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The Pennsylvania State University the Graduate School College Of The Pennsylvania State University The Graduate School College of Agricultural Sciences NATURAL HYBRIDIZATION AND SPECIATION IN RHAGOLETIS (DIPTERA: TEPHRITIDAE) A Thesis in Entomology by Dietmar Schwarz © 2004 Dietmar Schwarz Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2004 The thesis of Dietmar Schwarz was reviewed and approved* by the following: Bruce A. McPheron Professor of Entomology Thesis Adviser Chair of Committee Warren G. Abrahamson, II David Burpee Professor of Plant Genetics Bucknell University Special Member Thomas C. Baker Professor of Entomology Ottar N. Bjornstad Assistant Professor of Entomology Stephen W. Schaeffer Associate Professor of Biology Gary W. Felton Professor of Entomology Head of the Department of Entomology *Signatures are on file in the Graduate School ABSTRACT Hybridization has long been regarded as an important source of evolutionary novelty in plants. Zoologists, in contrast, have regarded hybridization merely as an artifact of incomplete reproductive isolation. Especially the formation of new animal species via hybridization has been deemed highly unlikely (unless it results in parthenogenetic, polyploid taxa). Here I present the first case of hybridization in an insect that has resulted in an isolated, diploid and bisexually reproducing population. I discovered the infestation of invasive honeysuckle, Lonicera spp., by flies belonging to the R. pomonella species complex (Diptera: Tephritidae). Because all members of this species complex are native to North America, the infestation of Lonicera has to be the result of a recent host shift. Multilocus nuclear genotypes and mitochondrial DNA sequences showed that the Lonicera Fly originated via hybridization between the blueberry maggot R. mendax and the snowberry maggot R. zephyria. The same data also provide indirect evidence for the reproductive isolation of the Lonicera Fly from its parent taxa. I tested the acceptance of different host fruits by the Lonicera Fly, R. mendax and R. zephyria in behavioral experiments. These experiments suggest that, compared to host races and described sibling parent species, the Lonicera Fly shows an intermediate level of behavioral isolation from its parent taxa. At the same time, the Lonicera Fly's host selection behavior indicated a higher phenotypic variability when compared to R. mendax and R. zephyria. iii This unique combination of host shift and hybridization suggests sympatric speciation via host shift as the mechanism by which the hybrid Lonicera Fly formed. I discuss how the increased phenotypic variability of hybrid origin populations could facilitate adaptive speciation. I further argue that hybrid speciation in parasitic animals could be common because the ecological conditions of the Lonicera Fly system are frequently encountered in nature. Finally I integrate the findings of this study with previous results on speciation and hybridization in the genus Rhagoletis and other animal taxa. I propose the term “biological metaspecies” to describe the evolution of the Rhagoletis pomonella species group. A biological metaspecies is a group of ecologically differentiated sibling taxa that are linked by occasional hybridization. Each single taxon might lack the necessary variation to colonize a new niche, but such variation could be maintained on the metaspecies level and become mobilized by hybridization. iv TABLE OF CONTENTS List of Tables ................................................................................................................. vii List of Figures............................................................................................................... viii Acknowledgements...........................................................................................................x Chapter 1. INTRODUCTION...........................................................................................1 References.................................................................................................................10 Chapter 2. HOST SHIFT TO AN INVASIVE PLANT TRIGGERS RAPID ANIMAL HYBRID SPECIATION...........................................................................................14 Methods.....................................................................................................................21 Supplementary Material............................................................................................24 References.................................................................................................................30 Tables........................................................................................................................34 Figures.......................................................................................................................40 Chapter 3. REPRODUCTIVE AND ECOLOGICAL ISOLATION OF THE LONICERA FLY AND ITS PARENTS........................................................................................45 Introduction...............................................................................................................45 Host choice behavior...........................................................................................45 Host-independent assortative mating..................................................................51 Materials and Methods..............................................................................................53 Fly populations....................................................................................................53 Host choice and acceptance experiments............................................................55 Host-independent assortative mating..................................................................63 Results.......................................................................................................................65 No-choice host acceptance experiments .............................................................65 Proportion of females showing oviposition behavior ...................................65 Length of initial search interval ....................................................................67 Differences in behavior preceding the first ovipositor probingt...................69 Three-way host choice experiment .....................................................................71 Ovipositor probing and oviposition ..............................................................71 Search behavior until first oviposition..........................................................73 Host independent assortative mating ..................................................................75 Frequency of con- and heterospecific matings .............................................75 Influence of live body mass on mating success............................................76 Discussion.................................................................................................................77 Behavioral isolation by host acceptance and host preference.............................77 Hypothesis 1.a.: Each fly taxon shows greater preference (or acceptance) for its own host fruit species than for host fruits of other taxa...........................77 Behavioral isolation between described Rhagoletis species...................77 v No-choice host acceptance versus three-way choice experiment...........80 Is the Lonicera Fly ecologically isolated? ..............................................82 How do the described Rhagoletis species respond to Lonicera fruit?82 How does the Lonicera fly respond to the host fruit of described parent species? .............................................................................................85 Hypothesis 2.a.: The Lonicera Fly is less discriminant in its host choice (or, conversely, accepts a greater spectrum of hosts) than its parent taxa...........87 Is the Lonicera Fly more variable in its host selection than its parent taxa? ........................................................................................................87 What is the mechanism that generates phenotypic variability in the Lonicera Fly?..........................................................................................89 Hypothesis 2.b.: Lonicera flies will discriminate less against Lonicera (or more readily accept Lonicera as a host) than will the parental taxa.............91 Does hybridization facilitate a host shift to Lonicera? ...........................91 Conclusions...................................................................................................93 Is the Lonicera Fly a likely example of a herbivore hybrid bridge?.......93 A model for the initial formation of the Lonicera Fly............................94 Host independent assortative mating ..................................................................94 Sexual selection versus sexual isolation .......................................................95 Asymmetry of heterospecific matings ..........................................................96 Consequences for hybridization....................................................................98 References.................................................................................................................98 Tables......................................................................................................................102 Figures.....................................................................................................................105
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