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Evolution 2018, Dobzhansky Prize Talk

Evolution 2018, Dobzhansky Prize Talk

Amanda Kyle Gibson

August 22, 2018
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  1. “The most that the average species can achieve is to

    dodge its minute enemies…” ~JBS Haldane, 1949
  2. “The most that the average species can achieve is to

    dodge its minute enemies by constantly producing new genotypes” ~JBS Haldane, 1949
  3. “The most that the average species can achieve is to

    dodge its minute enemies by constantly producing new [or rare] genotypes” ~JBS Haldane, 1949
  4. Hypothesis: the Red Queen Assumption: adaptation to common hosts dodging

    minute enemies Alternative: dodging by dispersal Z Dinges outline
  5. Hypothesis: the Red Queen Assumption: adaptation to common hosts dodging

    minute enemies Alternative: dodging by dispersal Z Dinges outline
  6. sex shouldn’t exist Lively 2009 JEB Generation N cost of

    males Two-fold cost of males sexual asexual
  7. sex shouldn’t exist Lively 2009 JEB Generation N extinct in

    <10 generations cost of males sexual asexual
  8. “Why all this silly rigmarole of sex? Why this gavotte

    of chromosomes? Why all these useless males, this striving and wasteful bloodshed, these grotesque horns [and] colors?” ~WD Hamilton, 1975 “Gamblers since life began”
  9. “The most that the average species can achieve is to

    dodge its minute enemies by constantly producing new [or rare] genotypes” ~JBS Haldane, 1949 Red Queen hypothesis solution?
  10. Red Queen hypothesis Lively 2009 JEB Generation N sexual +

    coevolving parasites asexual solution?
  11. Lively 2009 JEB Freq. infection *periodic over-infection of common clones

    + under-infection of rare clones Generation solution?
  12. asexual sexual coexist with cost of males Gibson et al.

    2017 Evol Lett a natural host-parasite system
  13. Year Asexual females Vergara et al. 2014 Am Nat Sexual

    females Proportion infected (Weighted mean ± se) Are asexuals over-infected? field 4 sites
  14. Year Asexual females – 53% Sexual females -42% Proportion infected

    (Weighted mean ± se) Are asexuals over-infected? field Vergara et al. 2014 Am Nat
  15. Year Asexual females – 53% Sexual females -42% Proportion infected

    (Weighted mean ± se) Sexual Asexual Are asexuals over-infected? Yes! field Vergara et al. 2014 Am Nat
  16. 6 sites Year Proportion infected (Weighted mean ± se) Asexual

    females Sexual females Are asexuals over-infected? field Gibson et al. in press; Am Nat
  17. Year Proportion infected (Weighted mean ± se) Asexual females –

    10% Sexual females – 26% Are asexuals over-infected? field Gibson et al. in press; Am Nat
  18. Year Proportion infected (Weighted mean ± se) Sexual Asexual Asexual

    females – 10% Sexual females – 26% Are asexuals over-infected? NO! field Gibson et al. in press; Am Nat
  19. 2001-2005 2012-2016 Asexual females Sexual females Year Proportion infected GEE:

    year * reproductive mode Shift in relative infection field
  20. 2001-2005 2012-2016 Asexual females Sexual females Year Proportion infected GEE:

    year * reproductive mode Shift driven by variation in asexuals Shift in relative infection field
  21. Sexual Asexual 10 years of field sampling 2001-2005 + 2012-2016

    Proportion infected Shift in relative infection field Gibson et al. in press; Am Nat
  22. No overall difference in infection Sexual Asexual Proportion infected GEE:

    no effect of reproductive mode 10 years of field sampling 2001-2005 + 2012-2016 field
  23. But much greater variation for asexuals Sexual Asexual Proportion infected

    10 years of field sampling 2001-2005 + 2012-2016 1.02 [0.80,1.30] 0.66 [0.53,0.79] << Coefficient of variation field GEE: no effect of reproductive mode
  24. 2001 - 2005 2012 - 2016 past over-infection recent under-infection

    Proportion asexual Asexuals are under-infected when rare 1 field Gibson et al. in press; Am Nat
  25. 2001 - 2005 2012 - 2016 past over-infection recent under-infection

    Proportion asexual Asexuals are under-infected when rare 35% 23% GLM: sampling period 1 field
  26. 2001 - 2005 2012 - 2016 past over-infection recent under-infection

    Proportion asexual Asexuals are under-infected when rare 35% 23% No asexuals at 3 of 6 sites 1 field GLM: sampling period
  27. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field predictions
  28. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field Asexuals spread when under-infected 2 predictions
  29. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field Asexuals spread when under-infected 2 Do asexuals have a fitness advantage? predictions
  30. 2

  31. Control Exposed 1 year later t parental generation t+1 offspring

    generation 2 Do asexuals have a fitness advantage? experiment
  32. Control Exposed 1 year later 2 q freq. asexuals Do

    asexuals have a fitness advantage? experiment t parental generation t+1 offspring generation
  33. Control Exposed 1 year later Sam Klosak Peyton Joachim Julie

    Xu 12 mesocosms x 4 years = 48 replicates 2 Do asexuals have a fitness advantage? experiment q freq. asexuals t parental generation t+1 offspring generation
  34. Control Exposed Control Exposed Generation t Generation t+1 28% 2

    Do asexuals have a fitness advantage? experiment Gibson et al. in press; Am Nat q Proportion asexual
  35. Control Exposed Control Exposed Generation t Generation t+1 28% 2

    Do asexuals have a fitness advantage? experiment Gibson et al. in press; Am Nat q Proportion asexual
  36. Control Exposed Control Exposed Generation t Generation t+1 28% 46%

    2 Do asexuals have a fitness advantage? experiment Gibson et al. in press; Am Nat q Proportion asexual
  37. Control Exposed Control Exposed Generation t Generation t+1 28% 46%

    52% GLM: treatment - marginal 2 Do asexuals have a fitness advantage? experiment q Proportion asexual
  38. Control Exposed Control Exposed Generation t Generation t+1 1.64x 1.86x

    GLM: treatment - marginal 2 q Proportion asexual Do asexuals have a fitness advantage? experiment
  39. Control Exposed Control Exposed Generation t Generation t+1 1.64x 1.86x

    GLM: treatment - marginal 2 Do asexuals have a fitness advantage? experiment q freq. asexuals
  40. 2 Do asexuals have a fitness advantage? q freq. asexuals

    +1 = ഥ = fitness cost of sex theory
  41. + = 1 + − 1 2 Do asexuals have

    a fitness advantage? q freq. asexuals theory
  42. + = 1 + − 1 2 Do asexuals have

    a fitness advantage? q freq. asexuals = + net cost of sex theory
  43. + = ( + ) 1 + ( + )

    − 1 2 Do asexuals have a fitness advantage? q freq. asexuals baseline cost of sex cost of parasites theory = + net cost of sex
  44. Control + = ( + ) 1 + ( +

    ) − 1 2 Do asexuals have a fitness advantage? q freq. asexuals 2.18 [1.85,2.57] cost of parasites theory = + net cost of sex
  45. Exposed + = ( + ) 1 + ( +

    ) − 1 2 Do asexuals have a fitness advantage? q freq. asexuals 2.18 [1.85,2.57] 0.97 [0.19,1.97] theory = + net cost of sex
  46. Exposed + = ( + ) 1 + ( +

    ) − 1 2 Do asexuals have a fitness advantage? q freq. asexuals 2.18 [1.85,2.57] 0.97 [0.19,1.97] theory = . net cost of sex
  47. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field Asexuals spread when under-infected 2 Asexuals have a fitness advantage predictions
  48. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field Asexuals spread when under-infected 2 Asexuals have a fitness advantage Do asexuals increase in the field? predictions
  49. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field Asexuals spread when under-infected 2 Asexuals have a fitness advantage Do asexuals increase in the field? the ultimate test predictions
  50. Year Proportion asexual (Mean ± se) 2 Do asexuals increase

    in the field? field 6 sites Gibson et al. in press; Am Nat
  51. Year Proportion asexual (Mean ± se) 2 Do asexuals increase

    in the field? field GLM: reproductive mode
  52. Year Proportion asexual GLM: reproductive mode 11.5% 29.8% 2.6x (Mean

    ± se) 2 Do asexuals increase in the field? field
  53. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field Asexuals spread when under-infected 2 Asexuals have a fitness advantage Do asexuals increase in the field? the ultimate test predictions
  54. Reduced infectivity to asexuals Red Queen predicts: Asexuals are under-infected

    when rare 1 Asexuals are rare in the field Asexuals spread when under-infected 2 Asexuals have a fitness advantage Do asexuals increase in the field? predictions
  55. Vergara et al. 2014 Am Nat Freq. infection *parasites favor

    sex when asexual hosts are common Generation asexual sexual summary
  56. Gibson et al. Am Nat in press Freq. infection parasites

    favor sex when asexual hosts are common Generation * rare asexuals evade parasite selection and spread summary
  57. Gibson et al. Am Nat in press Freq. infection Generation

    asexual sexual parasite-mediated oscillations in asexual frequency maintenance of sexual females summary
  58. “Why all this silly rigmarole of sex? Why this gavotte

    of chromosomes? Why all these useless males, this striving and wasteful bloodshed, these grotesque horns [and] colors?” ~WD Hamilton, 1975 “Gamblers since life began”
  59. "...it seems to me that we need environmental fluctuations around

    a trend line of change.“ "For the source of these we may look to fluctuations and periodicities...generated by life itself." ~WD Hamilton, 1975 “Gamblers since life began”
  60. Year (Mean ± se) Proportion asexual 5 sites Zoe Dinges

    Fluctuations and periodicities field
  61. Year (Mean ± se) Proportion asexual Zoe Dinges 46% 11.5%

    Fluctuations and periodicities field
  62. Year (Mean ± se) Proportion asexual Zoe Dinges 46% 11.5%

    Will parasites adapt to common clones? Fluctuations and periodicities field
  63. Hypothesis: the Red Queen Assumption: adaptation to common hosts dodging

    minute enemies Alternative: dodging by dispersal Z Dinges outline
  64. Hypothesis: the Red Queen Assumption: adaptation to common hosts dodging

    minute enemies Alternative: dodging by dispersal Z Dinges outline
  65. Do parasites adapt to common host genotypes? John Lubbock, ca.

    1850 Z Dinges Chondrilla juncea Ill. Flora B.C. Chaboudez and Burdon, 1995 Oecologia Lively and Dybdahl, 2000 Nature; Koskella and Lively, 2009 Evolution Wolinska and Spaak, 2009 Evolution
  66. experimental evolution 6 replicates per treatment design control 90% 75%

    100% 75% 90% 100% 20 passages under selection to kill
  67. experimental evolution 30 dead hosts 40 parasite colonies Passage t+1

    archived hosts archived hosts 24 hr design Passage t
  68. experimental evolution 30 dead hosts 40 parasite colonies archived hosts

    archived hosts Passage 20 24 hr design Passage t+1 Passage t
  69. Adaptation to common hosts 90% 75% 75% 90% 1 2

    Parasites kill sympatric hosts Parasites kill common hosts predictions
  70. measuring adaptation 48 hr 48 hr 1 − mortality rate

    mortality rate design archived hosts parasite lineage
  71. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts predictions 100% 100% control
  72. Parasites kill sympatric hosts 1 host A host B Mortality

    Rate Control 0% 100% Control 0% 100% results Parasite
  73. Parasites kill sympatric hosts 1 host A host B Mortality

    Rate Control 0% 100% Control 0% 100% Ancestor ± SEM results Parasite
  74. Parasites kill sympatric hosts 1 host A host B Mortality

    Rate Control 0% 100% Control 0% 100% results Parasite
  75. Parasites kill sympatric hosts 1 host A host B Mortality

    Rate Control 0% 100% Control 0% 100% GLMM: parasite p < 0.001 * results Parasite
  76. Parasites kill sympatric hosts 1 host A host B Mortality

    Rate Control 0% 100% Control 0% 100% GLMM: parasite p < 0.001 * 1.8x results Parasite
  77. Parasites kill sympatric hosts 1 host A host B Mortality

    Rate Control 0% 100% Control 0% 100% GLMM: parasite p < 0.001 GLMM: parasite p = 0.279 * results Parasite
  78. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts predictions 100% 100% control
  79. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x predictions 100% 100% control
  80. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x 90% 75% 75% 90% predictions
  81. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x 90% 75% 25% 10% >>> predictions
  82. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x 10% 25% 75% 90% ≅ predictions
  83. Parasites kill common hosts host A host B Mortality Rate

    Rare Common 2 Rare Common results Parasite
  84. Parasites kill common hosts host A host B Mortality Rate

    Rare Common 2 Rare Common GLMM: rare/common p < 0.001 * 1.4x results Parasite
  85. Parasites kill common hosts host A host B Mortality Rate

    Rare Common GLMM: rare/common p < 0.001 * 2 Rare Common GLMM: rare/common p = 0.215 results Parasite
  86. Parasites kill common hosts host A host B Mortality Rate

    Rare Common GLMM: rare/common p < 0.001 * 2 Rare Common GLMM: rare/common p = 0.215 a neutral host? results Parasite
  87. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x predictions
  88. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x x predictions
  89. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x x “defended” “neutral” predictions
  90. Defended vs. neutral hosts host A Control 100% Mortality Rate

    host C Control 100% JU1395 results Helena Baffoe-Bonnie Parasite
  91. host A Control 100% Mortality Rate host C Control 100%

    GLMM: parasite p = 0.037 Defended vs. neutral hosts results Helena Baffoe-Bonnie Parasite
  92. host A Control 100% Mortality Rate host C Control 100%

    GLMM: parasite p = 0.037 GLMM: parasite p < 0.001 Defended vs. neutral hosts results Helena Baffoe-Bonnie Parasite
  93. host A Control 100% Mortality Rate host C Control 100%

    GLMM: parasite p = 0.037 GLMM: parasite p < 0.001 specialization Defended vs. neutral hosts results Helena Baffoe-Bonnie Parasite
  94. Defended vs. neutral hosts Helena Baffoe-Bonnie host B Control 100%

    Mortality Rate host C Control 100% * Prediction no specialization predictions Parasite
  95. Adaptation to common hosts 1 Parasites kill sympatric hosts 2

    Parasites kill common hosts x x “defended” “neutral” predictions
  96. Hypothesis: the Red Queen Assumption: adaptation to common hosts dodging

    minute enemies Alternative: dodging by dispersal Z Dinges outline
  97. Hypothesis: the Red Queen Assumption: adaptation to common hosts dodging

    minute enemies Alternative: dodging by dispersal Z Dinges outline
  98. “The most that the average species can achieve is to

    dodge its minute enemies by constantly producing new [or rare] genotypes” ~JBS Haldane, 1949
  99. “Sex, with attendant genetic change, may allow escape in time.”

    ~J Jaenike, 1978 “Escape in space is the strategy of fugitive species.”
  100. “Sex, with attendant genetic change, may allow escape in time.”

    ~J Jaenike, 1978 “Escape in space is the strategy of fugitive species.” Fontaneto et al. 2008 Wilson and Sherman, 2010 Science; 2013 Proc B
  101. the case of the missing males Caenorhabditis elegans self outcross

    x lab Morran et al. 2011 Science background coevolution favors outcrossing Parasites
  102. the case of the missing males Caenorhabditis elegans self outcross

    x lab field males are vanishingly rare coevolution favors outcrossing Barrière and Félix 2005 Curr Biol background Parasites
  103. lab field Coevolving parasites can maintain outcrossing (lab) background males

    are vanishingly rare coevolution favors outcrossing Parasites
  104. lab field Coevolving parasites can maintain outcrossing (lab) but they

    don’t (field) background males are vanishingly rare coevolution favors outcrossing Parasites
  105. Disconnect between lab and field Why? virulent parasites are absent

    in the field 1 2 life history limits parasitism hypotheses
  106. Disconnect between lab and field Why? virulent parasites are absent

    in the field 1 2 life history limits parasitism hypotheses
  107. 1 Nematocida parisii Troemel et al. 2008 PLoS Biology Felix

    and Duveau 2012 BMC Biology Gibson and Morran 2017 Journal of Nematology; review There are parasites system
  108. 1 Nematocida parisii “nematode killer from Paris” Troemel et al.

    2008 PLoS Biology Felix and Duveau 2012 BMC Biology Gibson and Morran 2017 Journal of Nematology; review There are parasites system
  109. 1 Exposed Healthy Relative population size lab field N2 HW

    wild lines Are they virulent? results (Mean ± se) Hosts
  110. 1 Exposed Healthy Relative population size lab field N2 HW

    wild lines (Mean ± se) Are they virulent? results Hosts
  111. 1 Exposed Healthy Relative population size lab field N2 HW

    wild lines GLMM: treatment p < 0.001 (Mean ± se) Are they virulent? results Hosts
  112. 1 Exposed Healthy Relative population size lab field N2 HW

    wild lines GLMM: treatment p < 0.001 (Mean ± se) Are they virulent? Yes results Hosts
  113. Disconnect between lab and field Why? virulent parasites are absent

    in the field 1 2 x life history limits parasitism hypotheses
  114. Disconnect between lab and field Why? virulent parasites are absent

    in the field 1 2 x life history limits parasitism hypotheses
  115. 2 dodging by dispersal Felix and Duveau 2012 BMC Biol

    Schulenburg and Felix 2017 Genetics system
  116. 2 dodging by dispersal Felix and Duveau 2012 BMC Biol

    Schulenburg and Felix 2017 Genetics system
  117. 2 dodging by dispersal dauer Felix and Duveau 2012 BMC

    Biol Schulenburg and Felix 2017 Genetics system
  118. 2 dodging by dispersal dauer Felix and Duveau 2012 BMC

    Biol Schulenburg and Felix 2017 Genetics natchapohn system
  119. 2 dodging by dispersal dauer Felix and Duveau 2012 BMC

    Biol Schulenburg and Felix 2017 Genetics system
  120. 2 dodging by dispersal Felix and Duveau 2012 BMC Biol

    Schulenburg and Felix 2017 Genetics system
  121. Disconnect between lab and field Why? virulent parasites are absent

    in the field 1 2 x life history limits parasitism hypotheses
  122. Disconnect between lab and field Why? virulent parasites are absent

    in the field 1 2 x Do hosts migrate successfully from infected sites? life history limits parasitism hypotheses
  123. 2 Do hosts migrate successfully from infected sites? infected migrants

    Troemel et al. 2008 PLoS Biology Felix and Duveau 2012 BMC Biology predictions
  124. 2 infected migrants Troemel et al. 2008 PLoS Biology Felix

    and Duveau 2012 BMC Biology ? ? ? predictions Do hosts migrate successfully from infected sites?
  125. 2 transmission Troemel et al. 2008 PLoS Biology Felix and

    Duveau 2012 BMC Biology ? ? ? predictions Yes Do hosts migrate successfully from infected sites? coevolution
  126. 2 Troemel et al. 2008 PLoS Biology Felix and Duveau

    2012 BMC Biology ? ? ? predictions No Do hosts migrate successfully from infected sites? transmission coevolution
  127. 2 healthy exposed (Prop ± se) Healthy low mid high

    Fraction establishing results Exposed (dose) Do hosts migrate successfully from infected sites?
  128. 2 healthy exposed results (Prop ± se) Healthy low mid

    high Fraction establishing Exposed (dose) N=19-20 Do hosts migrate successfully from infected sites?
  129. 2 healthy exposed results (Prop ± se) Healthy low mid

    high Fraction establishing Exposed (dose) N=19-20 Do hosts migrate successfully from infected sites?
  130. 2 healthy exposed results (Prop ± se) Healthy low mid

    high Fraction establishing Exposed (dose) Do hosts migrate successfully from infected sites? No
  131. 2 results (Prop ± se) Healthy low mid high Fraction

    establishing Exposed (dose) Do hosts migrate successfully from infected sites? transmission coevolution No
  132. Disconnect between lab and field Why? virulent parasites are absent

    in the field 1 2 x life history limits parasitism Parasitized hosts don’t migrate successfully hypotheses
  133. “The most that the average species can achieve is to

    dodge its minute enemies by constantly producing new genotypes” ~JBS Haldane, 1949
  134. Hypothesis: the Red Queen Assumption: adaptation to common hosts dodging

    minute enemies Alternative: dodging by dispersal Z Dinges outline
  135. Lynda Delph Daniela Vergara Amrita Bhattacharya Zoe Dinges Spencer Hall

    Christiane Hassel Peyton Joachim Sam Klosak Eliza Oldach Ngaire Perrin Julie Xu McKenna Penley Helena Baffoe-Bonnie Arooj Khalid Julie Lin Raythe Owens Dilys Osei Kayla Stoy Emily Troemel Marie-Anne Felix Gaotian Zhang Acknowledgements Curt Lively Levi Morran
  136. Red Queen predicts: Asexuals are under-infected when rare 1 Asexuals

    are rare in the field Are parasites less able to infect asexuals? Freq. infection
  137. 1

  138. + parasite eggs juvenile snails 6 control; 6 exposed 2012-2015

    1 Are parasites less able to infect asexuals?
  139. + parasite eggs juvenile snails 1 Are parasites less able

    to infect asexuals? 6 control; 6 exposed 2012-2015 Sexual Asexual
  140. Proportion infected Sexual Asexual Sexual Asexual Control Exposed 31% 11%

    GEE: reproductive mode 1 Are parasites less able to infect asexuals?
  141. Red Queen predicts: Asexuals are under-infected when rare 1 Asexuals

    are rare in the field Are parasites less able to infect asexuals? Freq. infection
  142. “The most that the average species can achieve is to

    dodge its minute enemies by constantly producing new [or rare] genotypes” ~JBS Haldane, 1949
  143. Intro on sex – can we tie it into parasites?

    Make it clear where you’re going – parasites Don’t go straight into sex – preview Change arrows with dispersal section Add successfully migrate Don’t use generations in experimental evolution – use passage Add in few more words – make sure you’re clarifying host v. parasite in conclusions/predictions Failed to falsify the red queen – return to this wording Mention how related hosts are when you introduce c Add in poster number Dirty secret Mention what the systems are on intro slide – why snail? Why nematode?