ESEB 2017, John Maynard Smith Prize talk

August 25, 2017 in Groningen, the Netherlands

Transcript

1. What use is sex? Amanda K Gibson
2. “What use is sex?” ~John Maynard Smith, 1971
3. 1. the problem
4. 1. the problem 2. a solution
5. 1. the problem 2. a solution
6. the two-fold cost of males problem
7. “Although absurdly simple, the point is so fundamental and so often misunderstood” ~Maynard Smith, 1978 problem the two-fold cost of males
8. Maynard Smith 1971, 1978 sexual problem the two-fold cost of males
9. asexual Maynard Smith 1971, 1978 sexual problem the two-fold cost of males
10. asexual 50% decrease in per-capita birth rate! Maynard Smith 1971, 1978 sexual problem the two-fold cost of males
11. Maynard Smith 1971, 1978 sexual asexual doubling problem the two-fold cost of males
12. problem the two-fold cost of males Generation No. individuals Lively JEB 2009 Asexual Sexual
13. problem the two-fold cost of males Generation No. individuals Lively JEB 2009 Asexual Sexual
14. problem the two-fold cost of males Generation No. individuals Lively JEB 2009 Asexual Sexual extinction <10 generations
15. obligately asexual animal species Vrijenhoek 1998 sexual problem but males are everywhere!
16. nematode phylum Gibson and Fuentes 2015 Evolution selfing/asexual (few ♂s) outcrossing (many ♂s) problem but males are everywhere!
17. “The evolution of sex is the hardest problem in evolutionary biology” ~Maynard Smith, 1999 problem
18. “There is a kind of crisis at hand in evolutionary biology” ~GC Williams, 1975 problem
19. crisis! problem
20. crisis! but is there really a two-fold cost? problem
21. crisis! but is there really a two-fold cost? We need a direct estimate of the cost of sex problem
22. © Bart Zijlstra problem
23. Potamopyrgus antipodarum © Bart Zijlstra problem
24. “Further investigation of these cases could be most interesting” ~ Maynard Smith, 1978 © Bart Zijlstra problem
25. J Xu K Bensen asexual sexual coexist with problem Potamopyrgus antipodarum
26. J Xu K Bensen asexual sexual diploid triploid coexist with problem Potamopyrgus antipodarum
27. J. Jokela
28. J. Jokela 1985, L Delph
29. J. Jokela
30. J. Jokela Curt Lively Lynda Delph problem
31. J. Jokela juveniles problem
32. field juveniles problem
33. field juveniles 1 year later problem
34. field juveniles 1 year later t parental generation t+1 offspring generation t parental generation t+1 offspring generation problem
35. Sam Klosak Peyton Joachim field juveniles 1 year later t parental generation t+1 offspring generation q freq. asexuals problem
36. 6 mesocosms x 4 years = 24 replicates Sam Klosak Peyton Joachim field juveniles 1 year later t parental generation t+1 offspring generation q freq. asexuals problem
37. field juveniles 1 year later t parental generation t+1 offspring generation q freq. asexuals generation Gibson et al. Evol Lett problem
38. field juveniles 1 year later t parental generation t+1 offspring generation q freq. asexuals generation Gibson et al. Evol Lett logistic model 1.60x [1.48, 1.73] problem
39. the two-fold cost © Bart Zijlstra asexuals will double in frequency when rare
40. the two-fold cost © Bart Zijlstra asexuals will double in frequency when rare asex sex generation N
41. the two-fold cost © Bart Zijlstra asexuals will double in frequency when rare asex sex generation N
42. the two-fold cost © Bart Zijlstra asexuals will double in frequency when rare how much should they increase otherwise?
43. the two-fold cost © Bart Zijlstra asexuals will double in frequency when rare how much should they increase otherwise? let’s expand the prediction
44. = birth rate cost of sex Gibson et al. Evol Lett problem
45. = fitness cost of sex Gibson et al. Evol Lett problem
46. = fitness cost of sex = frequency of asexuals mean fitness Gibson et al. Evol Lett
47. = fitness cost of sex = frequency of asexuals mean fitness = 1 + − 1 cost of sex
48. = fitness cost of sex = frequency of asexuals mean fitness = 1 + − 1 cost of sex = 1 + − 1 fold-increase as a function of qt and c
49. Fold increase Gibson et al. Evol Lett problem = 1 + − 1 qt freq asexuals: parents c=1, no cost c=2 prediction
50. Gibson et al. Evol Lett problem qt freq asexuals: parents c=1 c=2 = 1 + − 1 prediction Fold increase
51. Gibson et al. Evol Lett problem Original prediction qt freq asexuals: parents c=1 c=2 = 1 + − 1 prediction Fold increase
52. Gibson et al. Evol Lett problem ~1.54-fold qt freq asexuals: parents c=1 c=2 = 1 + − 1 prediction Fold increase
53. qt freq asexuals: parents Gibson et al. Evol Lett problem qt+1 freq asexuals: offspring c=1 prediction = 1 + − 1
54. qt freq asexuals: parents Gibson et al. Evol Lett problem c=1 c=2 qt+1 freq asexuals: offspring prediction = 1 + − 1
55. qt freq asexuals: parents Gibson et al. Evol Lett problem c=1 c=2 qt+1 freq asexuals: offspring prediction vs. data = 1 + − 1
56. qt freq asexuals: parents Gibson et al. Evol Lett problem c=1 c=2 mesocosm estimate = 2.14, [1.81, 2.55] qt+1 freq asexuals: offspring = 1 + − 1 prediction vs. data
57. qt freq asexuals: parents Gibson et al. Evol Lett problem c=1 c=2 mesocosm The two-fold cost is real prediction vs. data qt+1 freq asexuals: offspring
58. “There is a kind of crisis at hand in evolutionary biology” ~GC Williams, 1975 problem
59. “There is a kind of crisis at hand in evolutionary biology” Is sex really so costly? problem
60. the crisis stands the cost of sex is two-fold, or slightly greater problem © Bart Zijlstra
61. 1. the problem “Why do parthenogenetic varieties not replace sexual ones?” ~Maynard Smith, 1978 [asexual]
62. 1. the problem 2. a solution?
63. 1. the problem 2. a solution? a strong selective force must counterbalance the cost of sex
64. solution a “bloody-minded” environment
65. solution allele combinations fitness time a “bloody-minded” environment
66. allele combinations fitness time allele combinations solution a “bloody-minded” environment
67. “It is hard to believe that God is as bloody-minded as that” ~Maynard Smith, 1985 solution
68. “It is hard to believe that God is as bloody-minded as that” ~Maynard Smith, 1985 J Tenniel Coevolving parasites solution
69. No. individuals Asexual Sexual Lively JEB 2009 Generation - parasites solution rapid extinction the Red Queen hypothesis
70. No. individuals Lively JEB 2009 + parasites Generation - parasites rapid extinction Asexual Sexual solution the Red Queen hypothesis
71. No. individuals Lively JEB 2009 + parasites Generation - parasites rapid extinction Asexual Sexual solution the Red Queen hypothesis
72. No. individuals Lively JEB 2009 + parasites Generation Asexual Sexual solution the Red Queen hypothesis Freq. infection
73. No. individuals Lively JEB 2009 + parasites Generation Asexual Sexual solution the Red Queen hypothesis Freq. infection
74. Lively JEB 2009 + parasites Generation Freq. infection Asexual Sexual periodic over-infection of common clones solution the Red Queen hypothesis
75. © Bart Zijlstra support from nature
76. © Bart Zijlstra support from nature Gabe Harp
77. © Bart Zijlstra support from nature Gabe Harp Microphallus
78. © Bart Zijlstra support from nature Gabe Harp Microphallus
81. Year Asexual females Vergara et al. Am Nat 2014 Sexual females 4 sites Proportion infected (Weighted mean ± se) periodic over-infection solution
82. Year Asexual females – 53% Vergara et al. Am Nat 2014 Sexual females -42% 4 sites Proportion infected (Weighted mean ± se) periodic over-infection solution
83. Lively JEB 2009 Generation Freq. infection Asexual Sexual periodic over-infection of common clones periodic over-infection solution
84. Lively JEB 2009 Generation Freq. infection Asexual Sexual periodic under-infection? solution
85. Generation Freq. infection Red Queen predicts: periodic under-infection? solution
86. Generation Freq. infection Red Queen predicts: periodic under-infection? solution Asexuals are under-infected when rare 1
87. Generation Freq. infection Red Queen predicts: periodic under-infection? solution Asexuals are under-infected when rare 1 Asexuals spread when under-infected 2
88. Generation Freq. infection Red Queen predicts: periodic under-infection? solution Asexuals are under-infected when rare 1 Asexuals spread when under-infected 2 We can test these!
89. Year Asexual females Gibson et al. in review Sexual females 6 sites Proportion infected (Weighted mean ± se) periodic under-infection solution
90. Year Asexual females – 10% Sexual females – 26% 6 sites Proportion infected (Weighted mean ± se) periodic under-infection solution Gibson et al. in review
91. 2001-2005 2012-2016 Asexual females Sexual females Year Proportion infected GEE: year * reproductive mode periodic under-infection solution
92. Generation Freq. infection Red Queen predicts: periodic under-infection solution Asexuals are under-infected when rare 1 Asexuals spread when under-infected 2
93. 2001 - 2005 2012 - 2016 past over-infection recent under-infection Proportion asexual Asexuals are under-infected when rare 1 solution
94. 2001 - 2005 2012 - 2016 past over-infection recent under-infection Proportion asexual Asexuals are under-infected when rare 1 35% 23% GLM: sampling period solution
95. 2001 - 2005 2012 - 2016 past over-infection recent under-infection Proportion asexual Asexuals are under-infected when rare 1 35% 23% GLM: sampling period No asexuals at 3 of 6 sites solution
96. Asexuals are under-infected when rare Asexuals spread when under-infected 2 Generation Freq. infection Red Queen predicts: periodic under-infection? solution
97. Asexuals are under-infected when rare 1 Asexuals spread when under-infected 2 Generation Freq. infection Red Queen predicts: periodic under-infection? solution
98. 2012 2013 2014 2015 2016 Proportion asexual Asexuals spread when under-infected 2 solution (mean ± se) 6 sites
99. 2012 2013 2014 2015 2016 Proportion asexual Asexuals spread when under-infected 2 GLM: year 11% 30% 2.6-fold increase solution (mean ± se)
100. Asexuals are under-infected when rare 1 Asexuals spread when under-infected Generation Freq. infection Red Queen predicts: periodic under-infection? solution
101. Asexuals increase a lot at some sites Variation between sites 2 2012 2013 2014 2015 2016 2012 2013 2014 2015 2016 Proportion asexual Year solution (binomial CI)
102. Asexuals increase a lot at some sites 2012 2013 2014 2015 2016 2012 2013 2014 2015 2016 Southwest End Camp 72% 42% Proportion asexual GLM: site*year Year Variation between sites 2 solution (binomial CI)
103. 2012 2013 2014 2015 2016 2012 2013 2014 2015 2016 West Point Halfway 17% 34% Proportion asexual GLM: site*year Year Asexuals increase (less so) at other sites Variation between sites 2 solution (binomial CI)
104. 2012 2013 2014 2015 2016 2012 2013 2014 2015 2016 JMS Swamp 8% 6% Proportion asexual GLM: site*year Year Asexuals fail to increase at two sites Variation between sites 2 solution (binomial CI)
105. Asexual increase covaries with parasites 2 Change in proportion asexual 2012 to 2016 Mean proportion infected solution
106. Asexual increase covaries with parasites 2 Change in proportion asexual 2012 to 2016 Spearman rank: ρ= -0.94, p=0.02 Mean proportion infected SW End Camp W Point Halfway JMS Swamp solution
107. Red Queen predicts: Asexuals are under-infected when rare Asexuals spread when under-infected (at sites with low parasite risk) Generation Freq. infection Red Queen predicts: periodic under-infection? solution
108. Generation Freq. infection consistent with the Red Queen solution Parasites favor sex when asexuals are common Vergara et al. 2014 Am Nat
109. Generation Freq. infection consistent with the Red Queen solution Parasites favor sex when asexuals are common Rare asexuals spread in the absence of selection by parasites
110. Generation Freq. infection consistent with the Red Queen solution Oscillations in asexual frequency Maintenance of sexual females
111. “It is hard to believe that God is as bloody-minded as that” solution
112. “It is hard to believe that God is as bloody-minded as that” solution “It is not God, but a parasite, that is being bloody-minded” ~Maynard Smith, 1985
113. 1. the problem 2. a solution
114. “If I do no more than encourage experimentalists and field workers to collect the relevant data, I shall be well satisfied.” ~ J Maynard Smith 1978, Evolution of Sex Anita Corbin, John O’Grady
115. © Bart Zijlstra Curt Lively Lynda Delph Daniela Vergara Spencer Hall Levi Morran Ngaire Perrin, UC Peyton Joachim Sam Klosak Julie Xu Amrita Bhattacharya Eliza Oldach IU CTRD Christiane Hassel Lively, Hall, Morran labs Acknowledgements DEB DDIG Join the lab in 2019! UVA and Mountain Lake