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Post-Emergence Development of Male Genitalia in Schistocerca Americana

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Post-Emergence Development of Male Genitalia in Schistocerca Americana Copyright by Hojun Song 2002 ABSTRACT Post-emergence development of male genitalia in Schistocerca americana (Orthoptera: Acrididae: Cyrtacanthacridinae) was studied. The present study demonstrates for the first time that the internal skeletal structures in the male genitalia continue to develop after the adult emergence. Also, the taxonomic use of the genitalic characters is reevaluated. An experiment was set up to examine the developmental patterns in the male genitalia and female ovipositor. The mechanism of the genitalic apodeme development is explained by the resilin deposition possibly affected by bursicon secretion. Overall, the structures affected by the cuticle deposition are the apodemes providing muscle attachment sites that enable the necessary movement during copulation. Non-changing structures in the genitalia may be directly involved in the internal courtship during copulation. Therefore, sexually immature individuals can be considered functionally incapable of copulation because the necessary structures have not been fully matured. In order to test if the post-emergence development is widespread, the different aged specimens of Schistocerca gregaria (Forskål) and Locusta migratoria (Linnaeus) were studied. Although the morphology was different between Schistocerca and Locusta, the overall developmental patterns were similar. The sexual maturation period of Schistocerca takes at least 30 days after the emergence. The life history theory predicts that the age at maturity is shaped by the trade-off between survival and reproduction. In Schistocerca, the structures associated with the flight mature earlier in adult development whereas the genitalia continue to develop for about thirty days after emergence. Delayed maturation is well explained by the life history theory when considering that the flight may be the most important trait for survival and that the reproduction is usually costly. A morphological phylogeny of the North American Schistocerca is proposed for the first time. The monophyly of the alutacea complex sensu Dirsh is not supported. I argue that the previous subspecies of S. alutacea are morphologically distinct species. The origin of S. gregaria and the evolution of swarming behavior are briefly discussed in the light of the present phylogenetic hypothesis. ACKNOWLEDGMENTS I wish to thank my advisers, Norm Johnson and John Wenzel, for intellectual support and encouragement, which made this thesis possible, and for their patience in correcting both my stylistic and scientific errors. I also wish to thank Hans Klompen for his valuable criticism on the earlier draft. I thank Greg Sword (USDA ARS Sidney, MT) for allowing me to work at the USDA facility. The enthusiasm for the mysterious Schistocerca that we share will someday result in a fruitful way. Also, my thanks go out to Reg Chapman (University of Arizona) for his constant encouragement and helpful suggestions on our "Schisto Problem." I am grateful to Ted Cohn (University of Michigan) for introducing me to the study of genitalia. His great insight and humor are always appreciated. I also wish to thank Steve Simpson and Stephen Roberts (University of Oxford) for generously providing locust specimens. Some of the ideas in the thesis came from lengthy, but friendly discussions with my fellow graduate students, especially, Marc Branham, Eric Dotseth, and Kurt Pickett. Finally, I wish to thank my parents, Young-Gil Song and Jee-Y eon Koo, and my brother Wonjun, for enduring my whining and for giving moral support. I am also grateful to my soulmate, Haeran Park, for always believing in me. lV VITA March 31, 1977 . Born - Seoul, Korea 2000 ..................................... B.S. Entomology, Cornell University. 2000 -present .......................... Graduate Teaching and Research Associate, The Ohio State University FIELDS OF STUDY Major Field: Entomology v TABLE OF CONTENTS ABSTRACT .................................................................................................................... ii ACKN"OWLEDGMENTS .............................................................................................. iv VITA ............................................................................................................................... v LIST OF TABLES ......................................................................................................... ix LIST OF FIGURES ......................................................................................................... x CHAPTERS: 1. LITERATUREREVIEW ........................................................................................... l 1.1. POST-EMERGENCE DEVELOPMENT IN SCHISTOCERCA .................... 2 1.1. 1. Cuticular development .................................................................... 2 1.1.2. Muscular development. ................................................................... 4 1.1. 3. Ultrastructural development ............................................................ 5 1.1.4. Role of endocrine system during development ................................ 6 1.1.5. Summary ........................................................................................ 7 1.2. EVOLUTION OF LIFE HISTORIES IN SCHISTOCERCA .......................... 9 1.2.1. Biology of Schistocerca .................................................................. 9 1.2.2. Evolution of age at maturity .......................................................... 11 1.2.3. Summary ...................................................................................... 15 1.3. TAXONOMIC USE OF GENITALIC CHARACTERS .............................. 16 1. 3 .1. History of internal genitalia use in Orthoptera ............................... 17 1.3 .2. Variability of male genitalia .......................................................... 19 1.3.3. Male genitalia vs. female genitalia ................................................ 21 1.3.4. Evolution of male genitalia ........................................................... 22 1.3.5. Summary ...................................................................................... 24 V1 2. EXPERIMENTS ...................................................................................................... 25 2.1. SCHISTOCERCA AMERICANA GENITALIA ............................................ 25 2.1.1. Endophallus .................................................................................. 26 2.1.2. Ectophallus ................................................................................... 26 2.1.3. Epiphallus ..................................................................................... 27 2.1.4. Ovipositor..................................................................................... 27 2.2. FUNCTIONAL MORPHOLOGY OF MALE GENITALIA ....................... 33 2.3. MATERIALS AND METHODS ................................................................. 35 2.3.1. Rearing ......................................................................................... 35 2.3.2. Dissection and Data collection ...................................................... 36 2.3.3. Statistical Analysis ....................................................................... 41 2.4. RESULTS ................................................................................................... 42 2.4.1. Developmental sequence of the phallic complex .......................... .42 2.4.2. Rate of development ..................................................................... 44 2.4.3. Post-emergence development of male genitalia in other species .... 61 2.5. DISCUSSION ............................................................................................. 67 2.5.1 Development of genitalia and benefit of delayed maturation .......... 67 2.5.2. Similarities and differences in developmental patterns .................. 72 2.5.3. Taxonomic implication of genitalia development .......................... 74 3. PHYLOGENETIC ANALYSIS ................................................................................ 76 3.1. TAXONOMIC REVIEW ............................................................................ 77 3.2. BIOGEOGRAPHY ..................................................................................... 81 3.3. SWARMING BEHAVIOR AND PHASE POLYMORPHISM ................... 85 3.4. CLADISTIC ANALYSIS ........................................................................... 90 3.4.1. Tax.a ............................................................................................. 90 3.4.2. Characters ..................................................................................... 90 3.4.3. Character coding andAnalysis ...................................................... 91 3.4.4. Results .......................................................................................... 91 3.5. DISCUSSION ............................................................................................. 93 3.5.1. Taxonomic implication ................................................................. 93 3.5.2. Biogeographical implication ......................................................... 95 3.5.3. Evolutionary implication .............................................................. 99 Vll APPENDIX ................................................................................................................. 101 Appendix A Data matrix ..................................................................... 101 Appendix A Data matrix (cont'd)
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