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Evolutionary Studies of Dawson's Burrowing

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Evolutionary Studies of Dawson's Burrowing MOLECULAR ECOLOGY OF DAWSON’S BURROWING BEE Amegilla dawsoni (HYMENOPTERA: ANTHOPHORINI) Maxine Beveridge (BSc Hons. PG Dip.) School of Animal Biology The University of Western Australia This thesis is presented for the degree of Master of Science Of The University of Western Australia 2006. SUMMARY In the last two decades, the use of microsatellites has revolutionized the study of ecology and evolution. Microsatellites, or short tandem repeats (STRs), are stretches of DNA repeats, 1 to 5 nucleotides long, where the number of repeats varies between individuals. They are co-dominant, highly variable, neutral markers, and are inherited in a Mendelian fashion. Microsatellite loci were isolated from Dawson's burrowing bee, Amegilla dawsoni, a large, fast-flying solitary nesting bee endemic to the arid zone of Western Australia. Twelve polymorphic loci were found with an observed number of alleles ranging from two to 24 and observed heterozygosities between 0.17 and 0.85. These loci were used to examine two aspects of this bee’s molecular ecology; its population structure and mating system. The population structure of Dawson’s burrowing bee was examined using the 8 most variable microsatellite loci. Adult female bees were collected from 13 populations across the species range. The mean number of alleles per locus ranged from 4 to 38 and expected heterozygosity was uniformly high with a mean of 0.602. Pairwise comparisons of FST among all 13 populations ranged from 0.0071 to 0.0122 with only one significant estimate and an overall FST of 0.001. The entire sample collection was in Hardy-Weinberg equilibrium and there was no evidence of inbreeding with a mean FIS of 0.010. The mating and nesting behaviour of this bee suggests that gene flow would be limited by monandry and the fact that almost 90% of females mate immediately on emergence. Nevertheless there is obviously sufficient gene flow to maintain panmixia and I suggest that this results from infrequent and unreliable rainfall in the species range, which causes the bees to congregate at limited food resources, allowing a small number of unmated females from one emergence site to come into contact with males from another population. In addition, when drought eliminates food resources near an emergence site, the whole population may move elsewhere, increasing gene flow across the species range. From behavioural data and observations, Dawson’s burrowing bee appears to be monandrous. The same microsatellite markers were used to analyse the genotypes of offspring from individual nests to determine the number of effective mates for each female. From these data it was determined that females almost certainly mate only once, which is consistent with male reproductive tactics that include protandry and intense male-male competition for access to virgin females. The molecular data were i also used to show that the nesting female is the mother of all her offspring and that brood parasitism is unlikely in this species. The data indicate that females make daughters at the beginning of the season followed by large sons in the middle, and then small sons at the end. Females often place one brood cell directly above another. The distribution of sex and morph in these doublets follows a pattern with most containing a female on the bottom and a minor male on the top, followed by almost equal numbers of female on top of female and minor male on top of major male. This pattern is likely favoured by emergence patterns, with males emerging before females and minor males emerging before major males. I suggest that although minor males have low reproductive success, their production may nonetheless be beneficial in that minor males open up emergence tunnels for their larger and reproductively more valuable siblings. In addition, minor males may represent the ‘best of a bad job’ provisioning tactic arising from changes in the costs to nesting females of gathering brood provisions over the course of the flight season. This thesis demonstrates that microsatellites can be used to answer many questions regarding the molecular ecology of a species from the behaviour of the bees on a population scale to the mating behaviour of individual bees and how they allocate resources for the next generation. Many other aspects of the bee’s ecology could also be examined now that suitable molecular markers exist. ii TABLE OF CONTENTS SUMMARY i TABLE OF CONTENTS iii ACKNOWLEDGEMENTS v PUBLICATIONS vi CHAPTER 1: General Introduction 1.1. Molecular markers and their applications 2 1.2. Dawson’s burrowing bee – a natural history 3 1.3. Population genetics of Dawson’s burrowing bee 4 1.4. Genetic breeding system of Dawson’s burrowing bee 5 1.5. References 5 CHAPTER 2: Development of microsatellite loci for Dawson's burrowing bee (Amegilla dawsoni) and their cross-utility in other Amegilla species. 2.1. Abstract 10 2.2. Introduction 11 2.3. Materials and methods 11 2.4. Results and discussion 12 2.5. References 13 CHAPTER 3: Panmixia: an example from Dawson’s burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini) 3.1 Abstract 18 3.2 Introduction 19 3.3 Materials and methods 20 3.4 Results 22 3.5 Discussion 23 3.6 References 26 iii CHAPTER 4: Genetic breeding system and investment patterns within nests of Dawson's burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini) 4.1. Abstract 34 4.2. Introduction 35 4.3. Materials and methods 37 4.4. Results 40 4.5. Discussion 44 4.6. References 46 CHAPTER 5: General Discussion 5.1. Microsatellites as a tool 57 5.2. Molecular markers of the future 58 5.3. References 60 iv ACKNOWLEDGEMENTS Firstly, I would like to thank Professor Leigh Simmons for his help, support and encouragement over the past 4 years. I would also like to thank Professor John Alcock and his wife Sue for making those field trips to Carnarvon and beyond so much fun. Thanks must also go to Charlotta Kvarnemo for helping in the onerous task of excavating bee nests. I must also thank Melissa Bell for supplying two species of bee, Amegilla holmesi and Amegilla bombiformis for microsatellite evaluation and Kings Park and Botanical Gardens for generously allowed access to their sequencer. In the School of Animal Biology, UWA, thanks must go to Jason Kennington for helping me wade through population genetics software packages and Mike Johnson for his comments on draft manuscripts. I must also thank Blair Parsons for producing Figure 3.1. I would also like to thank all the members of the Centre for Evolutionary Biology, in particular Dr Francisco García-González for all his help and support over the last 4 years and Renée Firman for keeping me entertained. Finally, I would like to thank Andrew for his unwavering support and love. v PUBLICATIONS This thesis is submitted as a series of discrete papers. The following papers are either published or in press. I. Beveridge, M. & Simmons, L. W. (2004) Microsatellite loci for Dawson's burrowing bee (Amegilla dawsoni) and their cross-utility in other Amegilla species. Molecular Ecology Notes 4, 379-381. II. Beveridge, M. & Simmons, L. W. (2006) Panmixia: an example from Dawson's burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini). Molecular Ecology 15, 951-957. III. Beveridge, M., Simmons, L. W. & Alcock, J. (2006) Genetic breeding system and investment patterns within nests of Dawson's burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini). Molecular Ecology in press. The first two papers were written in collaboration with Leigh Simmons and the third with the addition of John Alcock. In all papers, I was responsible for the experimental design, data collection, analysis of results and writing. Leigh Simmons contributed to the experimental design, analysis of results and writing. John Alcock contributed to the experimental design and writing. I was the main contributor in each paper (estimated as % contribution: I, MB = 95%, LWS = 5%; II, MB = 75%, LWS = 25%; III, MB = 75%, LWS = 20%, JA = 5%) vi CHAPTER 1 GENERAL INTRODUCTION 1 1.1 Molecular markers and their applications Over the last two decades, molecular markers have become invaluable in answering the questions raised by ecological and evolutionary studies (Rosenbaum & Deinard 1998). Several markers have been utilised including allozymes, restriction fragment length polymorphisms (RFLPs), multi-locus and single-locus minisatellites, and randomly amplified polymorphic DNA (RAPDs) (Queller et al. 1993). However, each of these methods has disadvantages and they have largely been superseded by microsatellites. These are highly variable, neutral, co-dominant markers inherited in a Mendelian fashion (Jarne & Lagoda 1996). They consist of stretches of DNA repeats, 1 to 5 nucleotides long, where the number of repeats varies between individuals. This variability is so high that when using several microsatellite loci, even closely related organisms can be individually identified. Since their introduction, microsatellites have been used in a wide range of applications, the first of which is in behavioural ecology. Male mating success was traditionally estimated by behavioural observations in the field but this has obvious limitations. In their study of pilot whales, Amos et al. (1993) used microsatellites to uncover a completely novel mating system which could not have been discovered by observation alone. There has been a long held view that the majority of bird species were monogamous but molecular markers have shown that 86% of passerine bird species show extra-pair paternity (Griffiths et al. 2002). Statistical techniques have also improved to the point where the number of potential fathers for a set of offspring can be estimated without their putative fathers’ genotypes being sampled (Bretman & Tregenza 2005). In the field of evolutionary biology, microsatellites continue to be an invaluable tool for analysing the current questions such as why females mate polyandrously (Simmons 2005).
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