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Transmission of Chemosensory Information in Drosophila Melanogaster: Behavioural Modification and Evolution

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Transmission of Chemosensory Information in Drosophila Melanogaster: Behavioural Modification and Evolution Transmission of chemosensory information in Drosophila melanogaster: Behavioural modification and evolution A thesis submitted to The University of Manchester for the degree of Doctor of Philosophy in Evolutionary Biology in the School of Life Sciences 2014 Rebecca Lockyer Contents ________________________________________ List of Figures……………………………………………………………………………….8 List of Tables……………………………………………………………………………....13 Abstract………………………………………………………………………………….…14 Declaration & Copyright Statement……………………………………………………..15 Acknowledgements…………………………………………………………………….…17 Glossary of Terms……………………………………………………………………...…18 Chapter 1 – Introduction 20 ___________________________________________________________________ 1.1. Introduction……………………………………………….………………….20 1.2. Transmission of information across generations………………………...21 1.3. Social transmission of information………………………………………...24 1.3.1. Social transmission and oviposition behaviour………………..25 1.3.2. The apple maggot fly…………………………………………….28 1.4. Plasticity and its significance……………………………………………....29 1.5. Genomic imprinting and epigenetics………………………………………32 2 1.6. Olfactory plasticity…………………………………………………………..34 1.7. Factors influencing olfactory plasticity.……………………………………36 1.8. Drosophila as a model……………………………………………………...43 1.9. Drosophila larval olfaction……………………………………………….....44 1.10. Drosophila adult olfaction………………………………………………....46 1.11. OrCo (previously Or83b)………………………………………………….50 1.12. Drosophila nociception…………………………………………………....52 1.12.1. Trp mutants……………………………………………………...52 1.12.2. Painless mutants…………………………………………….….55 1.13. Drosophila larval gustation………………………………………………..56 1.14. Drosophila adult gustation………………………………………………..62 1.15. Chemosensory processing and oviposition behaviour..…………….…64 1.16. Measuring responses to chemostimulants……………………………...66 1.17. Drosophila courtship and mating……………………………..................70 1.18. Aims and objectives……………………………………………………….72 Chapter 2 – Materials and Methods 76 __________________________________________________________________ 2.1. Fly stocks…………………………………………………………………….76 2.2. Chemostimulants…………………………………………………………....77 2.3. Rearing peppermint- and menthol-exposed flies………………………...78 3 2.3.1. P1 and M1: Flies reared in one generation in peppermint (P1) or menthol (M1)………………………………………………………….78 2.3.2. P2: Flies reared on 0.1% peppermint medium for two generations………………………………………………………………78 2.3.3. P1C1: Control food-reared flies, the offspring of flies reared on 0.1% peppermint medium………………………………………………79 2.3.4. P1C2: Control food-reared second generation offspring reared on 0.1% peppermint medium………………………………….............79 2.4. Larval behaviour: Rearing………………………………………………....82 2.5. Larval behaviour: Olfaction……………………………………………..…83 2.6. Adult behaviour: Gustation……………………………………………...…85 2.7. Adult behaviour: Settling (assessment of host-selection behaviour)….87 2.8. Adult behaviour: Oviposition...……………………………………………..88 2.9. ‘No contact’ rearing………………………………………………………….89 2.10. Impact of peppermint on survival to adulthood…………………………90 2.11. Analysis of data…………………………………………………………….91 Chapter 3 – Results: Do rearing conditions influence behaviour? 92 ___________________________________________________________________ 3.1. Introduction…………………………………………………………………..92 3.2. Responses of control larvae to peppermint………………………………94 4 3.3. Settling behaviour in control adults………………………………………..99 3.4. Experiments on larvae reared on peppermint food………………….…102 3.5. Settling behaviour in P1 adults…………………………………………...106 3.6. P1 oviposition behaviour………………………………………………….108 3.7. Mating trials……………………………………………………………...…110 3.8. Chapter summary………………………………………………………….112 Chapter 4 – Results: Exploring the effects of environment and rearing conditions on chemosensory behaviours 114 ___________________________________________________________________ 4.1. Introduction…………………………………………………………….….114 4.2. Necessity of contact…………………………………………………….…115 4.3. The behaviour of individual larvae……………………………………….120 4.4. Effect of rearing conditions on behaviour…………………………….…122 4.5. Effect of peppermint on juvenile survival……………………………..…126 4.6. Chapter Summary…………………………………………………………129 Chapter 5 – Results: Influence over generations 132 ___________________________________________________________________ 5.1. Introduction…………………………………………………………………132 5 5.2. Influence of repeated generational exposure…………………………..133 5.3. Effects of exposure to peppermint for a single generation...………….141 5.4. Influence of re-exposure to peppermint…………………………………153 5.5. Chapter summary.…………………………………………………………155 Chapter 6 – Results: Investigation into underlying causes 157 ___________________________________________________________________ 6.1. Introduction…………………………………………………………………157 6.2. Parental inheritance……………………………………………………….158 6.3. The responses of peripheral receptor mutants…………………………164 6.4. Testing the chemical legacy hypothesis………………………………...173 6.5. Male only and female only assays……………………………………….175 6.6. Menthol assays…………………………………………………………….177 6.7. Chapter Summary…………………………………………………………180 Chapter 7 – Discussion 182 ___________________________________________________________________ 7.1. Overview……………………………………………………………………182 6 7.2. Naïve flies find peppermint repellent, but rearing in its presence reduces this aversion……………………………………………………………………..183 7.3. Parental and larval environments influence behaviour………………..185 7.4. Direct contact with peppermint is not required for behavioural changes to occur…………………………………………………………………………..187 7.5. Impact of peppermint upon survival.…………………………………….189 7.6. Repeated exposure to peppermint for several generations may result in a preference for it……………………………………………………………….191 7.7. Transgenerational effects of exposure to peppermint…………………194 7.8. Transmission of preference across life stages…………………………196 7.9. Input from both parents is used to modify offspring behaviour……….198 7.10. Chemosensory mutants do not find peppermint aversive……………201 7.11. Menthol and peppermint evoke similar behavioural responses……..202 7.12. Comparison of single sex and mixed sex settling assays……………203 7.13. Further work………………………………………………………………204 7.14. Overall conclusions………………………………………………………206 References 208 ___________________________________________________________________ Word count =49, 784 7 List of Figures . Figure 1.1 Schematic of a typical olfactory sensillum housing two OSN’s…41 . Figure 1.2 Anatomy of the dorsal organ in Drosophila melanogaster larvae………………………………………………………………………………45 . Figure 1.3 Scanning electron micrograph of a fly head, indicating the major chemosensory organs…………………………………………………………...46 . Figure 1.4 Scanning electron micrograph of the head of an adult Drosophila melanogaster female with a surface-rendered 3-D reconstruction of the brain………………………………………………………………………………..48 . Figure 1.5 Comparative circuitry of the adult and larval olfactory systems..49 . Figure 1.6 Anatomical placement of Do and TO on the larval head………..59 . Figure 1.7 Immunofluorescence stain of the fly brain indicates the location of the AL and SOG in respect to one another, as well as indicating OSNs ….61 . Figure 1.8 Schematic indicating the position of olfactory and gustatory neurons on the body of the fly…………………………………………….........62 . Figure 1.9 Locomotor behaviours involved in the olfactory response of Drosophila melanogaster larvae………………………………………………..67 . Figure 1.10 Courtship behaviour of Drosophila melanogaster ……………..71 . Figure 2.1 Rearing of peppermint (P1) flies………………………………...…80 . Figure 2.2: Rearing of P2 flies…………………………………………………..80 . Figure 2.3: Rearing of P1C1 flies……………………………………………….81 . Figure 2.4: Rearing of P1C2 flies……………………………………………….81 . Figure 2.5: Olfactory behavioural test plate……………………………………83 . Figure 2.6: Gustatory behavioural test plate………………………………….86 8 . Figure 2.7: Location of oviposition sites within a laying box………………...89 . Figure 3.1: Olfactory behavioural response indices for second instar control CS larvae in response to increasing concentrations of peppermint ….…….95 . Figure 3.2: Gustatory behavioural response indices for second instar control CS larvae when presented with a choice between control agar and 0.1% peppermint agar, or a choice between control agar and 1% peppermint agar………………………………………………………………………………..97 . Figure 3.3: Gustatory behavioural response indices for second instar control CS and OrCo- larvae when presented with a choice between control agar and 0.1% peppermint agar, or a choice between control agar and 1% peppermint agar…………………………………………………………………..98 . Figure 3.4: Behavioural assay of adult settling behaviour in control CS flies……………………………………………………………………………….100 . Figure 3.5: Olfactory behavioural response indices for second instar control and P1 larval offspring………………………………………………………….103 . Figure 3.6: Gustatory behavioural response indices for second instar control CS and P1 larval offspring when presented with a choice between control agar and 0.1% peppermint agar, or a choice between control agar and 1% peppermint agar…………………………………………………………………105 . Figure 3.7: Behavioural assay of settling behaviour using P1 flies in the presence of control food and 0.1% peppermint food………………………..107 . Figure 3.8: Oviposition behaviour for control flies and P1 flies when presented with 3 choices – control agar, 0.05% peppermint agar, and 0.1% peppermint agar………………………………………………………………...108 . Figure 3.9: CC = C♀C♂ mating pair; CP = C♀P1♂ mating pair; PC = P1♀C♂ mating pair; PP = P1♀P1♂ log courtship duration, log
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