Mimicry and the hoverflies By Salma Azmeh, BSc (Hons) Thesis submitted to the University of Nottingham for the degree of Doctor of Philosophy, October 1999 Table of Contents Chapter One: General review of mimicry with reference to hoverflies 1.1Introduction 1 1.2Aposematism 8 1.2.1 The evolution of aposematism 8 1.2.2 Are hoverflies distasteful? 13 1.2.3 Aposematism for other types of unprofitability 16 1.2.3.1 Examples of aposematism not for distastefulness 16 1.2.3.2 Are hoverflies advertising their unprofitability? 18 1.3Abundance of models and mimics 20 1.3.1 Frequency-dependence in mimicry 20 1.3.2 Synchrony in time and space 24 1.3.3 Frequency patterns in hoverflies and their models 26 1.4 Colourpatterns in mimicry 30 1.4.1 Evolution and genetics of mimetic patterns 30 1.4.1.1 The evolution of mimicry 30 1.4.1.2 The two-step system 32 1.4.1.3 Supergenes and linkage 33 1.4.2 Perfect and imperfect mimicry 35 1.4.2.1 Why perfect mimicry? 35 1.4.2.2 Perfect mimicry via imperfect mimicry 36 1.4.2.3 The coevolutionary chase 38 1.4.2.4 Evidence of protection by imperfect mimicry 40 1.4.3 Predator perception 44 1.4.3.1 Predator perception and imperfect mimicry 44 1.4.3.2 Variation among predators 46 1.4.3.3 Do predators avoid innately or learn to avoid? 47 1.4.4 Polymorphism and diversity in mimicry 49 1.4.4.1 Polymorphism in Batesian and MUllerian mimicry 49 1.4.4.2 Geographical races in MUllerian mimicry 51 1.4.4.3 Polymorphism in MUllerian mimics 53 1.5Distastefulness and unprofitability 55 1.5.1 Relationships between unpalatability and avoidance 55 1.5.2 Automimicry 57 1.5.3 The palatability spectrum and its implications 60 1.5.3.1 The distinction between Mullerian and Batesian mimicry 60 1.5.3.2 Predator behaviour and mathematical models 61 1.5.4 Relationships between mimicry, unprofitability and flight morphology 64 1.5.4.1 Temperature and flight muscle 67 1.5.4.2 Body shape and its implications 68 1.5.4.3 Mimicry and flight morphology 70 1.5.4.4 Flight morphology in hoverflies 73 1.6Mimicry in hoverflies 74 Chapter Two: Abundance of Batesian mimics and their models in a suburban garden 2.1 Introduction 80 2.2 Methods 84 2.2.1 Hoverfly data 84 2.2.2 Data analysis 89 2.3 Results 89 2.3.1 Within year data 91 2.3.1.1. Relative proportions of hover fly types within years 91 2.3.1.2 Abundance of hover flies relative to wasps within years 92 2.3.1.3 Relative timing of hover flies and wasps within years 95 2.3.2 Among-year data 101 2.3.2.1 Wasps and wasp mimics 101 2.3.2.2 Bees and bee mimics 106 2.4 Discussion 113 Chapter Three: Reproductive characters and body size in hoverflies 3.1 Introduction 123 3.2Methods 127 3.2.1 Morphological data 127 3.2.2 Comparative method and statistical analysis 128 3.2.3 Phylogeny 131 3.3 Results 133 3.3.1 Is the evolution of body size related to changes in tongue length?133 3.3.2 Are body size changes related to changes in parameters of egg production? 135 3.3.3 Is body size related to parameters of sperm production? 141 3.4 Discussion 145 Chapter Four: Exploring the measurement of similarity 4.1 Introduction 151 4.2 How are the patterns compared? 154 4.2.1 How the image analysis technique works 154 4.2.2 The role of colour 158 4.2.3 The role of pattern distribution 160 4.3 Fine-tuning of the measurement of similarity 163 4.3.1 Allowing for different body sizes 163 4.3.2 Allowing for all-black tergites 165 4.4 Images used in the image analysis 174 4.4.1 Use of one model image 174 4.4.2 Other model species 176 4.4.3 Colour pattern groups 181 4.4.4 Discussion of images 182 4.5 Conclusions 184 Chapter Five: Testing the disturbed habitat hypothesis 5.1 Introduction 186 5.2Methods 190 5.2.1 Measuring similarity to wasps 190 5.2.2 New data on hoverfly abundance 192 5.2.3 Literature data 194 5.3 Results 200 5.4 Discussion 203 Chapter Six: Are hoverflies really mimics? 6.1 Introduction 206 6.2Methods 210 6.2.1 Morphological data 211 6.2.2 Measuring similarity to wasps 212 6.2.3 Comparative method and statistical analyses 213 6.2.4 Phylogeny 215 6.3 Results 217 6.3.1 Is there a positive relationship between the evolution of mimetic similarity and reproductive potential? 217 6.3.2 Is the evolution of'mimicry' associated with a reduction in reproductive potential? 218 6.4 Discussion 224 Chapter Seven: Are hoverflies really mimics?: Direct measurement of flight agility using centre-of-body-mass position 7.1 Introduction 231 7.2Methods 238 7.2.1 Measuring centre-of-body-mass position 239 7.2.2 Measuring similarity 240 7.2.3 Comparative method 242 7.2.4 Phylogeny 243 7.2.5 Statistical analysis 243 7.3 Results 246 7.4 Discussion 251 Conclusions 255 References 260 Appendix 1: Measurements of morphological characters A1-1 Appendix 2: Image analysis programs A2-1 BITMAP source code A2-2 A2-2 SHIFT source code A2-6 A2-3 SEGMENT source code A2-13 Acknowledgements lowe a great deal to many people who enabled this thesis to be completed. Firstly I would like to thank all those who helped me on my field trips, including Pavel Gorski, B. Jaroscziewicz, 1. Gotowski and especially Matthew Clarke in Poland, and Dr. Valeri Mutin, Marina Serednyakova, Professor V.N. Danjukov and Antony for an unforgettable time in Russia. Thanks also to NERC and the Carr Scholarship (Nottingham University) for funding the trips. Also of great help were Dr P. Ackery and N. Wyatt for access to specimens at the Natural History Museum (London), as well as Phil Bragg who handled the specimens and Brian Case who took photographs and allowed me many hours at his scanner. The Wollaton Natural History Museum gave me access to their collections to hone my hoverfly identification skills. Thanks also to those who allowed me to use their data and skills, especially Jennifer Owen for access to her huge dataset, Charles Ellington for advice on how to measure centre-of-body-mass, and Andy Purvis for information on the CAlC program. The phylogenies in this thesis were drawn using TreeView, available on the Internet at http://taxonomy.zoology.gla.ac.uk/rod/treeview.html. Most of all, thanks to colleagues, family and friends for their long- standing support and faith in me. Francis Gilbert always gave helpful and friendly advice, was inspirational, and let me think for myself. My parents and sister Hanne offered continual love and support and always believed in me. Antony Foubister gave limitless patience, tolerance, encouragement and washing-up services. Jane Wykes always listened, and kept my social life alive. Fiona Burford was unflinching in her support on the email. I thank Charlie Nevison for her friendship especially in 1998. All those in the Behaviour and Ecology Research Group at Nottingham in 1995-1998 deserve thanks for contributing to an excellent working and social atmosphere in those years (especially Tom Peake, Alex Gage, Ze Tavares, Sam Gray, Rosi Hare, the late Pete Smithurst and Chris Barnard). To Pete McGregor go special thanks for help in the first two years. Sarah Collins and Malcolm Edmunds provided valuable comments on this thesis. My studentship was provided by the NERC, without whom this work would not have been possible. Abstract Hoverflies (Diptera: Syrphidae) vary widely in their mimetic associations, comprising wasp-mimetic, bee-mimetic and non-mimetic species. Social wasp mimics are dominated by 'imperfect mimics' which outnumber their supposed models (Hymenoptera: Vespidae) by large factors. The purpose of this thesis is to determine to what degree Batesian mimicry can account for these paradoxes, and to test alternative hypotheses for the evolution of the yellow-and-black patterns. There is little evidence of an efTect of wasp abundance on 'imperfect mimic' abundance across 23 years of trapping data, as predicted if mimics are protected from predators through their resemblance to wasps. The seasonal asynchrony and high abundance of 'imperfect mimics' relative to their models is also notable, as well as the possible significance of wasp predation on hoverflies. Predictions concerning the function of the colour patterns of 'imperfect mimics' are tested using the association between similarity to the model and flight agility (indirectly measured assuming a trade-ofT between reproductive potential and flight agility). There is no strong indication that mimetic protection is the primary function of the colour patterns, but the evidence concurs with an aposematic function, signalling to predators the unprofitability of attempting capture. These conclusions are tentatively supported by direct measures of flight agility, though the small differences among species are difficult to pick up. The data on reproductive morphology of hover flies show .considerable variation across species, especially in males. The existence of giant testes in some species suggests that methods of dealing with sperm competition in hoverflies are diverse and deserve further study. The high ratio of 'imperfect mimics' to both models and good wasp mimics is also partly explained by habitat disturbance; undisturbed habitats show significantly less 'imperfect mimics' as a proportion of the hoverfly population.