREN

BEES

BIJEN

WESPEN

WASPS

Workers most related tothe sons of other workers

werksters meest verwantmet zonen koningin→ worker policing

% adult males producedby workers

Workers most relatedto the sons of the queen

10

10

1

1

t-test, p=0.0000000001

n=90 species

0

0

-

-

0.15

0.15

-

-

0.10

0.10

-

-

0.05

0.05

0.00

0.00

0.05

0.05

0.10

0.10

0.15

0.15

relatedness difference between workers’ and queen’s sons

Wenseleers & Ratnieks Am. Nat. 2006

in queenless colonies basic relatedness prediction recovered
In queenless colonies: basic relatedness prediction recovered

40

honeybee

35

german wasp

30

common wasp

Asian paper wasp

25

level of selfishness

% of egg-laying workers

red wasp

20

tree wasp

15

median wasp

saxon wasp

10

hornet

norwegian wasp

5

0

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

0.3

0.4

0.5

0.6

0.7

Wenseleers & Ratnieks Nature 2006

genetic relatedness

supports worker control
Supports worker control

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.

queenrightqueenless

35

30

25

20

% of egg-laying workers

15

10

5

0

0.3

0.4

0.5

0.6

0.7

relatedness among workers

slide41

What about the variation in specieswith single-matedqueens?

RELATEDNESSLOW HIGH

100

100

ANTS

MIEREN

BEES

BIJEN

WASPS

WESPEN

werksters meest verwantmet zonen koningin→ worker policing

% adult males producedby workers

10

10

1

1

0

0

-

-

0.15

0.15

-

-

0.10

0.10

-

-

0.05

0.05

0.00

0.00

0.05

0.05

0.10

0.10

0.15

0.15

relatedness difference between workers’ and queen’s sons

variation in male parentage not linked to policing
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 model2
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 commonif colony produces a lot of workers, i.e. if the queen lays mostly female eggs (smaller colony-level cost)
conclusion1
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!

acknowledgements
Acknowledgements

F.LW. Ratnieks

D.A. Alves

V.L. Imperatriz-Fonseca

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