CONFLICT AND COOPERATION

Jacobus J. Boomsma

Institute of Biology University of

Copenhagen

Parasitism versus Mutualism

Resource Allocation

Sex

Cooperation does not come easy

• Who gives alarm calls?• Can policing and punishment evolve?• Are policing and punishment necessary

for stable cooperation?• How important are kinship and

reciprocity?• How special are human societies?• Reciprocal exploitation and conflicts in

mutualisms

Evolution is essential for all biology

“Nothing in biology makes sense,

except in the light of evolution”

(Dobzhansky, 1973)

A Portrait Gallery of Evolutionary Biologists

1800 1850 1900 1950 2000

Malthus

Darwin

Wallace

Source of inspiration

A Portrait Gallery of Evolutionary Biologists

1800 1850 1900 1950 2000

Malthus

Darwin

Wallace

Mendel

Source of inspiration

A Portrait Gallery of Evolutionary Biologists

1800 1850 1900 1950 2000

Malthus

Darwin

Wallace

Mendel

Fisher

Haldane

Wright

Source of inspiration

A Portrait Gallery of Evolutionary Biologists

1800 1850 1900 1950 2000

Malthus

Darwin

Wallace

Mendel

Fisher

Haldane

Wright

Dobzhansky

Mayr

Source of inspiration

The roots of Behavioral Ecology: Tinbergen, Hamilton

and WilliamsTinbergen (1963)

Survival valueof behaviour

Hamilton (1964)

Evolutionaryroots of social behaviour

Williams (1966)

The first synthesis

Ecology is essential for understanding evolution

• “ Nothing in biology makes sense, except in the light of evolution ”

(Dobzhansky, 1973)

• “ Very little in evolution makes sense except in the light of ecology ”

(Townsend, Harper & Begon, 2000)

“Ecology provides the stageon which the “evolutionary play” is performed”

Darwinian Ecology

Evolutionary Ecology proper (animals, plants, micro-

organisms)

Behavioural Ecology (animals)

Sociobiology (social animals)

Darwinian Ecology

Natural selection and Sexual selection

Kin selection:The only realInnovation

after Darwin

e.g. Life Histories

Darwinian sexual selection

Female choice Male-male competition

Darwin’s Problem with Insect Societies

“ I……… will confine myself to one special difficulty, which at first appeared to me insuperable, and actually fatal to my whole theory. I allude to the neuters or sterile females in insect communities: for these neuters often differ widely in instinct and in

structure from both the males and the fertile females, and yet, from being sterile, they cannot propagate their kind.”

Darwin (1859) “The Origin of Species”

queen

workers

Hamilton’s Solution

Reproductive “altruism” evolves when:

br > c b = benefit (extra offspring of

relatives raised because of helping)

r = relatedness of donor to recipient

c = cost (own offspring not raised due to helping)

Parent-offspring conflict (Trivers 1974)

• Benefits gradually decrease per u.o.i.

• Costs stay constant or increase

• Parents weigh costs and benefits equally

• Offspring discount parental costs by their average relatedness to future sibs

Parent-offspring conflict (Trivers 1974)

• Young want more PI (y) than parents are selected to provide (p)

• y-p is even larger when current of future sibs have a different father (maximize B – C/4)

• Mother equally related to all offspring

• Offspring related to itself by r=1

Parent-offspring conflict theory

Dad 2

Dad 1

Mom

Parents Offspring

R.L. Trivers

Genetic relatedness

r = 0.25r = 0.5r = 1.0r = 0.5Parent-offspring conflict and sib-rivalry are relatedness-linked

Reciprocal altruism - The “ prisoner’s dilemma ”

1 2

Swap?

“Defection” is favoured. Mutual cooperation only pays in repeated exchanges.

1 2Defect Cooperate

1 2

1 2

1 2

1 2

Defe

ctC

oopera

te

“ Nature, red in tooth and claw ”

Tennyson (1850)

• Merciless• Exploitative• Fundamentally selfish

• Cooperation in nature needs to be explained by individual (gene) level selection and not by group selection

“Good for the species arguments”

Insect colonies as model systems

Simple ant colony in an acorn

Primitive waspcolony

2 cm 2 cm

From centimeters…...

Large insect colonies

Length: ~100 xArea: ~10 000 xMass: ~1 000 000 x

2 cm

2 m…. to meters

Advanced tropical ant colony

Previous slide

Large colonies are like societies

Tropical honey bee

Tropical waspTropical termite

Long-lived Elaborate nests

Simple and complex family structures

x

x

complexhalf-sib family

offspring

Parentsx

simplefull-sib family

daughter queenmates and takes over

x

x

Queens are specialized egg-laying females

Single queen per colony Multiple queens per colony

Reproduction in haplodiploid social insects (ants, bees,

wasps)

Mother queen

father

Queen ovaries

workers

Not matedNo stored sperm

worker ovaries

worker sons

no Fertiliz ation

queen sons

noFertiliz ation

queen daughters

Fert ilization

Relatedness consequences of haplodiploidy

Mother queen

father

workers

queen sonqueen daughter

worker son

0.75

0.50 (own son)0.375 (other worker’s son)

0.25

0.500.25

0.50

0.500.25

0.00

Reproductive Conflict overSex ratio

and Male production

The conflict over Male Production

Mother queen

father

workers

queen sonqueen daughter

worker son

0.75

0.50 (own son)0.375 (other worker’s son)

0.25

0.500.25

0.50

0.500.25

0.00

When there are more half sisters thanfull sisters workers are selected to

remove each other’s eggs

Worker-Queen Conflict in Ants, Bees, Wasps

• Worker control over sex allocation is common

• Worker production of males is not

Who wins reproductive conflicts ?

In species with small colonies many try to reproduce but queens manipulate reproduction to their own advantage

Queens always win in Bumblebees

Who wins reproductive conflicts ?

In species with large colonies queens monopolize reproduction but workers raise sisters or brothers depending on their own best interests

Workers tend to win sex ratio conflicts in large ant societies

Nepotism is prevented by worker policing

• Queen eggs are marked with a queen pheromone

• Worker male eggslack this pheromone

• Worker eggs arerecognised by other workers and removed

• Worker policing is evolutionary stable in honey bees

Photos and data: Francis Ratnieks

Cooperation does not come easy

• Who gives alarm calls?• Can policing and punishment evolve?• Are policing and punishment necessary

for stable cooperation?• How important are kinship and

reciprocity?• How special are human societies?• Reciprocal exploitation and conflicts in

mutualisms

How special are Human Societies?

• We have culture !!!• But is culture really 100%

independent of genes?• How relevant is fitness in human

societies and can it be measured?• Do humans fit inclusive fitness

theory?• If so, what does this imply?• Cooperation does not come easy

Mutualistic Symbiosis and Co-evolution

mitochondria

gut bacteria

nitrogenbindingbacteria chloroplasts corals

mycorrhizae

lichens

termites and fungiants and fungi

Ectosymbionts of Insect Societies

The Conceptual Paradigm

“Many of the benefits sought by living things are disproportionally available to co-operating groups......

The problem is that while an individual can benefit from mutual co-operation, each one can also do even better by exploiting the co-operative efforts of others”.

R. Axelrod and W.D. Hamilton, The evolution of co-operation. Science 211: 1390-1396 (1981)

When and Why do Symbiotic Partners Cooperate?

• Exploitation and monopolization of novel resources

• Sufficient alignment of reproductive interests to stabilize interactions in spite of potential conflict

• ....... i.e., to allow Stable Bilateral Exploitation

Agricultural Insect Societies

Attine Ants in Panama Macrotermitinae in West Africa

Attine ants Fungus growing termites

Fieldwork in Panama

Panama Canal

Smithsonian TropicalResearch Institute

Ant fungus-farming started simple

Mycocepurus nest

Dead Substrate:

Leaf debrisWood chipsInsect body partsInsect frass

The evolutionary history of fungus-growing ants

Leafcutters

Lower Attines

Higher Attines

Fungusrearing

SpecialClones

LeafcuttingHerbivory

Large Colonies

Ant Phylogeny:

Schultz & Meier (1995) and Schultz et al. unpublished

Mueller et al., 1998

Ant agriculture became “herbivorous”, ……

Split into two genera, …… One of which became really

dominant, ……

QuickTime™ and aCinepak decompressor

are needed to see this picture.

Damaging, ……

Biggggg..

An underground metropoliswhich may live for decades

A society with millions of workers, all daughters of the same long-lived queen

After Jonkman

And highly sophisticated

Atta

From Hölldobler and Wilson, 1990

castes

Acromyrmex

anal droplets gongylidia

The Leafcutter Ants

How an Atta colony starts

Winged queen and male One year old nest

fungusfragment

And What it Finally Becomes

Fungus rearing Assembly Lines

• Evolution towards clonal fungi

• More genetic diversity of ants per nest via multiple queen mating

• Worker policing phenomena expected

Photo: Mark W. Moffett

Ongoing work Mischa Dijkstra

Genetic Marker Studies

Microsatellite tandem repeat sequence

# repeats variable among individuals

Villesen, Murakami, Schultz & Boomsma (2002)

Leafcutters

Lower Attines

Higher Attines

Leafcutter Ants Have Highly Harmonious Societies

Large Colonies, Worker Castes & Live Substrate associated with genetic diversity

A Symbiosis of at least four parties

C. CurrieM. Poulsen

From Schultz, 1999

Acromyrmex As Laboratory Model System

Three sympatric species inGamboa, Panama:A. octospinosusA. echinatiorA. insinuator (inquiline)

Division of labour

Ac. echinatior

0

0.1

0.2

0.3

0.4

0.5

0.6

0.6 0.8 1 1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 2.8

Head width (mm)

Pro

po

rtio

n o

f sa

mp

le

Internal

ForagersAcromyrmex echinatior

Data: Bill Hughes

How to cope with parasites and

diseases?

Incompatibility Issues

Acromyrmex

0

1

2

3

0 0,05 0,1 0,15 0,2 0,25 0,3 0,35 0,4 0,45

Inco

mp

atib

ility

re

act

ion

Mean genetic distance

Inco

mpa

tibi

lity

Social parasites: Do not build nests, but simply move in

Acromyrmex echinatior host

Picture: Klaus LechnerParasites never carry Streptomyces

Parasite and host are sister species

The world’slargest and smallest ant

“Go to the ant, thou sluggard: consider her ways, and be

wise”Proverbs 6:6

The discussion program this afternoon

• A recapitulation of social insect conflicts • An experimental study of policing and

punishment in ants• Linking social evolution in insects and

vertebrates• How important is kinship in

vertebrates?

The conflict over Male Production

Mother queen

father

workers

queen sonqueen daughter

worker son

0.75

0.50 (own son)0.375 (other worker’s son)

0.25

0.500.25

0.50

0.500.25

0.00

Queen always values own son most (0.5)Worker always values own son most (0.5)

Workers prefer full sister sons (0.375) over queen sons (0.25)

Workers prefer queen sons (0.25) over half sister sons (0.125)

SPLIT SEX RATIO THEORYBoomsma & Grafen 1990, 1991

SINGLE MATINGHIGH RA

“SPECIALIZE IN FEMALES”

MULTIPLE MATINGLOW RA

“SPECIALIZE IN MALES”

rf = 0.75rm = 0.25

RA=3rf = 0.50rm = 0.25

RA=ca. 2

Formica truncorum Sex allocation

Queen singly mated Queen multiply mated

0

1

2

3

4

5

6

7

8

0 - 0.2 0.2 - 0.4 0.4 - 0.6 0.6 - 0.8 0.8 - 1.0

1989

Investment in females

Nu

mb

er

of

colo

nie

s

Who wins reproductive conflicts ?

Males posthumously manipulate worker reproductive strategiesby clumping sperm After Hölldobler and Wilson, 1990

Sperm storage organ

Reproductive organsFormica queen

Formica nest mound

Males?