CONFLICT AND COOPERATION Sex Parasitism versus Mutualism Jacobus J. Boomsma Institute of Biology University of Copenhagen Resource Allocation

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

Source of inspiration Darwin Malthus Wallace

A Portrait Gallery of Evolutionary Biologists 1800 1850 1900 1950 2000

Source of inspiration Darwin Malthus Mendel Wallace

A Portrait Gallery of Evolutionary Biologists 1800 1850 1900 1950 2000

Source of inspiration Fisher Darwin Malthus Mendel Haldane Wallace Wright

A Portrait Gallery of Evolutionary Biologists 1800 1850 1900 1950 2000

Source of inspiration Fisher Darwin Dobzhansky Malthus Mendel Haldane Mayr Wallace Wright

The roots of Behavioral Ecology: Tinbergen, Hamilton and Williams

Tinbergen (1963) Survival value of behaviour Williams (1966) The first synthesis Hamilton (1964) Evolutionary roots of social behaviour

Ecology is essential for understanding evolution • “ Nothing in biology makes sense, except in the light of evolution ” (Dobzhansky, 1973)

“Ecology provides the stage on which the “evolutionary play” is performed”

• “ Very little in evolution makes sense except in the light of ecology ” (Townsend, Harper & Begon, 2000)

Darwinian Ecology Evolutionary Ecology proper (animals, plants, micro-organisms) Behavioural Ecology (animals) Sociobiology (social animals)

Darwinian Ecology Kin selection: The only real Innovation e.g. Life Histories after Darwin

Natural selection and Sexual selection

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:

queen

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.”

workers

Darwin (1859) “The Origin of Species”

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 ( to provide ( p ) y ) than parents are selected • 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 Parents Dad 1 Mom Dad 2 Offspring

R.L. Trivers

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

r = 1.0

r = 0.5

Genetic relatedness

r = 0.25

Reciprocal altruism - The “ prisoner’s dilemma ” 1 2 Defect 1 Swap?

2 Cooperate 1 2 1 2 1 2 1 2

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

“ 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”

2 cm Insect colonies as model systems 2 cm Primitive wasp colony Simple ant colony in an acorn

From centimeters…...

Large insect colonies

2 cm Previous slide …. to meters 2 m

Length: ~100 x Area: ~10 000 x Mass: ~1 000 000 x Advanced tropical ant colony

Large colonies are like societies Tropical wasp Tropical honey bee Long-lived Elaborate nests Tropical termite

Simple and complex family structures

x offspring simple full-sib family Parents complex half-sib family x x x x daughter queen mates and takes over

Queens are specialized egg-laying females Single queen per colony Multiple queens per colony

Reproduction in haplodiploid social insects (ants, bees, wasps)

Queen ovaries worker ovaries Mother queen father no Fertiliz ation Fert ilization no Fertiliz ation workers Not mated No stored sperm queen sons queen daughters worker sons

Relatedness consequences of haplodiploidy

Mother queen 0.50

Reproductive Conflict over Sex ratio and Male production

0.25

0.25

0.50

0.75

father workers 0.50 (own son) 0.375 (other worker’s son) 0.25

0.50

0.00

queen son worker son queen daughter

The conflict over Male Production

Mother queen

When there are more half sisters than full sisters workers are selected to remove each other’s eggs

0.25

0.25

0.50

0.50

0.75

father workers 0.50 (own son) 0.375 (other worker’s son) 0.25

0.50

0.00

queen son worker son queen daughter

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 ?

Workers tend to win sex ratio conflicts in large ant societies

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

Nepotism is prevented by worker policing • Queen eggs are marked with a queen pheromone • Worker male eggs lack this pheromone • Worker eggs are recognised 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 nitrogen binding bacteria mycorrhizae chloroplasts gut bacteria Ectosymbionts of Insect Societies mitochondria lichens corals ants and fungi termites and fungi

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 Smithsonian Tropical Research Institute Panama Canal

Ant fungus-farming started simple Dead Substrate: Leaf debris Wood chips Insect body parts Insect frass Mycocepurus nest

The evolutionary history of fungus-growing ants Lower Attines Ant Phylogeny: Schultz & Meier (1995) and Schultz et al. unpublished Mueller et al., 1998 Fungus rearing Higher Attines Special Clones Leafcutting Herbivory Leafcutters Large Colonies

Ant agriculture became “herbivorous”, ……

QuickTime™ and a Cinepak decompressor are needed to see this picture.

Damaging, ……

Biggggg..

An underground metropolis which may live for decades A society with millions of workers, all daughters of the same long-lived queen

After Jonkman

Atta Acromyrmex

From Hölldobler and Wilson, 1990 castes gongylidia anal droplets

How an

Atta

colony starts

Winged queen and male fungus fragment One year old nest

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 Ongoing work Mischa Dijkstra Photo: Mark W. Moffett

Genetic Marker Studies

Microsatellite tandem repeat sequence # repeats variable among individuals

Leafcutter Ants Have Highly Harmonious Societies Villesen, Murakami, Schultz & Boomsma (2002) Lower Attines Higher Attines Large Colonies, Worker Castes & Live Substrate associated with genetic Leafcutters

A Symbiosis of at least four parties From Schultz, 1999 C. Currie M. Poulsen

Acromyrmex

As Laboratory Model System Three sympatric species in Gamboa, Panama: A. octospinosus A. echinatior A. insinuator (inquiline)

Division of labour Internal Foragers 0.6

0.5

0.4

0.3

0.2

0.1

0 0.6

0.8

1 1.2

1.4

1.6

1.8

2 Head width (mm) 2.2

2.4

2.6

2.8

Data: Bill Hughes

How to cope with parasites and diseases?

Incompatibility Issues

Acromyrmex

3 2 1 0 0 0,05 0,1 0,15 0,2 0,25 0,3 Mean genetic distance 0,35 0,4 0,45

Social parasites: Do not build nests, but simply move in Acromyrmex echinatior host Parasite and host are sister species Parasites never carry Streptomyces Picture: Klaus Lechner

“Go to the ant, thou sluggard: consider her ways, and be wise” Proverbs 6:6

The world’s largest and smallest ant

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

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)

workers 0.25

0.25

0.50

0.50

0.75

father 0.50 (own son) 0.375 (other worker’s son) 0.25

0.50

0.00

queen son worker son queen daughter

SPLIT SEX RATIO THEORY Boomsma & Grafen 1990, 1991 r f = 0.75

r m = 0.25

RA=3

SINGLE MATING HIGH RA “SPECIALIZE IN FEMALES”

r f = 0.50

r m = 0.25

RA=ca. 2

MULTIPLE MATING LOW RA “SPECIALIZE IN MALES”

Formica truncorum

Sex allocation

Queen singly mated 4 3 2 1 0 8 7 6 5 1989 Queen multiply mated 0 - 0.2

0.2 - 0.4

0.4 - 0.6

0.6 - 0.8

Investment in females 0.8 - 1.0

Who wins reproductive conflicts ?

Males?

Reproductive organs Formica queen Formica nest mound Males posthumously manipulate worker reproductive strategies by clumping sperm

Sperm storage organ

After Hölldobler and Wilson, 1990