Conflict from Cell to Colony

1
Conflict from Cell to Colony
Tom Wenseleers University of
Leuven, Belgium Ph.D. defence
May 22nd, 2001
2
Major transitions in evolution

• Genes to Genomes
• Prokaryotes to Eukaryotes
• Unicellular to Multicellular Organisms
• Organisms to Societies

3
But potential for conflict

• Cooperation seems obvious to explain when viewed
  in terms of species-level benefits
• But erroneous logic non-cooperative
  free-riders outcompete altruists

• Conflicts may occur between organisms, but also
  between cells or genes (intragenomic conflict)

4
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(intragenomi
  c 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 (insectsCrustacea)
  nematodes
• Manipulates host reproduction to favour own spread

7
Effects on host reproduction

• Male Killing
• Feminisation
• Parthenogenesis Induction
• Cytoplasmic Incompatibility

8
Cytoplasmic incompatibility
Inviable

• 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

NormalOffspringProduction
9
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
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
Methodology PCR Assay

• Polymerase Chain Reaction using Specific Primers
• Targets ftsZ and wsp Wolbachia genes
• Positive, negative and nuclear DNA (18S rDNA)
  controls
• Negative samples retested twice

15
High Incidence Worldwide
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
Parthenogenesis induction?
Grasso et al. (2000) Ethology, Ecology
Evolution 12309-314 Wenseleers Billen (2000)
Journal of Evolutionary Biology 13277-280
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
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

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
Infection and sex-ratio
Wenseleers, Sundström Billen (2002) Proceedings
of the Royal Society of London series B, in
press.
25
Infection and colony fitness
Wenseleers, Sundström Billen (2002) Proceedings
of the Royal Society of London series B, in
press.
26
Infection rates
plt0.015
plt0.0001
N296
N158
N387
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 coloniesN70
7 coloniesN152
?2 10.51, p lt 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
Methodology Sequencing
28 sequencesAligned with previously sequenced
relatives

• 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)

32
High strain diversity
Solenopsis invicta (imported)
Coleomegilla maculata lengi
Doronomyrmex pacis A1
Myrmica sulcinodis (Pyrenees)
Plutella xylostella
Laodelphax striatellus
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
Acromyrmex octospinosus B3
Drosophila melanogaster (Cairns)
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
Culex pipiens (ESPRO)
Trichopria drosophilae
Isopods
Formica rufa
Teleutomyrmex schneideri
Bactocera sp 1 AscD
Aedes albopictus (Houston)
Myrmica sulcinodis (Russia)
Formica fusca (KH B)
Formica pratensis
Drosophila simulans (Watsonville)
Myrmica sulcinodis (Samso D)
Dacus destillatoria
Leptothorax acervorum
Formica fusca (SJW B)
Formica fusca (Mols D)
Formica truncorum
Doronomyrmex kutteri A
Doronomyrmex pacis A4
Formica polyctena
Neochrysocharis formosa
Doronomyrmex pacis B1
Doronomyrmex goesswaldi A2
33
No match with host phylogeny
Solenopsis invicta (imported)
Coleomegilla maculata lengi
Doronomyrmex pacis A1
Myrmica sulcinodis (Pyrenees)
Plutella xylostella
Laodelphax striatellus
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
Acromyrmex octospinosus B3
Drosophila melanogaster (Cairns)
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
Culex pipiens (ESPRO)
Trichopria drosophilae
Isopods
Formica rufa
Teleutomyrmex schneideri
Bactocera sp 1 AscD
Aedes albopictus (Houston)
Myrmica sulcinodis (Russia)
Formica fusca (KH B)
Formica pratensis
Drosophila simulans (Watsonville)
Myrmica sulcinodis (Samso D)
Dacus destillatoria
Leptothorax acervorum
Formica fusca (SJW B)
Formica fusca (Mols D)
Formica truncorum
Doronomyrmex kutteri A
Doronomyrmex pacis A4
Formica polyctena
Neochrysocharis formosa
Doronomyrmex pacis B1
Doronomyrmex goesswaldi A2
34
Multiple infections
Solenopsis invicta (imported)
Coleomegilla maculata lengi
Doronomyrmex pacis A1
Myrmica sulcinodis (Pyrenees)
Plutella xylostella
Laodelphax striatellus
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
Acromyrmex octospinosus B3
Drosophila melanogaster (Cairns)
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
Culex pipiens (ESPRO)
Trichopria drosophilae
Isopods
Formica rufa
Teleutomyrmex schneideri
Bactocera sp 1 AscD
Aedes albopictus (Houston)
Myrmica sulcinodis (Russia)
Formica fusca (KH B)
Formica pratensis
Drosophila simulans (Watsonville)
Myrmica sulcinodis (Samso D)
Dacus destillatoria
Leptothorax acervorum
Formica fusca (SJW B)
Formica fusca (Mols D)
Formica truncorum
Doronomyrmex kutteri A
Doronomyrmex pacis A4
Formica polyctena
Neochrysocharis formosa
Doronomyrmex pacis B1
Doronomyrmex goesswaldi A2
35
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
40
Generalised Hamiltons rule
Wenseleers Ratnieks submitted
41
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 Hamiltons rule allows
  detailed analysis

43
Spite Hamiltons unproven theory

• Medea killed her children to take away the smile
  from her husbands 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 15469-470 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 (r0.3)

45
New calculations

• Female should become a queen with a probability
  of (1-Rf)/(1Rm) (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
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 HAMILTOMS 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