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Mechanisms of Space Use in the Wood Mouse, Apodemus Sylvaticus

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Mechanisms of Space Use in the Wood Mouse, Apodemus Sylvaticus Mechanisms of space use in the wood mouse, Apodemus sylvaticus Benedict John Godsall 2015 Imperial College London Faculty of Natural Sciences Division of Biology A thesis submitted for the degree of Doctor of Philosophy Author's declaration I declare that this thesis is my own work and that all else is appropriately referenced. Copyright Declaration The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution Non-Commercial No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or redistribution, researchers must make clear to others the licence terms of this work. 1 Abstract "Space use” describes a wide set of movement behaviours that animals display to acquire the resources necessary for their survival and reproductive success. Studies across taxa commonly focus on the relationships between space use and individual-, habitat- and population-level factors. There is growing evidence, however, that variation in space use between individuals can also occur due to differences in 'personalities' and genetic variation between individuals. Using a wild population of the European wood mouse, Apodemus sylvaticus, this thesis aims to: i) investigate the roles of individual-level (body mass, body fat reserves and testosterone), habitat-level (Rhododendron and logs) and population-level (population density, sex ratio and season) factors as drivers of individual variation in the emergent space use patterns of individual home range size and home range overlap, estimated using spatial data collected in a mixed-deciduous woodland over three years. ii) Establish a link between genes and space use through the heritability and response to selection of phenotypic traits linked to individual variation in space use. A pedigree of the population is reconstructed from microsatellite data. Individual reproductive success is estimated from it and used to estimate selection gradients for three phenotypic traits. Heritability estimates are calculated using the animal model and together with selection gradients are used to predict the generational change in the population mean of traits using the Breeders equation. The results of this thesis suggest that the mechanism behind space use in this population of A. sylvaticus involves interactions between season, habitat, sex and the three individual-level factors (body mass, body fat and testosterone). The heritability of traits linked to emergent space use patterns suggests indirect effects of genes on individual variation in space use. Small responses to selection for traits suggests that gene-driven changes to space use patterns will most likely be indistinguishable between generations. 2 Acknowledgements First and foremost I would like to express my special thanks to my supervisors, Prof. Timothy Coulson and Dr. Aurelio Malo. I am very grateful, and feel privileged to have had the opportunity to work with and be mentored by both of them. The support and encouragement Tim and Aurelio provided throughout my thesis was invaluable. I have enjoyed being a part of the relaxed environment of the Coulson group, and it has been a real honour to be Dr. Malo's first PhD student. Severin Dreβen, a fellow PhD student, deserves special thanks for his hard work and efficiency in helping collect data during long days in the field, developing the GIS map of the study site, and introducing me to DTT. I am also extremely grateful to Jacques Deere and his wife Sam Hopkins, who showed me an abundance of generosity by giving me a hot meal, a warm bed and good company on the evenings preceding fieldwork. I thank all of the Masters students who worked for the project over the years for their efforts in data collection: C. Weevil, S. McCandless, T. Powell, G. Kingcome, M. Brouard, R. Moorhouse-Gann, O. Hicks, L. Sandbach, R. Barker, S. McLoughlin. A special thanks also goes to Michael Massam for his hard work as a volunteer. The genetic elements of this thesis would not have been possible without the help of Martyn Powell, who taught me how to extract DNA, and especially Helen Hipperson, who gave a lot of her time to patiently instruct me how to perform PCRs with microsatellites. Most of the genetic work was performed at the NERC Biomolecular Facility at Sheffield University. I would like to thank Prof. Terry Burke for giving me the opportunity and funding to work in his group and provide advice on pedigree reconstruction. Deborah Dawson, Andy Krupa and Gavin Horsburgh were exceptionally helpful in providing instruction and advice throughout my time in the lab, and I am extremely grateful to them for their help. 3 Mike Francis of Francis Scientific Instruments Ltd. built the pit-tag recording stations used to collect the spatial data in this thesis. The volume and quality of data collected during this project could not have been achieved without his support. I would also like to thank Igor Lysenko for his assistance in originally developing the digital map of the study site in GIS. Finally, but by no means least, I would like to say a huge thank you to Helen Meredith for her understanding, patience and support throughout the last 5 years, which at times must have required a lot of energy to maintain. 4 Table of contents Chapter 1: An overview of animal space use 13 Introduction 13 The importance of understanding rodent space use 14 Quantifying space use: the 'home range' concept 16 Drivers of space use 18 Habitat and resource distribution 20 The state of the individual 21 Population density, sex ratio and interspecific competition 26 Genes and space use 28 Study species: the European wood mouse, Apodemus sylvaticus (L.) 32 Study site 33 Spatial data collection 36 Aims and outline of thesis 38 Chapter 2: From physiology to space use: energy reserves and androgenisation explain home range size variation in Apodemus sylvaticus 41 Introduction 41 Methods 45 Study site 45 Trapping effort 45 Recording stations 46 Seasonal variation 47 5 Home range estimation 48 Habitat data 49 Statistical analysis 51 Results 52 Individual-level and habitat factors 53 Anogenital distance 56 Discussion 58 Chapter 3: Habitat interacts with phenotypic traits to determine home range overlap 64 Introduction 64 Methods 68 Data collection 68 Home range and overlap estimation 70 Statistical analysis 72 Home range overlap and season, dyad type and habitat 73 Intrasexual home range overlap and individual-level factors 74 Intersexual home range overlap and individual-level factors 76 Caveat for statistical analyses 76 Results 77 Home range overlap and season, dyad type and habitat 77 Intrasexual home range overlap and individual-level factors 79 Intersexual home range overlap and individual-level factors 81 Discussion 81 6 Chapter 4: Drivers of reproductive success, polygamy and the annual cycle of relatedness in the wood mouse 86 Introduction 86 Methods 89 Data collection 89 Tissue collection 90 DNA extraction 90 Genotyping 91 Pedigree reconstruction 95 Temporal variation in mean relatedness and the number of reproductive mates 96 Individual reproductive success, phenotypic traits and space use 98 Model simplification and significance tests 101 Results 103 Temporal variation in mean relatedness and the number of reproductive mates 103 Individual reproductive success, phenotypic traits and space use 105 Discussion 107 7 Chapter 5: Selection gradients, heritability and the response to selection of three phenotypic traits in the wood mouse, Apodemus sylvaticus 112 Introduction 112 Methods 116 Data collection and preparation 116 Selection 117 Heritability 119 Response to selection 120 Results 121 Selection 121 Heritability 125 Response to selection 126 Discussion 127 Chapter 6: Conclusions 133 Summary of findings 133 Limitations of the study 136 Conclusions 137 References 140 Appendix 170 Appendix I: Justification of body fat scoring system 170 Appendix II: Accounting for behaviour within recording stations 172 8 List of figures Chapter 1 Figure 1.1: Map of the study site showing microhabitat features. 34 Figure 1.2: A) Exterior view of a recording station. B) The inside of a recording station. C) The study site divided into regions, one per recording station. 37 Chapter 2 Figure 2.1: Example of male and female home ranges at the study site, showing delineation of home range core and periphery. 50 Figure 2.2: Core home range size and A) the interaction between body fat and sex, B) the interaction between body mass and sex. 54 Figure 2.3: Effect of androgenisation on home range core and periphery sizes. 57 Chapter 3 Figure 3.1: Example of different degrees of home range overlap using the UDOI metric. 71 Figure 3.2: Home range overlap during the breeding season for male-male, male-female and female-female overlapping dyads. 78 9 Figure 3.3: LMM-predicted relationships between home range overlap and the difference in body fat, during the breeding season: A) overlapping females in low quality habitat (open woodland); B) overlapping males in areas of high quality (Rhododendron cover). 79 Figure 3.4: A) LMM-predicted relationship between male-male overlap during the breeding season and the difference in AGDI in areas of low predation-risk (high shrub cover). B) LMM-predicted relationship between male-female overlap during the breeding season and male AGDI. 80 Chapter 4 Figure 4.1: Monthly mean relatedness, population density, offspring recruitment and immigration between January 2009 and March 2013. 102 Figure 4.2: Mean number of reproductive partners between years. 104 Figure 4.3: Mean of reproductive success between years. 106 Chapter 5 Figure 5.1: Relationships between population density and selection gradient estimates for body mass, foot length and AGDI during breeding seasons. 123 Figure 5.2: Relationships between sex ratio and selection gradient estimates for body mass, foot length and AGDI during breeding seasons.
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