Sex Ratio Strategies in the Facultatively Autoparasitic Wasp, Encarsia tricolor Forster. By TREVOR WILLIAMS A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Imperial College of Science, Technology and Medicine Department of Pure and Applied Biology Imperial College Field Station Silwood Park Ascot April 1989 Berkshire -2- ABSTRACT IA Heteronomous hypeiparasitoids are a group of aphelinid parasitoidsAwhich the sexes show different host relations. Females always develop as primary endoparasitoids of Homoptera. Male development is different and has been used to classify the group under three headings: a : obligate autoparasitoids - males develop hyperparasitically only on immature female conspedfics b: facultative autoparasitoids - males develop as hypeiparasitoids of primary endoparasitoids including consperific females c: alloparasitoids - males develop only as hyperparasitoids of non-conspecific primary endopa­ rasitoids. This study set out to explore the adaptive significance of heteronomous hyperparasitism and the effects that such remarkable host relations, have on the sex ratio and population dynamics of these parasitoids. Encarsia tricolor Fflrster, a facultative autoparasitoid native to the UK, was selected for study. Initially the biology of this spedes was investigated using a typical primary host, the Cabbage Whitefly, Aleyrodes proletella. E. tricolor was long-lived, had a low fecundity and could successfully parasitise all primary (female eggs) and secondary (male eggs) host instars. When all primary host stages were offered, larger hosts were preferentially parasitised, but all whitefly stages were used for host feeding. Factors affecting the wasp’s ovipositional decisions were investigated further. Encarsia inaron (Walker), a conventional bisexual endoparasitoid, was used throughout the study as a non-conspecific secondary host for the hyperparasiticE. tricolor males. Preferential exploitation of E. inaron rather than conspedfic E. tricolor, was shown in laboratory choice experiments. This ovipositional preference was a critical factor in illustrating the selective advantage to heteronomous hyperparasitism, and strongly influenced the sex ratio and the outcome of inter-spedfic competition between the conventional parasitoid and Encarsia tricolor. In practical terms, such preferences should also modify the use of heteronomous hyperparasitoids for biological control. Field studies supported the lab-findings of preferential hyperparasitism of E. inaron over con­ spedfics. E. tricolor and E. inaron occurred together in patches significantly more often than expected given random assodation. E. tricolor male production was more common in large parasitised patches of both spedes than in smaller patches. In the absence of alternative male hosts, a heteronomous hyperparasitoid must resort to hyper- parasitism of conspedfics (autoparasitism), to which she may be related Evidence is presented to show that when offered patches of different ratios of parasitised and unparasitised hosts for the production of males and females respectively, E. tricolor sex ratio was not influenced by the availability of each host type. Prior ovipositional experience however, was found to be important in affecting the sex ratio of these wasps. Four types of experience were offered: a: none b: laying male eggs in E. tricolor pupae c: laying female eggs in whitefly nymphs d: laying male eggs in E. inaron pupae Wasps exposed to the first two treatments produced unbiased mean sex ratios. Wasps given the third treatment laid a significantly female biased sex ratio. After exposure to E. inaron pupae (and then offered different ratios ofE. inaron and whitefly) a significantly male biased sex ratio was produced. The adaptive significance of such sex ratios are discussed. Caged competition experiments between these two species showed the heteronomous hyper­ parasitoid to have a remarkable competitive ability, and completely displaced large populations of the normally-reproducingE. inaron. E. inaron however, could not manage significant levels of reproduction in a culture cage containing an established population of E. tricolor. Finally, modifications to the classification of heteronomous hyperparasitoids are proposed which removed the strict divisions by which the group was previously recognised In place, a more ecologically realistic viewpoint is recommended under which ovipositional preferences (commonly observed) are distinguished from physiological necessity (rare) and allow the whole group to be identified simply as "heteronomous hyperparasitoids". The evolutionary pathway of other heteronomous parasitoids is also discussed in the light of these findings. -3- ACKNOWLEDGEMENTS As is traditional at this point, I acknowledge with thanks the part played by my supervisor, Jeff Waage, for advice and guidance in the experimental work, and for his constructive criticism of my written ideas. Likewise, Charles Godffay was always willing to discuss sex ratio theory and has helped improve some of the chapters herein by his comments. I am very grateful to Zdenek Boucek and especially Andy Polaszek of the CAB International Institute of Entomology who both helped me with parasitoid identifications. I seem to recall that Mark Rees gave advice on GLIM analysis on more than one occasion. My parents supported me in many ways. Financial assistance came in the form of a NERC Studentship. Finally, I would like to thank deeply my friends at Silwood for making my stay there what it was. I shall miss them all. -4- TABLE OF CONTENTS Page Abstract 2 Acknowledgements 3 Table of Contents 4 List of Figures 7 List of Tables 8 Chapter 1: SEX RATIO THEORY 9 1.1 When mating is random 9 1.2 Structured populations 11 1.2.1 Local mate competition 11 1.2.2 Sibling interaction 12 1.2.3 Haystack models 13 13 Changing fitness 13 13.1 Host quality 14 13.2 Seasonality 15 1.4 Asymmetry of relatedness 15 1.5 Sex ratio diseases 15 1.6 Testing the theory 16 1.7 Summary 19 Chapter 2: INTRODUCTION TO HETERONOMOUS HYPERPARASITOIDS 20 2.1 What are heteronomous hyperparasitoids? 20 2.2 Sex ratio and population dynamics in autoparasitoids 24 2 3 Introduction toE. tricolor 28 2.4 Aims of the study 28 Chapter 3: MATERIALS AND METHODS 29 3.1 Collection of whitefly and parasitoids 29 3.2 Whitefly and parasitoid cultures 29 3 3 Clip cage experiments 30 3.4 Data collection 31 Chapter 4: BIOLOGY OF ENCARSIA TRICOLOR 36 4.1 Introduction 36 4.2 Biological characteristics of Encarsia tricolor 41 4.2.1 Longevity 41 4.2.2 Instar acceptability for female eggs and female 45 development time 4.23 Instar acceptability for male eggs and male 48 development time 4.2.4 Fecundity 49 4.2.5 Culture sex ratio 50 -5- 4.2.5.1 Sex ratio dynamics on individual leaves as a function of their 52 period of exposure to parasitism 4.2.5.2 Sex ratio dynamics in the culture cage as a function o f the age 52 of the culture 4.2.6 Oviposition time 54 43 Summary 60 Chapters: SPECIES DISCRIMINATION AND KIN RECOGNITION 62 5.1 Species discrimination 62 5.2 Kin recogition 65 53 Summary 68 Chapter 6: HOST AVAILABILITY AND SEX RATIO IN E. TRICOLOR 69 6.1 Introduction 69 6 2 Methodology 71 63 Statistical analysis 72 6.4 Results 73 6.5 Discussion 77 Chapter 7: INTERSPECIFIC COMPETITION 81 7.1 Introduction 81 7.2 Methodology 82 73 Results 83 7.4 Discussion 88 7.4.1 Some classic examples of competition in biological control 89 7.4.2 Competition involving heteronomous hyperparasitoids 90 7 .4 3 Parasitoid complexes containing a heteronomous hypeiparasitoid 94 Chapter 8: FIELDWORK 101 8.1 Methodology 101 8.1.1 Honeysuckle: 1986-1987 102 8.1.2 Brussels Sprout: 1987 102 8.13 Brussels Sprout: 1988 103 8.2 Results 105 8.2.1 Honeysuckle: 1986-1987 105 8.2.2 Brussels Sprout: 1987 105 8.23 Brussels Sprout: 1988 112 8.23a parasitism on the lab-treated plants 112 8.23b parasitism within the Brussels crop 112 8 3 Discussion 115 - 6 - Chapter 9: DISCUSSION 118 9.1 Decision making during opposition 118 9.2 Host selection and sex ratio 119 93 Autoparasitoid classification 122 9.4 Biological control 124 9.5 The evolution of heteronomous hyperparasitism 127 9.6 Conclusions 130 Chapter 10: SUMMARY 133 References 136 Appendix 1: Aphelinid fecundities from the literature 152 - 7 - LIST OF FIGURES Number Title Page 1.1 The observed sex ratio changes for four fig wasp species and Nasjtnia 17 vitripennis 2.1 Diagramatic form of heteronomous parasitoid classification 22 Photographs: Clip cage (side view) 32 Clip cage (from beneath) 32 Several clip cages set up on the same plant 33 Culture cages in the 25°C room 33 E. tricolor parasitising whitefly nymphs 34 E. inarort parasitising whitefly nymphs 34 Parasitised and unparasitised whitefly on Brussels leaf 35 Emergence cases of whitefly and E. tricolor 35 4.1- 4.2 Regression of parasitoid longevity on size for both sexes E.of tricolor 43 43 Pattern of mortality for both sexes ofE. tricolor over the duration of the 44 longevity experiment 4.4 Pattern of emergence of female E. tricolor from each host instar 47 4.5 Fecundity ofE. tricolor when laying female eggs in unparasitised hosts 51 over the lifetime of the wasp 4.6-4.9 Emergence of both sexes ofE. tricolor from samples taken from plants 53 exposed to parasitism for 14-35 days 4.10 Mean percentage parasitism of whitefly on individual leaves after 55 different periods of exposure to parasitism 4.11 Overall sex ratio of E. tricolor emerging from leaves sampled following 55 different periods of exposure to parasitism 4.12 Predicted flucuations in culture sex ratio over the period of the formal 56 sampling regime 6.1- 6.4 Scatter plots of sex ratios laid following four types of prior ovipositional 74-75 experience 6.5 Mean sex ratio (with 95% CL) laid following four types of ovipositional 76 experience 6.6 Mean number of hosts parasitised (with 95% CL) following each type of 76 ovipositional experience 7.1a-7.4a Mean percentage parasitism in each sample from competition 84-87 experiment: cages 1-4 7.1b-7.4b Changes in the number of E.