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The Adaptive Significance and Prevalence of Courtship Feeding Behavior in Hawaiian Swordtail Crickets

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The Adaptive Significance and Prevalence of Courtship Feeding Behavior in Hawaiian Swordtail Crickets ABSTRACT Title of Document: THE ADAPTIVE SIGNIFICANCE AND PREVALENCE OF COURTSHIP FEEDING BEHAVIOR IN HAWAIIAN SWORDTAIL CRICKETS Tagide deCarvalho, Doctor of Philosophy, 2008 Directed By: Dr. Kerry L. Shaw, Professor Males of many insect species feed their partner during courtship and mating. Studies of male nutrient donation in various systems have established that nuptial feeding has evolved mostly through sexual selection. Although there is extensive diversity in form, the function of nuptial gifts is typically limited to either facilitating copulation or increasing ejaculate transfer, depending on the time at which the gift is consumed by females. Unlike other insects, the Hawaiian swordtail cricket Laupala (Gryllidae: Trigonidiinae) exhibits serial transfer of nuptial gifts. Males transfer multiple spermless ‘micro’ spermatophores over several hours before mating at the end of the day (i.e. before the transfer of a single sperm-containing ‘macro’ spermatophore). By experimental manipulation of male microspermatophore donation, I tested several hypotheses pertaining to the adaptive significance of nuptial gifts in this system. I found that microspermatophore transfer improves insemination, by causing the female reproductive tract to take in more sperm. This result reveals a previously undocumented function for premating nuptial gift donation among insects. Enhanced sperm transfer due to microspermatophore donation may represent male manipulation or an internal mechanism of post-copulatory choice by females. I also performed experimental manipulation of male photoperiod to investigate how time and gender influence nuptial gift production and mating behavior. I found that the timing of mating is limited in males but not females and that the time of pair formation has consequences for the degree of nuptial gift donation, which suggests that both mating timing and microspermatophore number is important for male reproductive success. Finally, I observed the mating behavior of several trigonidiine taxa for a comparative analysis of sexual behavior and found that other genera also utilize spermless microspermatophores, which suggests that microspermatophore donation may be a common nuptial gift strategy among swordtail crickets. The elaborate nuptial feeding behavior of Hawaiian swordtail crickets prior to mating represents a newly discovered strategy to increase male insemination success rather than mating success. Based on this unexpected result, it is worth exploring whether courtship behaviors in other cricket or insect mating systems have also evolved to increase sperm uptake. THE ADAPTIVE SIGNIFICANCE AND PREVALENCE OF COURTSHIP FEEDING BEHAVIOR IN HAWAIIAN SWORDTAIL CRICKETS By Tagide deCarvalho Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2008 Advisory Committee: Professor Kerry Shaw, Chair Professor Charles Mitter Professor Kaci Thompson Professor Barbara Thorne Professor Gerald Wilkinson © Copyright by Tagide deCarvalho 2008 Preface This dissertation contains a single introduction section and three chapters. Each chapter is presented in manuscript form, with abstract, introduction, methods, results, and discussion, followed by tables, figure legends, and figures. A single bibliography section occurs at the end for references cited throughout the dissertation. ii Dedication To my grandfather, Dr. Sergio deCarvalho, who started me on the path of scientific inquiry and inspired me to pursue this degree. iii Acknowledgements I would like to thank my dissertation advisor, Kerry Shaw, for serving as a role model for excellence in the scientific process and writing, as well as her support in my endeavor to raise a family during my graduate studies. Thank you to Pat Danley and Tami Mendelson for their guidance and support during their postdoc tenure in the Shaw lab. Thanks to my labmates: Jamie Grace, Jenna Jadin and Sky Lesnick for their help with all things cricket related. Thanks to Dan Fergus for providing an enormous amount of help with technical issues and experimental design. Thanks to my committee members, Emily Amitin, Dan Fergus, and Brian Coyle for their valuable comments on this manuscript. Thanks to Dan Otte for sharing his expertise on Hawaiian crickets and fielding all of my pestering emails. Thanks to Betsy Gagne at the Department of Land and Natural Resources in Hawaii for her advice and help acquiring collection permits. Thanks to Dave Funk for sharing his unpublished work on cricket behavior. Thank you to Carol Coyle and my mother for their support and help in raising my children. Thank you to my father for imparting his love of knowledge and passion for science to me. Special thanks to my husband, Brian Coyle, for his support with absolutely everything including fieldwork assistance, manuscript editing, illuminating discussions and child rearing. My research was financially supported by the Dr. Mabel S. Spencer Award for Excellence in Graduate Achievement and a BEES Darwin fellowship and grants from the Animal Behavior Society, the NSF Biology of Small Populations RTG, the Orthopterists Society and the University of Maryland Ilene H. Nagel Travel Award. iv Table of Contents Preface................................................................................................................................. ii Dedication..........................................................................................................................iii Acknowledgements............................................................................................................ iv Table of Contents................................................................................................................ v List of Tables .................................................................................................................... vii List of Figures.................................................................................................................... ix INTRODUCTION .............................................................................................................. 1 CHAPTER I Premating nuptial gifts enhance sperm transfer in the Hawaiian swordtail cricket, Laupala cerasina ................................................................................................................ 7 ABSTRACT.................................................................................................................... 7 INTRODUCTION .......................................................................................................... 8 METHODS ................................................................................................................... 13 RESULTS ..................................................................................................................... 20 DISCUSSION............................................................................................................... 24 TABLES ....................................................................................................................... 31 FIGURE LEGENDS..................................................................................................... 34 FIGURES...................................................................................................................... 35 CHAPTER II Males drive nuptial gift number and timing of mating activity in the Hawaiian swordtail cricket, Laupala cerasina.................................................................................. 38 ABSTRACT.................................................................................................................. 38 INTRODUCTION ........................................................................................................ 39 METHODS ................................................................................................................... 44 RESULTS ..................................................................................................................... 48 DISCUSSION............................................................................................................... 50 TABLES ....................................................................................................................... 57 FIGURE LEGENDS..................................................................................................... 60 FIGURES...................................................................................................................... 61 v CHAPTER III A comparative analysis of Hawaiian swordtail cricket mating behavior ......................... 64 ABSTRACT.................................................................................................................. 64 INTRODUCTION ........................................................................................................ 65 METHODS ................................................................................................................... 72 RESULTS ..................................................................................................................... 75 DISCUSSION............................................................................................................... 82 TABLES ....................................................................................................................... 90 FIGURE LEGENDS....................................................................................................
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