Global and Local Population Genetics of the Mediterranean Fruit Fly, Ceratitis Capitata, an Invasive Pest of Fruit Crops
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Global and local population genetics of the Mediterranean fruit fly, Ceratitis capitata, an invasive pest of fruit crops Maria Belen Arias Mella A thesis submitted for the degree of Doctor of Philosophy Department of Life Sciences Imperial College London U.K. September 2018 Abstract Invasive species are recognised as one of the most important, growing threat to food biosecurity, causing a significant economic loss in agricultural systems. Despite their damaging effect, they are attractive models for the study of evolution and adaptation in newly colonised environments. Currently, the global climate represents one key potential stressors to impact the food biosecurity because of its influence in the distribution and change in the abundance of agricultural pests. The tephritid fruit flies (Diptera: Tephritidae) contain some of the most successful invaders and most devastating agricultural pests recognised worldwide. Among them, the Mediterranean fruit fly Ceratitis capitata and the South American fruit flies in the genus Anastrepha are particularly important for crop production. Insecticides have been used extensively for their control. This thesis investigates factors that are related to invasiveness in these species, in order to provide novel information that will ultimately improve management control methods. First, environmental niche modelling was used to determine the influence of climate change in the potential habitat distribution of C. capitata, predicting both polewards expansion as well as greater connectivity. Next, historical global dispersal patterns of the medfly over the past two centuries were investigated using molecular and genetic approaches. In Chapter 4, different attempts to identify the point mutation G328A Ccace2 gene that confers resistance to insecticides were assessed at local and intercontinental scale, in part by studying museum specimens from before and after the use of pesticides. Additionally, to improve genetic knowledge of this invasive species, the mitogenome of different species of Anastrepha were sequenced and analysed together with others tephritid. This investigation provides crucial information revealing the evolutionary factors that influence the medfly’s successful invasions and will contribute to the development of evidence-driven pest management protocols, especially in the Americas, including the choice among different control methods as well as the establishment of quarantine procedures to interrupt colonisation routes. 2 Table of Contents List of Figures .................................................................................................................. 5 List of Tables ................................................................................................................... 7 Declaration of Originality ................................................................................................. 8 Copyright Declaration ...................................................................................................... 9 Acknowledgements ....................................................................................................... 10 CHAPTER 1 General Introduction ...................................................................................................... 11 CHAPTER 2 The impact of climate change on the potential distribution of the agricultural pest Ceratitis capitata: implication for pest control management ........................................................ 24 2.1 Introduction .......................................................................................................... 24 2.2 Data and Methods ................................................................................................ 27 2.3 Results ................................................................................................................. 30 2.4 Discussion ............................................................................................................ 40 CHAPTER 3 Population genetics and migration pathways inference of the Mediterranean fruit fly Ceratitis capitata inferred with coalescent methods ...................................................... 45 3.1 Introduction .......................................................................................................... 45 3.2 Material and Methods .......................................................................................... 48 3.3 Results ................................................................................................................. 53 3.4 Discussion ............................................................................................................ 69 3 CHAPTER 4 Molecular approach to insecticide resistance in museum specimens and modern natural populations of the medfly: looking for Ccace2 point mutation ....................................... 76 4.1 Introduction .......................................................................................................... 76 4.2 Material and Methods .......................................................................................... 83 4.3 Results ................................................................................................................. 92 4.4 Discussion .......................................................................................................... 103 CHAPTER 5 Complete mitochondrial genome and molecular phylogeny of three species of Anastrepha .................................................................................................................................... 110 5.1 Introduction ........................................................................................................ 110 5.2 Material and Methods ........................................................................................ 112 5.3 Results ............................................................................................................... 115 5.4 Discussion .......................................................................................................... 125 CHAPTER 6 General Discussion ..................................................................................................... 129 REFERENCES ............................................................................................................ 136 APPENDICES APPENDIX I: ............................................................................................................ 157 Chapter 2 Supplementary Materials ..................................................................... 157 APPENDIX II: ........................................................................................................... 158 Chapter 3 Supplementary Materials ..................................................................... 158 APPENDIX III: .......................................................................................................... 161 Chapter 4 Supplementary Materials ..................................................................... 161 APPENDIX IV: ......................................................................................................... 165 Chapter 5 Supplementary Materials ..................................................................... 165 4 List of Figures Figure 2.1 Global distribution data of the Mediterranean fruit fly Ceratitis capitata used to build the MaxEnt models. .............................................................................................. 31 Figure 2.2 The Receiver Operating Characteristics curve (ROC) for training data of medfly with the area under the ROC curve (AUC). ................................................................... 33 Figure 2.3 Potential distribution for Medfly. ................................................................... 35 Figure 2.4 Potential distribution for Medfly at worldwide scale and regional scale under two RCP emissions scenarios for the future climate conditions for 2050. ..................... 37 Figure 2.5 Potential distribution for Medfly at worldwide scale and regional scale under two RCP emissions scenarios for the future climate conditions for 2070………………..39 Figure 3.1 Median-joining network of the Mediterranean fruit fly ................................... 58 Figure 3.2 Distribution of COI haplotypes across the study area for Ceratitis capitata. 61 Figure 3.3 Bayesian skyline plot (BSP) estimate of Medfly demographic history for the biogeographic regions ................................................................................................... 65 Figure 3.4 Values of theta and migration rates between the biogeographical regions. 67 Figure 3.5 Hypothesised historical migration paths worldwide of C. capitata using a molecular rate of 4.2% .................................................................................................. 68 Figure 4.1 Cumulative number of arthropod species reported insecticide resistance through time .................................................................................................................. 78 5 Figure 4.2 Molecular map of the Ache gene of medfly. ................................................. 80 Figure 4.3 Diagram representing the genetic variants described in Ccace gene. ......... 81 Figure 4.4 Map of study areas in Colombia. .................................................................. 86 Figure 4.5 Alignment of Ccace2 fragments gene and their respective genomic mapping to C. capitata.