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

2. 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

3. Evolution is essential for all biology “Nothing in biology makes sense, except in the light of evolution” (Dobzhansky, 1973)

4. A Portrait Gallery of Evolutionary Biologists 1800 1850 1900 1950 2000 Malthus Darwin Wallace Source of inspiration

5. A Portrait Gallery of Evolutionary Biologists 1800 1850 1900 1950 2000 Malthus Darwin Wallace Mendel Source of inspiration

6. A Portrait Gallery of Evolutionary Biologists 1800 1850 1900 1950 2000 Malthus Darwin Wallace Mendel Fisher Haldane Wright Source of inspiration

7. A Portrait Gallery of Evolutionary Biologists 1800 1850 1900 1950 2000 Malthus Darwin Wallace Mendel Fisher Haldane Wright Dobzhansky Mayr Source of inspiration

8. The roots of Behavioral Ecology: Tinbergen, Hamilton and Williams Tinbergen (1963) Survival value of behaviour Hamilton (1964) Evolutionary roots of social behaviour Williams (1966) The first synthesis

9. 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 stage on which the “evolutionary play” is performed”

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

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

12. Darwinian sexual selection Female choiceMale-male competition

13. 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

14. 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)

15. 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

16. 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

17. Parent-offspring conflict theory Dad 2 Dad 1 Mom ParentsOffspring R.L. Trivers Genetic relatedness r = 0.25r = 0.5r = 1.0r = 0.5 Parent-offspring conflict and sib-rivalry are relatedness-linked

18. Reciprocal altruism - The “ prisoner’s dilemma ” 12 Swap? “Defection” is favoured. Mutual cooperation only pays in repeated exchanges. 12 DefectCooperate 12 12 12 12 Defect Cooperate

19. “ 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”

20. Insect colonies as model systems Simple ant colony in an acorn Primitive wasp colony 2 cm From centimeters…...

21. Large insect colonies Length: ~100 x Area: ~10 000 x Mass: ~1 000 000 x 2 cm 2 m …. to meters Advanced tropical ant colony Previous slide

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

23. Simple and complex family structures x x complex half-sib family offspring Parentsx simple full-sib family daughter queen mates and takes over x x

24. Queens are specialized egg-laying females Single queen per colonyMultiple queens per colony

25. Reproduction in haplodiploid social insects (ants, bees, wasps) Mother queen father Queen ovaries workers Not mated No stored sperm worker ovaries worker sons no Fertiliz ation queen sons no Fertiliz ation queen daughters Fert ilization

26. Relatedness consequences of haplodiploidy Mother queen father workers queen son queen daughter worker son 0.75 0.50 (own son) 0.375 (other worker’s son) 0.25 0.50 0.25 0.50 0.25 0.00 Reproductive Conflict over Sex ratio and Male production

27. The conflict over Male Production Mother queen father workers queen son queen daughter worker son 0.75 0.50 (own son) 0.375 (other worker’s son) 0.25 0.50 0.25 0.50 0.25 0.00 When there are more half sisters than full sisters workers are selected to remove each other’s eggs

28. Worker-Queen Conflict in Ants, Bees, Wasps Worker control over sex allocation is common Worker production of males is not

29. 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

30. 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

31. 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

32. 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

33. 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

34. Mutualistic Symbiosis and Co-evolution mitochondria gut bacteria nitrogen binding bacteria chloroplasts corals mycorrhizae lichens termites and fungiants and fungi Ectosymbionts of Insect Societies

35. 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)

36. 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

37. Agricultural Insect Societies Attine Ants in Panama Macrotermitinae in West Africa

38. Attine ants Fungus growing termites

39. Fieldwork in Panama Panama Canal Smithsonian Tropical Research Institute

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

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

42. Ant agriculture became “herbivorous”, ……

43. Split into two genera, …… One of which became really dominant, ……

44. Damaging, ……

45. 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

46. And highly sophisticated Atta From Hölldobler and Wilson, 1990 castes Acromyrmex anal droplets gongylidia The Leafcutter Ants

47. How an Atta colony starts Winged queen and maleOne year old nest fungus fragment

48. And What it Finally Becomes

49. 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

50. Genetic Marker Studies Microsatellite tandem repeat sequence # repeats variable among individuals

51. 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

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

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

54. Division of labour Acromyrmex echinatior Data: Bill Hughes

55. How to cope with parasites and diseases?

56. Incompatibility Issues Acromyrmex Mean genetic distance Incompatibility

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

58. The world’s largest and smallest ant “Go to the ant, thou sluggard: consider her ways, and be wise” Proverbs 6:6

59. 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?

60. The conflict over Male Production Mother queen father workers queen son queen daughter worker son 0.75 0.50 (own son) 0.375 (other worker’s son) 0.25 0.50 0.25 0.50 0.25 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)

61. SPLIT SEX RATIO THEORY Boomsma & Grafen 1990, 1991 SINGLE MATING HIGH RA “SPECIALIZE IN FEMALES” MULTIPLE MATING LOW RA “SPECIALIZE IN MALES” r f = 0.75 r m = 0.25 RA=3 r f = 0.50 r m = 0.25 RA=ca. 2

62. Formica truncorum Sex allocation Queen singly matedQueen multiply mated 1989 Investment in females Number of colonies

63. Who wins reproductive conflicts ? Males posthumously manipulate worker reproductive strategies by clumping sperm After Hölldobler and Wilson, 1990 Sperm storage organ Reproductive organs Formica queen Formica nest mound Males?