is coevolution going anywhere?

259 Pages·2016·8.59 MB·English

IS COEVOLUTION GOING ANYWHERE?
AN INVESTIGATION OF SEX, VIRULENCE, AND RECIPROCAL
ADAPTATION

Amanda Kyle Gibson

Submitted to the faculty of the University Graduate School
in partial fulfillment of the requirements
for the degree
Doctor of Philosophy
in the Department of Biology,
Indiana University
July 2016
Accepted by the Graduate Faculty, Indiana University, in partial
fulfillment of the requirements for the degree of Doctor of Philosophy

Doctoral committee

Curtis M. Lively, Ph.D. (Chairperson)

Keith Clay, Ph.D.

Spencer R. Hall, Ph.D.

Michael J. Wade, Ph.D.

July 1 2016

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ACKNOWLEDGEMENTS
Above all, I thank my advisor Curt Lively. As a mentor, Curt gave me the opportunities and
the freedom to discover my own path. His door, however, was always open, and his thoughtful,
sincere advice will remain the first to which I turn. Curt took every opportunity to promote me
and my work, and the interests of his students so clearly come first. As a scientist, Curt showed
me the joy and power in big questions, simple tests, historical context, integrity, and a healthy
dose of philosophy. The fact that scientists like Curt exist gives me enormous hope for the future
of our discipline. As a teacher, Curt impressed upon me the value of kindness and respect. He
projected full confidence that my fellow students and I, with our untrained minds, could reach
insights as deep as his own. As a friend, Curt took me on great adventures, withstood my endless
teasing, and shared lots of laughs with me. I promise that all comments about Curt’s
neanderthalness and general confusion were made with the utmost affection and admiration.
I extend my sincere gratitude to my committee. Spencer Hall supported me from day one. He
spent time that I am sure he did not have in sharing analytical approaches, statistical techniques,
and career advice. Spencer’s influence encouraged me to prioritize natural relevance and to
develop the analytical tools I’ll need to do so. Keith Clay welcomed me into his lab for a
semester, and I remember fondly our discussions of blood-sucking arthropods and their
remarkable endosymbionts. I continue to call upon the skills I acquired during my time in the
Clay lab. I thank Mike Wade for pointing me to new places in the literature and welcoming me to
his lab meetings. Covariance now pervades my thinking. Kristi Montooth was a role model to me,
and I thank her for the time and energy that she committed to helping me succeed.
I have been fortunate to have many inspirational mentors throughout my scientific career. I
thank my future postdoctoral advisor, Levi Morran, for his kindness, his respect for my ideas, and
for his ongoing support and friendship. I look forward to our future collaborations. Lynda Delph
was my teammate in both monotonous data collection and exciting adventures. She has had my
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back, pushed me to think deeply, and kept me laughing. I hope to be just like Tatiana Giraud
someday. I admire her generosity, creativity, productivity, and mycophilia. The nine months I
spent in Tatiana’s office, and the opportunities she gave me during that time, inspired me to
pursue a life in science. Michael Hood introduced me to the world of disease in natural
populations and all the wonders that come with it: international travel, alpine scenery, fine
cheeses, and good friends. Michael welcomed me into the marvelous Microbotryum community
with open arms, and I am forever grateful to be deeply rooted in the blend of rigor, scholarship,
curiosity, and fun that is Michael’s science.
The Lively lab, including Kayla King, Deanna Soper, Daniela Vergara, Sam Slowinski,
Amrita Bhattacharya, Kara Million, Zoe Austin, Maurine Neiman, Britt Koskella, Idelle Cooper,
and Farrah Bashey-Visser, has been a constant source of thought-provoking ideas, constructive
criticism, advice, and inspiration. I feel fortunate to be included in this line-up of accomplished,
thoughtful scientists. The Hall lab, including Dave Civitello, Marta Shocket, Jessica Hite, Alex
Strauss, Paul Orlando, Jason Walsman, and Maja Sljivar, welcomed me at their lab meetings, and
their brains and passion helped me to keep thinking about disease ecology, math, and complexity.
Many people at Indiana University made possible the successful completion of my
dissertation. First and foremost, I could not have asked for a more dedicated and enthusiastic
group of undergraduates, including Kayla Mitman, Ian Gelarden, Laura Sloan, McKenna Penley,
Peyton Joachim, Sam Klosak, and Julie Xu. This work would not have happened without them,
and it would have been a whole lot less fun. You all remind me why I do what I do. The Common
Themes in Reproductive Diversity training grant provided me with the funding necessary to do
my work. I am very grateful for the diverse and lively discussions of the CTRD group and the
support of the faculty, including Ellen Ketterson, Armin Moczek, Greg Demas, Troy Smith and
many others. Christiane Hassel at the Flow Cytometry Core Facility put up with my questions
and my clogs and was superb company during my many hours in the basement of Jordan Hall.
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Jesualdo Fuentes is the finest coauthor with whom I have had the fortune to work. Thank you for
your patient explanations, thoughtful reflections, and kind support. Leonie Moyle and her lab
generously allowed me to spend hours on their fancy computer and invited me to contribute to
one of their many fine studies. Gretchen Clearwater and other members of the Biology
Department staff have smoothed many a hurdle for me.
Last, but by no means least, I thank my friends and family for their unconditional support.
My cohort is undoubtedly the smartest, fiercest and most extraordinarily good-looking cohort to
ever have graced the halls of Jordan. Thank you for the friendship and hilarity. I extend my
sincere gratitude to Ngaire Perrin for her herculean efforts to let snail science happen in Kaikoura
and for her friendship. I am a saner, happier and fuller person thanks to you, and I will recall our
Kaikoura adventures as the best moments of my Ph.D. To my Amherst Biffles and high school
pals, I am honored to be friends with such clever, funny, and strong people. I thank my mother for
editing nearly all of my grant applications and for breaking the barrier for future Dr. Gibsons. I
thank my father for his sage advice and for keeping me out of prison for tax evasion. I thank my
brother for keeping me semi-cool. I am eternally grateful to Jered Wendte for always seeing the
best in me. You make me a better scientist and a better person.

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Amanda Kyle Gibson
IS COEVOLUTION GOING ANYWHERE? AN INVESTIGATION OF SEX,
VIRULENCE AND RECIPROCAL ADAPTATION
The overarching motivation of evolutionary ecology is to explain why natural
populations harbor so much genetic and phenotypic diversity. This dissertation features
two particularly important and puzzling forms of diversity: variation in reproductive
mode and variation in species interactions. The ultimate conclusion of this dissertation is
that host-parasite coevolution underlies variation in both.
Why do females produce genetically variable offspring, via sexual outcrossing?
The evolution and maintenance of sex remains one of the great enigmas of evolutionary
biology. Chapter 1 lays the foundation for the problem. A combination of theory and data
from semi-natural mesocosms shows that sex has a two-fold cost relative to asexual
reproduction in the freshwater snail Potamopyrgus antipodarum. Yet asexual and sexual
females coexist in nature. A strong selective force must therefore counterbalance the cost
of sex. Previous work had shown that a sterilizing trematode, Microphallus sp.,
commonly infects P. antipodarum in natural populations. In Chapter 2, field surveys and
experimental inoculations reveal substantial variation in both infection prevalence and in
host susceptibility to local Microphallus around a single small lake. Variation in
prevalence arises from variation in environmental factors and variation in susceptibility, a
proxy for coevolutionary selection. Chapter 3 shows that the frequency of sexual females
also varies substantially around this lake and is tightly positively correlated with
susceptibility. Susceptibility can explain the majority of geographic variation in sex, far
more than can infection prevalence. This result specifically points to the significance of
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coevolutionary selection in the maintenance of sex. Chapter 4 provides support for the
Red Queen that is taxonomically and conceptually unique. Applying phylogenetic
comparative methods to the nematode phylum reveals that parasitic nematode taxa are
more likely to be obligately outcrossing than their free-living relatives.
Variation in parasite virulence is another curious anomaly in evolutionary
biology. Chapter 5 presents the results of experimental selection on reduced antagonism
between a nematode host and its virulent bacterial parasite. Reduced antagonism evolved
only when host and parasite were able to coevolve. This result argues that coevolution
contributes to the evolution of virulence. Ultimately, this dissertation shows that
coevolution lies at the root of some of evolution’s most puzzling phenomena and can
explain the maintenance of genetic and phenotypic diversity in natural populations.

Curtis M. Lively, Ph.D. (Chairperson)

Keith Clay, Ph.D.

Spencer R. Hall, Ph.D.

Michael J. Wade, Ph.D.

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TABLE OF CONTENTS
Title Page…………………………………………………………………………………..i
Acceptance Page…………………………………………………………………………..ii
Acknowledgements………………………………………………………………………iii
Abstract…………………………………………………………………………………...vi
Table of Contents………………………………………………………………………..viii
List of Appendixes………………………………………………………………………...x
Introduction………………………………………………………………………………..1
Chapter 1 - The two-fold cost of sex: experimental evidence from a natural system…...21
Introduction………………………………………………………………………22
Results and Discussion………………………………………...………………...23
Methods…………………………………………………………………………..34
Supporting Information…………………………………………………………..42
Chapter 2 – Fine-scale spatial covariation between infection prevalence and susceptibility
in a natural population…………………………………………………………………...53
Introduction………………………………………………………………………54
Methods…………………………………………………………………………..58
Results……………………………………………………………………………68
Discussion………………………………………………………………………..78
Supporting Information…..………………………………………………………84
Chapter 3 – Within-population covariation between sexual reproduction and
susceptibility to local parasites…………………………………………………………..86
Introduction………………………………………………………………………87
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Methods…………………………………………………………………………..93
Results…………………………………………………………………………..101
Discussion………………………………………………………………………111
Supporting Information…………………………………………………………115
Chapter 4 – A phylogenetic test of the Red Queen hypothesis: outcrossing and parasitism
in the Nematode phylum………………………………………………………………..129
Introduction……………………………………………………………………..130
Methods…………………………………………………………………………133
Results…………………………………………………………………………..140
Discussion………………………………………………………………………147
Supporting Information…………………………………………………………153
Chapter 5 – The evolution of reduced antagonism: a role for host-parasite
coevolution.......................................................................................................................155
Introduction……………………………………………………………………..156
Methods…………………………………………………………………………159
Results…………………………………………………………………………..168
Discussion………………………………………………………………………174
Supporting Information…………………………………………………………178
References………………………………………………………………………………190
Curriculum vita

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LIST OF APPENDIXES
Appendix I - The Red Queen’s race: an experimental card game to teach coevolution..224
Introduction……………………………………………………………………..225
The Red Queen’s Game...………………………………………………………230
Extensions………………………………………………………………………238
Conclusion……………………………………………………………………...242

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