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My research

My research. Current research : Caste conflict in social insects (stingless bees & termites). sperm 100% females. autosome 50% females. plasmagenes 100% females. INTRAGENOMIC CONFLICT. Sex allocation. queen 50% females. PARENT-OFFSPRING CONFLICT. workers 75% females. Wolbachia.

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My research

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  1. My research Current research : Caste conflict in social insects (stingless bees & termites)

  2. sperm100% females autosome 50% females plasmagenes100% females INTRAGENOMIC CONFLICT Sex allocation queen50% females PARENT-OFFSPRING CONFLICT workers75% females

  3. Wolbachia • Maternally transmitted symbiont that manipulates host to produce female biased broods • “Cytoplasmic sex ratio distorter” • Alpha-proteobacterium • Occurs mainly in arthropods (insects+Crustacea) + nematodes

  4. Male Killing Feminisation Parthenogenesis Induction FemaleBiasedSex-Ratios Effects on host reproduction

  5. 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 - + - -

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

  7. Aims • 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?

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

  9. Methodology: PCR Assay

  10. High Incidence Worldwide Indonesia Europe # species=50 Wenseleers et al. (1998) Proceedings of the Royal Society of London # 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

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

  12. Aims • 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?

  13. Aims • 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?

  14. None infected. Wolbachia does not induce parthenogenesis in ants. Grasso et al. (2000) Ethology, Ecology & Evolution 12:309-314 Wenseleers & Billen (2000) Journal of Evolutionary Biology 13:277-280 Parthenogenesis induction? • 6 Parthenogenetic Ants Cape honeybeeCataglyphis cursor Apis mellifera capensisCataglyphis piliscapa • Pristomyrmex pungens • Cerapachys biroi • Messor capitatus • Platythyrea punctata • 250 samples, avg. 6 cols./species

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

  16. 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?

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

  18. 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 B, in press

  19. 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 B, in press

  20. 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 B, in press

  21. 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 B, 269: 623-629

  22. Clearance in lab experiments p < 0.0001 After 2 month exposure to 20°C Worker pupae 7 colonies N=89 N=90

  23. 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

  24. 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

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

  26. Aims • 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?

  27. 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

  28. 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

  29. 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

  30. 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

  31. 70 74 76 100 100 70 100 100 88 87 96 99 85 69 85 79 96 93 96 100 65 71 56 Wolbachia in Leafcutter Ants • Two free-living species (A. octospinosus, A. echinatior) have multiple “Solenopsis-like” Wolbachia infections • Infection males < gynes + workers  possibly partial male killers • No evidence for abnormal sex ratios Neochrysocharis Eulophidae Dacus destillatoria Drosophila simulans Drosophila melanogaster Aedes albopictus Acromyrmex insinuator A1 InsA Muscidifurax uniraptor Nasonia vitripennis A Drosophila bifasciata Drosophila simulans Formica truncorum Asobara tabida Acromyrmex echinatior A1 Solenopsis richteri InvA Acromyrmex octospinosus A1 Solenopsis invicta Armadillidium vulgare Culex pipiens Encarsia Formosa Diplolepis rosae Acromyrmex insinuator B2 Naw Telenomus nawai Adalia bipunctata B Trichogramma kaykai Tribolium madens Acraea encedon Solenopsis invicta Acromyrmex octospinosus B3 Acromyrmex octospinosus B2 Acromyrmex insinuator B1 InvB Solenopsis invicta Acromyrmex echinatior Bc Van Borm, Wenseleers, Billen & Boomsma, Mol. Phyl. Evol., in press Van Borm, Wenseleers, Billen & Boomsma (2001) J. Evol. Biol. 13: 277-280. Acromyrmex octospinosus B1

  32. 70 74 76 100 100 70 100 100 88 87 96 99 85 69 85 79 96 93 96 100 65 71 56 Wolbachia in Leafcutter Ants • Several unrelated Wolbachia infections in inquiline A. insinuator • Equally common in males and females  cytoplasmic incompatibility? Neochrysocharis Eulophidae Dacus destillatoria Drosophila simulans Drosophila melanogaster Aedes albopictus Acromyrmex insinuator A1 InsA Muscidifurax uniraptor Nasonia vitripennis A Drosophila bifasciata Drosophila simulans Formica truncorum Asobara tabida Acromyrmex echinatior A1 Solenopsis richteri InvA Acromyrmex octospinosus A1 Solenopsis invicta Armadillidium vulgare Culex pipiens Encarsia Formosa Diplolepis rosae Acromyrmex insinuator B2 Naw Telenomus nawai Adalia bipunctata B Trichogramma kaykai Tribolium madens Acraea encedon Solenopsis invicta Acromyrmex octospinosus B3 Acromyrmex octospinosus B2 Acromyrmex insinuator B1 InvB Solenopsis invicta Acromyrmex echinatior Bc Van Borm, Wenseleers, Billen & Boomsma, Mol. Phyl. Evol., in press Van Borm, Wenseleers, Billen & Boomsma (2001) J. Evol. Biol. 13: 277-280. Acromyrmex octospinosus B1

  33. ...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

  34. Sequencing conclusions • No host-parasite coevolution • But distinct ant Wolbachia clades – implies degree of host specialisation • Frequent horizontal transmission • Single ants may be infected with up to 6 different strains • Different populations usually, but not always, infected by same strains

  35. Conclusions • Does Wolbachia occur in ant societies? YES, IN HIGH FREQUENCY • Alternative explanation for female biased sex-ratios?NO STRONG EVIDENCEOther effects?INCOMPATIBILITY (SPECIATION?) • Host-parasite coevolution? NO, OCCASIONAL HORIZONTAL TRANSMISSION

  36. References S. Van Borm, T. Wenseleers, J. Billen and J.J. Boomsma (2002) Cloning and sequencing of wsp encoding gene fragments reveals a diversity of co-infecting Wolbachia strains in Acromyrmex leafcutter ants. Molecular Phylogenetics and Evolution, in press. T. Wenseleers, L. Sundström and J. Billen (2002) Deleterious Wolbachia in the ant Formica truncorum. Proceedings of the Royal Society of London Series B-Biological Sciences, 269: 623-629. S. Van Borm, T. Wenseleers, J. Billen and J.J. Boomsma (2001) Wolbachia in leafcutter ants: a widespread symbiont that may induce male killing or incompatible matings. Journal of Evolutionary Biology, 14: 805-814. T. Wenseleers (2001) Conflict from Cell to Colony. Ph.D. thesis, University of Leuven, Belgium, 205 pp. Advisor: Prof. Dr. J. Billen. D. Grasso, T. Wenseleers, A. Mori, F. Le Moli and J. Billen (2000) Thelytokous worker reproduction and lack of Wolbachia infection in the harvesting ant Messor capitatus. Ethology, Ecology & Evolution, 12 : 309-314. T. Wenseleers and J. Billen (2000) No evidence for Wolbachia-induced parthenogenesis in the social Hymenoptera. Journal of Evolutionary Biology, 13 : 277-280. T. Wenseleers, F. Ito, S. Van Borm, R. Huybrechts, F. Volckaert and J. Billen (1998) Widespread occurrence of the micro-organism Wolbachia in ants. Proceedings of the Royal Society of London Series B-Biological Sciences, 265: 1447-1452. PDFs at www.shef.ac.uk/uni/projects/taplab/twpub.html

  37. Acknowledgements Prof. Dr. J. Billen Dr. F. Ito Prof. Dr. J.J. Boomsma Dr. F.L.W. Ratnieks Dr. D.A. Grasso Dr. L. Sundström Prof. Dr. R. Huybrechts S. Van Borm Prof. Dr. F. Volckaert Academy of Finland, British Council, FWO-Vlaanderen, Vlaamse Leergangen, EU “Social Evolution” & INSECTS networks, Marie Curie

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