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UNVIERSITY of CALIFORNIA RIVERSIDE the Biology of Reproductive Delays in Mammals

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UNVIERSITY of CALIFORNIA RIVERSIDE the Biology of Reproductive Delays in Mammals UNVIERSITY OF CALIFORNIA RIVERSIDE The Biology of Reproductive Delays in Mammals: Reproductive Decisions, Energetics, and Evolutionary Ecology A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Evolution, Ecology and Organismal Biology by Teri Jean Orr December 2012 Dissertation Committee: Dr. Kimberly A. Hammond, Chairperson Dr. Marlene Zuk Dr. Theodore Garland, Jr. The Dissertation of Teri Jean Orr is approved: Committee Chairperson University of California, Riverside Acknowledgments I would like to thank and acknowledge several people and funding sources for the success of this project. I would like to start by thanking my father for inspiring me to consider nature big and small on a daily basis. While I have yet to study the slugs or aphids he so patiently allowed me to drag into the house nor the tarantulas and horned lizards he brought home for me to see I owe to him my enthusiasm for nature. Furthermore, I thank him for the countless visits to bookstores and trips to museums, pet shops that ultimately led in some way to the pages that follow. I would also like to thank all of my brothers and sisters for their continual support as I have perused my degree. Funding.—My dissertation was supported by several funding sources including the UC Mexus, a UC Riverside Biology department Newell award, and Loomer award, as well as an American Society of Mammalogists grant-in-aid, and a UC dissertation year fellowship. This research would not have been possible without this support. UNAM and Polytechnico.—I am grateful to my Mexican collaborators for their help in establishing my field site and assistance with logistical issues. Specifically I would like to thank Drs. Rodrigo Medellin, and Jorge Ortega. I am also indebted to Dr. Rafael Avila-Flores and several students who assisted me in the field with data collection; Luis Guillermo Munoz Lacy, Tatyana Soberon, Maria Jose Soberon, Ruben Galicia and Dr. Gerardo Suzan helped secure supplies for use while in Mexico. iii Angelica Mancha helped hand-craft several items used during my project including netting materials. I would also like to thank and acknowledge Rene Colderon at Margaritas ranch for providing facilities and allowing the use of ranch equipment during my field work. I also thank Doña Conchita for feeding our stomachs and hearts in Ayotoxco. Department of Biology.—I would like to formally thank my committee members; Drs. Kimberly Hammond, Theodore Garland, Jr., and Marlene Zuk for their dedication, time and patience. Kimberly Hammond was a friend, mentor and inspiration. Ted Garland a statistical wiz who took many hours to help me with analyses. Marlene Zuk provided an exciting intellectual environment and helped me improve my writing. At UC Riverside I was helped by Dr. Rich Cardullo and Dr. Cathy Thaler on several occasions when trying to decipher various assays and Melissa Gomez on numerous occasions for the various crises that arise as a graduate student. Dr. Doug Altshuler served as an excellent sounding board and enthusiastic ear during the development of my project and while I was going through my comprehensive exams. I would also like to thank Dr. David Reznick for inspirational lab meetings. I thank Dr. Mark Chappell for general mentorship. Dr. Chris E. Oufiero helped extensively with general advice including how to stay sane in graduate school, but also helped with reading and revising nearly every proposal I wrote at UCR as well as countless other drafts. Additionally he helped numerous times with phylogenetic methodology type questions. Finally, I thank Dr. Sonia Diaz who has been a lab mate, field assistant and but most importantly a valuable friend throughout my graduate career at UCR. iv Other institutions.—Dr. Wendy Hood helped extensively with the milk chapter by sending me early drafts of her chapters on bat milk collection methodology and she spent extensive time tracking down protocols and responding to countless emails on how to set up milk assays. I would also like to thank her then-student Dr. Amy Skibiel for countless e-mails and telephone calls that made her help. Dr. Blair Wolf has remained a collaborator during my tenure as a PhD student helping me by providing insight into many methodologies including field metabolic rate and read drafts of proposals. Dr. John J. Rasweiler, IV will perhaps never know how helpful his suggestions and protocols were to the success of this research project, I am truly grateful for the time he took to address my questions. Miss Theresa ‘Phainapepla’ Hyde helped with data collection in Mexico. I would like to dedicate my dissertation in memory of my grandmother Leona May Thompson, who instilled in me a love of biology, learning and life. Acknowledgements (Chapter 1).—I would like to thank Dr. Johnathan Davies for sharing his latitude data, and Dr. Olaf Binina-Emmonds for providing his phylogenetic tree. Dr. Anothony Ives has been instrumental in this project through the sharing and continued development of his PGLMM program. Acknowledgements (Chapter 2).—I would like to thank two anonymous reviewers who provided detailed insightful comments on an earlier draft. I also thank E. Charnov, D. Fairbairn, A. Furness, V. Hayssen, P.D. Heidman, D.J. Hosken, C.E. Oufiero, P.A. Racey, D. Reznick, and J.J. Rasweiler, IV for insightful exchanges. v Acknowledgements (Chapter 3).—I thank the museum personnel who helped make this project possible: LA County Museum; J. Dines, Museum of Vertebrate Zoology; E. Lacey, C. Corbin, The American Museum of Natural History; D. Lunde, N. Simmons, E. Westwig. Additionally, C. Oufiero, P. Heidman and members of the Hammond and Zuk labs provided useful comments. vi “May your trails be crooked, winding, lonesome, dangerous, leading to the most amazing view. May your mountains rise into and above the clouds. “ Edward Abby vii ABSTRACT OF THE DISSERTATION The Biology of Reproductive Delays in Mammals: Reproductive Decisions, Energetics, and Evolutionary Ecology by Teri Jean Orr Doctor of Philosophy, Graduate Program in Evolution, Ecology, and Organismal Biology University of California, Riverside, September 2012 Dr. Kimberly A. Hammond, Chairperson My dissertation investigates the unique ways organisms put effort (time, energy, and/or nutrients) towards reproduction. My research asked how delays might allow mammals to allocate limited resources to reproduction (i.e., are delays adaptive?) and consisted of several components aimed at understanding the causes and consequences of reproductive delays in mammals. First, I used the phylogenetic comparative method to examine ecological and phylogenetic predictors of obligate delayed implantation in the order Carnivora in 157 species using published data. I evaluated whether average latitude of the geographic range, diet or phylogenetic position are predictors of whether a species exhibits delayed implantation. My results suggest that the presence of delays is positively related to body size and seasonality, and also varies with diet. Second, I dissected museum specimens of male bats (N = 47 species) to measure size of the testes and then indirectly assess if reproductive delays facilitate sperm competition. By reviewing the literature and inspecting museum specimens of bats with different types of delays, including viii some without delays, I was able to determine that delays might facilitate postcopulatory sexual selection (competition between the sperm from different males). Specifically, I tested and confirmed the prediction that males in species with delays between mating and egg-fertilization have larger testes than males in species that do not delay before fertilization. Third, I empirically evaluated some of the costs and benefits of delays in a species that has pregnancies both with and without delays, Artibeus jamaicensis. I compared diet, and food availability between the two pregnancies to evaluate the hypothesis that delays allow females to time the most expensive stage of reproduction, lactation, with periods of greatest food abundance. I found that previous hypotheses that A. jamaicensis uses delays to time lactation with fruit abundances may be more complex than previously realized including a dependence upon insects during late pregnancy and some lactational periods. My dissertation contributes important information on adaptive significance of delays in mammals. ix Table of Contents Introduction to the Dissertation………………………………………………………………………….1 Literature Cited…………………………………….………………………………………………..9 Chapter 1: Phylogenetic analysis of delayed implantation in the Carnivora…..………………11 Abstract…………………………………………………………………………………………….12 Introduction………………………………………………………………………………………...14 Methods…………………………………………………………………………………………….18 Results………………………………………………………………………….………................27 Discussion………………………………………………………………………………………….31 Literature Cited…………………………………………………………………………………….34 Chapter 2: Reproductive delays in mammals: an unexplored avenue for post-copulatory sexual selection………………………………………..………………………………………...63 Abstract…………………………………………………………………………………………….64 Introduction………………………………………………………………………………………...65 Results (consequences of delays)………………………………………………………………79 Conclusions……………………………………………………………………………………....108 Literature Cited…………………………………………………………………………………..110 Chapter 3: Reproductive delays facilitate post-copulatory sexual selection in bats: evidence from museum specimens…………………………………………………………………….133 Abstract…………………………………………………………………………………………...134 Introduction……………………………………………………………………………………….136
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