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Conflict from Cell to Colony

Conflict from Cell to Colony. Tom Wenseleers University of Leuven, Belgium Ph.D. defence May 22nd, 2001. Genes to Genomes Prokaryotes to Eukaryotes Unicellular to Multicellular Organisms Organisms to Societies.

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Conflict from Cell to Colony

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  1. Conflict from Cell to Colony Tom Wenseleers University of Leuven, Belgium Ph.D. defence May 22nd, 2001

  2. Genes to Genomes Prokaryotes to Eukaryotes Unicellular to Multicellular Organisms Organisms to Societies Cooperation is Key Feature in Evolution of Life on Earth Major transitions in evolution

  3. Cooperation seems obvious to explain when viewed in terms of species-level benefits But erroneous logic: non-cooperative ’free-riders’ outcompete altruists Potential for Conflict in Most Societies But potential for conflict • Conflicts may occur between organisms, but also between cells or genes (’intragenomic conflict’)

  4. ½ ½ ¼ ¾ Equal Sex-Ratio Equal Sex-Ratio F M F M 3:1 FemaleBiasedSex-Ratio Conflicts in insect societies In what ratio should males and females be reared?

  5. Cytoplasmic sex-ratio distorters • Conflict also occurs at the genomic level: maternally transmitted genes favour more female biased sex-ratios than nuclear genes(“intragenomic conflict”) • Cytoplasmic genes such as mitochondria or some bacterial symbionts may manipulate host to produce female biased broods (“cytoplasmic sex-ratio distorters”)

  6. Wolbachia • Example of a maternally transmitted symbiont • Alpha-proteobacterium • Occurs mainly in arthropods (insects+Crustacea) + nematodes • Manipulates host reproduction to favour own spread

  7. Male Killing Feminisation Parthenogenesis Induction Cytoplasmic Incompatibility FemaleBiasedSex-Ratios Effects on host reproduction

  8. Reduces fitness of Uninfected Female x Infected Male Crosses Gives an advantage to infected females Sterility in diploids, but production of males only in haplo-diploids Cytoplasmic incompatibility Inviable NormalOffspringProduction

  9. MitochondriaCMS CaedibacterMtK Ehrlichieae Rickettsia MK Neorickettsia Orientia MK Phylogeny Other alpha proteobacteria Gamma proteobacteria Wolbachia 0.1

  10. Aims of my thesis • Part I : empirical • Does Wolbachia occur in ant societies? • Alternative explanation for female biased sex-ratios in this group? • Part II : theoretical • What do animal and genomic conflicts have in common? • Can sociobiological theory be applied to both?

  11. Integrated approach S e q u e n c e o f E v e n t s Modelling Make predictions DNA Analysis Measure key parameters Experiments Formally test hypotheses Ideas Hypotheses Molecular Data Experimental Data

  12. Part I. Wolbachia - a cause of intragenomic conflict in ant colonies

  13. Work plan • Does Wolbachia occur in ant societies and if so in what frequency? • What effects does it have?Three case studies : • Parthenogenetic species • Wood ant Formica truncorum • Leptothorax nylanderi • Host-parasite coevolution?

  14. Polymerase Chain Reaction using Specific Primers Targets: ftsZ and wsp Wolbachia genes Positive, negative and nuclear DNA (18S rDNA) controls Negative samples retested twice Sensitive& Reliable Methodology: PCR Assay

  15. High Incidence Worldwide Indonesia Europe # species=50 Chapter 1 Wenseleers et al. (1998) Proceedings of the Royal Society of London Chapter 6 # species=50 Florida Panama # species=10 Jeyaprakash & Hoy (2000) Insect Molecular Biology # species=7 Van Borm et al. (2001) Journal of Evolutionary Biology 3451 samples

  16. Morphological evidence • Present in trophocytes and oocytes • Electron and light microscopical (DAPI) evidence

  17. Work plan • Does Wolbachia occur in ant societies and if so in what frequency? YES, IN HIGH FREQUENCY • What effects does it have?Three case studies : • Parthenogenetic species • Wood ant Formica truncorum • Leptothorax nylanderi • Host-parasite coevolution?

  18. Work plan • Does Wolbachia occur in ant societies and if so in what frequency? YES, IN HIGH FREQUENCY • What effects does it have?Three case studies : • Parthenogenetic species • Wood ant Formica truncorum • Leptothorax nylanderi • Host-parasite coevolution?

  19. PCR Assay • 6 Parthenogenetic Antsand Cape Honey Bee • Were not infected.Parthenogenesis not induced by Wolbachia. N=25036 cols. Parthenogenesis induction? Grasso et al. (2000) Ethology, Ecology & Evolution 12:309-314 Wenseleers & Billen (2000) Journal of Evolutionary Biology 13:277-280

  20. Wolbachia in F. truncorum With: Lotta Sundström University of Helsinki

  21. Formica truncorum • Extensive variation in sex-ratio produced by different colonies • Linked to facultative sex-ratio biasing : • Workers kill brothers in colonies headed by singly mated queen • But not in colonies with double mated queen • Does Wolbachia affect the sex-ratio too?

  22. Effect on the sex-ratio : Males should be infected less than queens Sex-ratio should be correlated with infection rates Predictions • Incompatibility : • Males and queens should be infected equally • Uninfected colonies should not be able to survive

  23. Formica truncorum • Males (96%) and queens (94%) infected equally • All colonies infected (total # 33) despite production of 6% uninfected queens by each colony • Consistent with an incompatibility effect:Uninfected queens do not survive past the founding stage due to incompatible matings Wenseleers, Sundström & Billen(2002) Proceedings of the Royal Society of London series B, in press.

  24. GLM Effects F p No. of mates 4.88 0.04 Infection rate 0.85 0.37 Colony size 0.69 0.42 Infection and sex-ratio Wenseleers, Sundström & Billen(2002) Proceedings of the Royal Society of London series B, in press.

  25. GLM Effects F p F p No. of mates 2.11 0.16 2.5 0.13 Infection rate 2.89 0.11 10.2 0.005 Infection and colony fitness Wenseleers, Sundström & Billen(2002) Proceedings of the Royal Society of London series B, in press.

  26. Adaptiveclearance to reduce colony load? Infection rates p<0.015 p<0.0001 N=296 N=158 N=387 Wenseleers, Sundström & Billen(2002) Proceedings of the Royal Society of London series B, in press.

  27. Conclusions • No effects on the sex-ratio • Probably causes incompatible matings • Deleterious effects on colony function, but partly mitigated by clearance of infection in adult workers

  28. Leptothorax nylanderi • Test experimentally whether Wolbachia causes incompatible matings • Setup: antibiotic treatment as an artificial means of creating the uninfected queen x infected male crossing type • Prediction: male production (infertility) following antibiotic treatment

  29. Antibiotics experiments 4 coloniesN=70 7 coloniesN=152 2 = 10.51, p < 0.001

  30. Work plan • Does Wolbachia occur in ant societies and if so in what frequency? YES, IN HIGH FREQUENCY • What effects does it have?Three case studies : • Parthenogenetic species • Wood ant Formica truncorum • Leptothorax nylanderi • Host-parasite coevolution?

  31. Wolbachia surface protein wsp was sequenced (approx. 550 bp) Direct cycle sequencing when ants were infected by single strain Cloning and sequencing when ants were infected by multiple strains (TA-cloning kit, pUC57 vector) Methodology: Sequencing 28 sequencesAligned with previously sequenced relatives

  32. 0.050(25 MY) High strain diversity Solenopsis invicta (imported) Coleomegilla maculata lengi Doronomyrmex pacis A1 Myrmica sulcinodis (Pyrenees) Laodelphax striatellus Plutella xylostella Diaphorina citri Porcellionides pruinosus Acraea encedon 1 Trichopria Tsp2 Myrmica rubra Acromyrmex insinuator A Formica lemani Plagiolepis pygmaea Sphaeroma rugicauda Dryinid wasp sp Trichogramma kaykai (LC110) Bactocera cucurbitae Muscidifurax uniraptor Trichogramma bourarachae Tribolium madens Tribolium confusum Rhinophoridae unid Leptopilina heterotoma 2 Doronomyrmex kutteri B Glossina morsitans centralis Doronomyrmex pacis B2 Trichogramma spp. Coleomegilla maculata Adalia bipunctata B Drosophila bifasciata Nasonia vitripennis A Aedes albopictus (Houston) Drosophila simulans (Coffs Harbour) Adalia bipunctata A A B Drosophila melanogaster (Cairns) Acromyrmex octospinosus B3 Drosophila melanogaster (CantonS) Acromyrmex insinuator B1 Acromyrmex echinatior B Drosophila simulans (Riverside) Solenopsis invicta (native) Acromyrmex echinatior A1 Acromyrmex octospinosus B1 Solenopsis richteri A Acromyrmex octospinosus B2 Doronomyrmex pacis A2 Acromyrmex insinuator B2 Myrmica sabuleti Solenopsis invicta A (native) Telenomus nawai Acromyrmex octospinosus A1 Encarsia formosa Diplolepis rosae Doronomyrmex goesswaldi A1 Leptopilina australis Cadra cautella Phlebotomus papatasi (Israel) Gnamptogenys menadensis Tetranychus urticae Doronomyrmex pacis A3 Cadra cautella 2 Acraea encedon Glossina austeni Asobara tabida Culex quinquefasciatus Asobara tabida 3 Drosophila sechellia Drosophila simulans (Hawaii) Cataglyphis iberica Trichopria drosophilae Culex pipiens (ESPRO) Formica rufa Isopods Teleutomyrmex schneideri Bactocera sp 1 AscD Aedes albopictus (Houston) Myrmica sulcinodis (Russia) Formica pratensis Formica fusca (KH B) Myrmica sulcinodis (Samso D) Dacus destillatoria Drosophila simulans (Watsonville) Leptothorax acervorum Formica fusca (SJW B) Formica truncorum Formica fusca (Mols D) Doronomyrmex kutteri A Doronomyrmex pacis A4 Formica polyctena Neochrysocharis formosa Doronomyrmex pacis B1 Doronomyrmex goesswaldi A2

  33. Doronomyrmex pacis A1 Hosts diverged 35 MY ago, but share a recently evolved W. strain(1.7 MY old) Doronomyrmex pacis A1 Myrmica sulcinodis (Pyrenees) Myrmica rubra Acromyrmex insinuator A Formica lemani Plagiolepis pygmaea Doronomyrmex kutteri B Doronomyrmex pacis B2 0.050(25 MY) Doronomyrmex pacis A2 Doronomyrmex goesswaldi A1 Doronomyrmex pacis A3 Doronomyrmex kutteri A Doronomyrmex pacis A4 Doronomyrmex pacis B1 Doronomyrmex goesswaldi A2 No match with host phylogeny Solenopsis invicta (imported) Coleomegilla maculata lengi Doronomyrmex pacis A1 Myrmica sulcinodis (Pyrenees) Laodelphax striatellus Plutella xylostella Diaphorina citri Porcellionides pruinosus Acraea encedon 1 Trichopria Tsp2 Myrmica rubra Acromyrmex insinuator A Formica lemani Plagiolepis pygmaea Sphaeroma rugicauda Dryinid wasp sp Trichogramma kaykai (LC110) Bactocera cucurbitae Muscidifurax uniraptor Trichogramma bourarachae Tribolium madens Tribolium confusum Rhinophoridae unid Leptopilina heterotoma 2 Doronomyrmex kutteri B Glossina morsitans centralis Doronomyrmex pacis B2 Trichogramma spp. Coleomegilla maculata Adalia bipunctata B Drosophila bifasciata Nasonia vitripennis A Aedes albopictus (Houston) Drosophila simulans (Coffs Harbour) Adalia bipunctata A A B Drosophila melanogaster (Cairns) Acromyrmex octospinosus B3 Drosophila melanogaster (CantonS) Acromyrmex insinuator B1 Acromyrmex echinatior B Drosophila simulans (Riverside) Solenopsis invicta (native) Acromyrmex echinatior A1 Acromyrmex octospinosus B1 Solenopsis richteri A Acromyrmex octospinosus B2 Doronomyrmex pacis A2 Acromyrmex insinuator B2 Myrmica sabuleti Solenopsis invicta A (native) Telenomus nawai Acromyrmex octospinosus A1 Encarsia formosa Diplolepis rosae Doronomyrmex goesswaldi A1 Leptopilina australis Cadra cautella Phlebotomus papatasi (Israel) Gnamptogenys menadensis Tetranychus urticae Doronomyrmex pacis A3 Cadra cautella 2 Acraea encedon Glossina austeni Asobara tabida Culex quinquefasciatus Asobara tabida 3 Drosophila sechellia Drosophila simulans (Hawaii) Cataglyphis iberica Trichopria drosophilae Culex pipiens (ESPRO) Formica rufa Isopods Teleutomyrmex schneideri Bactocera sp 1 AscD Aedes albopictus (Houston) Myrmica sulcinodis (Russia) Formica pratensis Formica fusca (KH B) Myrmica sulcinodis (Samso D) Dacus destillatoria Drosophila simulans (Watsonville) Leptothorax acervorum Formica fusca (SJW B) Formica truncorum Formica fusca (Mols D) Doronomyrmex kutteri A Doronomyrmex pacis A4 Formica polyctena Neochrysocharis formosa Doronomyrmex pacis B1 Doronomyrmex goesswaldi A2

  34. Doronomyrmex pacis A1 Doronomyrmex pacis B2 0.050(25 MY) Multi infections may drive speciation events! Doronomyrmex pacis A2 Doronomyrmex pacis A3 Doronomyrmex pacis A4 Doronomyrmex pacis B1 Multiple infections Solenopsis invicta (imported) Coleomegilla maculata lengi Doronomyrmex pacis A1 Myrmica sulcinodis (Pyrenees) Laodelphax striatellus Plutella xylostella Diaphorina citri Porcellionides pruinosus Acraea encedon 1 Trichopria Tsp2 Myrmica rubra Acromyrmex insinuator A Formica lemani Plagiolepis pygmaea Sphaeroma rugicauda Dryinid wasp sp Trichogramma kaykai (LC110) Bactocera cucurbitae Muscidifurax uniraptor Trichogramma bourarachae Tribolium madens Tribolium confusum Rhinophoridae unid Leptopilina heterotoma 2 Doronomyrmex kutteri B Glossina morsitans centralis Doronomyrmex pacis B2 Trichogramma spp. Coleomegilla maculata Adalia bipunctata B Drosophila bifasciata Nasonia vitripennis A Aedes albopictus (Houston) Drosophila simulans (Coffs Harbour) Adalia bipunctata A A B Drosophila melanogaster (Cairns) Acromyrmex octospinosus B3 Drosophila melanogaster (CantonS) Acromyrmex insinuator B1 Acromyrmex echinatior B Drosophila simulans (Riverside) Solenopsis invicta (native) Acromyrmex echinatior A1 Acromyrmex octospinosus B1 Solenopsis richteri A Acromyrmex octospinosus B2 Doronomyrmex pacis A2 Acromyrmex insinuator B2 Myrmica sabuleti Solenopsis invicta A (native) Telenomus nawai Acromyrmex octospinosus A1 Encarsia formosa Diplolepis rosae Doronomyrmex goesswaldi A1 Leptopilina australis Cadra cautella Phlebotomus papatasi (Israel) Gnamptogenys menadensis Tetranychus urticae Doronomyrmex pacis A3 Cadra cautella 2 Acraea encedon Glossina austeni Asobara tabida Culex quinquefasciatus Asobara tabida 3 Drosophila sechellia Drosophila simulans (Hawaii) Cataglyphis iberica Trichopria drosophilae Culex pipiens (ESPRO) Formica rufa Isopods Teleutomyrmex schneideri Bactocera sp 1 AscD Aedes albopictus (Houston) Myrmica sulcinodis (Russia) Formica pratensis Formica fusca (KH B) Myrmica sulcinodis (Samso D) Dacus destillatoria Drosophila simulans (Watsonville) Leptothorax acervorum Formica fusca (SJW B) Formica truncorum Formica fusca (Mols D) Doronomyrmex kutteri A Doronomyrmex pacis A4 Formica polyctena Neochrysocharis formosa Doronomyrmex pacis B1 Doronomyrmex goesswaldi A2

  35. ...and their symbionts Formica hosts... truncorum rufa 84 100 polyctena polyctena pratensis pratensis lemani truncorum fusca lemani 99 rufa 100 fusca O O Gyllenstrand, unpublished 0.02(10 MY) No match with host phylogeny

  36. Work plan • Does Wolbachia occur in ant societies and if so in what frequency? YES, IN HIGH FREQUENCY • What effects does it have?Three case studies : • Parthenogenetic species • Wood ant Formica truncorum • Leptothorax nylanderi • Host-parasite coevolution? NO, OCCASIONAL HORIZONTAL TRANSMISSION

  37. Part II. Theoretical aspects ofconflict and cooperation With: Francis Ratnieks and Kevin Foster University of Sheffield

  38. Animal vs. intragenomic conflict • What do animal and intragenomic conflict have in common? • Is there a “general theory of conflict” that provides insight into the evolution of conflict at both levels?

  39. Theories of conflict Two Approaches in the Study of Conflict Game Theoryvon Neumann & Morgenstern Kin SelectionHamilton • Cost Dependson Social Context • r.B > C • Single method

  40. Consequence ofboth cooperating Regression of genotype on joint behaviour Terms thattake intoaccount social context Hamilton’s rule (costs & benefits independent of social context) Generalised Hamilton’s rule Wenseleers & Ratnieks submitted

  41. GENOMIC CONFLICT (MEIOTIC DRIVE) ANIMAL CONFLICT PARTNER PARTNER COOPERATE DRIVE DOVE HAWK DOVE COOPERATE 0 -B 1/2 GDC.(1-k) ACTOR ACTOR DRIVE HAWK B -C GDC.k GDD/2 Animal vs. intragenomic conflict

  42. Animal vs. intragenomic conflict • Shows that game theoretic logic of conflict at both levels is the same • But can genes also be related? • Yes, kinship measures genetic correlation and for 2 genes at a locus this is the inbreeding coefficient FIT • When genes are related they are selected to be altruistic ! • Application of generalised Hamilton’s rule allows detailed analysis

  43. Spite: Hamilton’s unproven theory • Medea killed her children to take away the smile from her husband’s face. • Example of a paradoxical behaviour that harms another at no benefit to self (“spite”) • We showed that some forms of intragenomic conflict qualify as spiteful behaviour (Maternal effect lethals, queen killing in the fire ant) Foster, Ratnieks & Wenseleers (2000) Trends in Ecology & Evolution 15:469-470 Foster, Wenseleers & Ratnieks (2001) Annales Zoologici Fennici, in press

  44. Why become a worker? • Why do social insect females work for the benefit of others? • Usual explanation: indirect genetic benefit when altruism is directed towards relatives (’kin selection’) • But is relatedness in insect societies high enough? • E.g. honey bee: queen mates with several males so that workers mostly rear half-sisters (r=0.3)

  45. New calculations • Female should become a queen with a probability of (1-Rf)/(1+Rm) (self determination) • = 20% for stingless bees (singly mated) • = 56% for honey bees (polyandrous) • Too high for the colony as a whole, since queens are only needed for swarming (“tragedy of the commons”) • Adult workers and mother queen selected to prevent production of excess queens (“policing”)

  46. THE SAME TENSION OCCURS IN HUMAN SOCIETY ! stingless bees honey bees Self determination20% queen production Policing of caste fate 0.02% queen production Comparative predictions hold Individual Freedom Causes a Cost to Society But females prefer to become queen with probability of 56% ! Efficient Society but No Individual Freedom

  47. General conclusions • Part I : empirical • Does Wolbachia occur in ant societies? YES, IN HIGH FREQUENCY • Alternative explanation for female biased sex-ratios in this group? PROBABLY NOT • Other effects? INCOMPATIBILITY(SPECIATION?) • Part II : theoretical • What do animal and genomic conflicts have in common? SAME LOGIC • Can sociobiological theory be applied to both? YES (GENERALISED HAMILTOM’S RULE) • What do we learn from this more generally?DEEPER INSIGHT INTO THE FUNCTIONING OF HUMAN SOCIETIES (TOC)

  48. The End

  49. Acknowledgements Prof. Dr. J. Billen Prof. Dr. R. Huybrechts Prof. Dr. J.J. Boomsma Dr. F. Ito Dr. K.R. Foster Dr. F.L.W. Ratnieks Prof. S.A. Frank Dr. L. Sundström Dr. D.A. Grasso Drs. S. Van Borm Prof. Dr. F. Volckaert Academy of Finland, British Council, FWO-Vlaanderen, Vlaamse Leergangen, EU Network “Social Evolution”

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