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The Pennsylvania State University The Pennsylvania State University The Graduate School Department of Entomology ECOLOGY AND EPIDEMIOLOGY OF RNA VIRUSES IN HYMENOPTERAN POLLINATORS A Dissertation in Entomology by Rajwinder Singh © 2011 Rajwinder Singh Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2011 The dissertation of Rajwinder Singh was reviewed and approved* by the following: Edwin Rajotte Professor of Entomology Co-Chair of Committee Dissertation Co-Advisor Diana Cox-Foster Professor of Entomology Co-Chair of Committee Dissertation Co-Advisor Frederick Gildow Professor of Plant Pathology Edward Holmes Professor of Biology Rosalind James Research Leader, USDA-ARS Pollinating Insects Research Unit Department of Biology, Utah State University Logan, UT Special Member Gary Felton Professor of Entomology Head of the Department of Entomology *Signatures are on file in the Graduate School ABSTRACT Pollinators are critical to agricultural production and maintenance of natural plant communities. However, widespread declines in pollinator populations have become a cause of concern. RNA viruses are suspected as one of the major contributors to honey bee (Apis mellifera) losses including the recent malady, colony collapse disorder (CCD). But, our knowledge of viral diseases in other managed and wild bee species is very limited. This dissertation investigates the ecology and epidemiology of RNA viruses in different hymenopteran pollinators. Detection of RNA viruses in thirteen non-Apis hymenopteran species, using reverse transcriptase-PCR, indicated widespread occurrence of these viruses. This study provides the first evidence of pollen as a route of inter-taxa transmission of RNA viruses in hymenopteran pollinators. Molecular detection of viruses in pollen pellets from foragers and the subsequent phylogenetic analyses support that these viruses are disseminating freely among the pollinators via the pollen itself. The viruses in the pollen and honey stored in the hive were demonstrated to remain infectious for at least six months of storage. RNA viruses were also widespread in commercial colonies of the bumble bee, Bombus impatiens, the major pollinator of greenhouse crops, but were less prevalent in the alfalfa leafcutting bees (ALCB) (Megachile rotundata) and the alkali bees (Nomia melanderi), the two solitary bees essential for the alfalfa seed crop. Inter- taxa transmission of one of these viruses was further demonstrated in containment greenhouse experiments, where the recently described Israeli acute paralysis virus (IAPV) moved between honey bees and bumble bees within ten days. IAPV disseminated throughout the bee body including the ovaries and eggs when fed to virus-free bumble bee queens, but remained restricted in the gut of the ALCB larvae. IAPV infection negatively impacted the health of bumble bee and honey bee colonies under greenhouse conditions, and adult survivorship and larval diapause in ALCB laboratory bioassays. However, further studies are needed to understand the role of IAPV iii and related viruses in the recent declines in field populations of different pollinators. This study increases our understanding of RNA virus ecology and epidemiology and may help explain bee disease patterns and pollinator declines in general. iv TABLE OF CONTENTS LIST OF FIGURES..................................................................................................................vii LIST OF TABLES ...................................................................................................................x ACKNOWLEDGEMENTS .....................................................................................................xi Chapter 1 Introduction .............................................................................................................1 Literature cited .................................................................................................................7 Chapter 2 RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmsiion via Pollen and Potential Impact on Non-Apis Hymenopteran Species .......14 Abstract.............................................................................................................................14 Introduction ......................................................................................................................15 Materials and methods......................................................................................................19 Results ..............................................................................................................................25 Discussion.........................................................................................................................31 Literature cited..................................................................................................................39 Chapter 3 Prevalence of RNA viruses in the commercial greenhouse bumble bee (Bombus impatiens), and the pathology, health impacts and inter-taxa transmission of Israeli acute paralysis virus (IAPV) in bumble bees and honey bees ..........................60 Abstract.............................................................................................................................60 Introduction ......................................................................................................................61 Materials and methods......................................................................................................64 Results ..............................................................................................................................69 Discussion.........................................................................................................................75 Literature cited..................................................................................................................82 Chapter 4 Prevalence and Impact of RNA Viruses in Non-Apis Commercially Managed Bees Essential for Alfalfa Seed Production .....................................................................118 Abstract.............................................................................................................................118 Introduction ......................................................................................................................119 Materials and methods......................................................................................................121 Results ..............................................................................................................................127 Discussion.........................................................................................................................130 Literature cited..................................................................................................................135 Chapter 5 Conclusion...............................................................................................................149 Literature cited .................................................................................................................155 Appendix A Color and number of pollen pellets having detectable virus ..............................158 v Appendix B Primer sequences for gene regions detected and sequenced in the chapter 2.....159 Appendix C Primer sequences and the gene regions detected for RNA viruses in pollinators in the chapter 3. ..............................................................................................160 Appendix D Primer sequences and the gene regions detected for RNA viruses in pollinators in the chapter 4. ..............................................................................................161 vi LIST OF FIGURES Figure 1-1: Known routes for horizontal and vertical transmission of RNA viruses in the honey bee, Apis mellifera. ................................................................................................13 Figure 2-1: Comparison of viral presence in pollen pellets and their corresponding forager with her body dissected into two regions with or without salivary glands, to determine if salivary secretions of the forager are associated with virus in pollen pellets. ............................................................................................................................47 Figure 2-2: Proportion of virus species detected in 65 honey bee pollen foragers versus their pollen pellets. ...........................................................................................................49 Figure 2-3: Determination of how DWV and BQCV are associated with pollen....................50 Figure 2-4: Test of DWV infectivity in stored pollen and honey and detection of SBV movement from outside source through transmission of DWV and SBV to eggs by queens...............................................................................................................................51 Figure 2-5: Phylogenetic comparison of DWV sequences detected in honey bee foragers, pollen pellets, and non-Apis hymenopteran species.........................................................52 Figure 2-6: Phylogenetic comparison of BQCV sequences detected in honey bee foragers, pollen pellets, and non-Apis hymenopteran species.........................................................54 Figure 2-7: Phylogenetic comparison of IAPV sequences detected in honeybees and non-
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