The Spatial Ecology of Host Parasite Communities Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Shaun Patrick Keegan August 2019 TABLE OF CONTENTS TABLE OF CONTENTS ................................................................................................................. i ACKNOWLEDGMENTS .............................................................................................................. iii ABSTRACT ...................................................................................................................................... v 1 INTRODUCTION & LITERATURE REVIEW .................................................................. 7 1.1 Why space is important for epidemiology? .................................................................................................... 7 1.2 Spatial scale ............................................................................................................................................... 8 1.3 Transmission mode and the spatial clustering of infections ............................................................................ 9 1.4 Quantifying spatial clustering .................................................................................................................... 10 1.5 The application of network theory to epidemiology ...................................................................................... 11 1.6 Overview of study systems .......................................................................................................................... 12 1.7 Coinfection ............................................................................................................................................... 13 1.8 Thesis outline ........................................................................................................................................... 14 2 SPATIAL CLUSTERING OF PARASITES WITH DIFFERING TRANSMISSION MODES .......................................................................................................................................... 15 2.1 Abstract ................................................................................................................................................... 15 2.2 Introduction .............................................................................................................................................. 16 2.2.1 Studies into the clustering of infectious diseases ....................................................................... 18 2.2.2 Quantifying clustering: spatial point patterns and K function analysis ................................. 19 2.2.3 A natural model of clustering of diverse parasite types: The wood mouse parasite system 20 2.2.4 Hypotheses ...................................................................................................................................... 23 2.3 Methods ................................................................................................................................................... 23 2.3.1 Data .................................................................................................................................................. 23 2.3.2 K function analysis ......................................................................................................................... 25 2.3.3 Statistical analysis of K functions ................................................................................................ 27 2.4 Results ..................................................................................................................................................... 28 2.4.1 Differences between host and parasite clustering ..................................................................... 28 2.4.2 Null Model Testing ........................................................................................................................ 32 2.5 Discussion ................................................................................................................................................ 33 2.5.1 Apparently high degrees of clustering of Wood Mouse Herpes Virus .................................. 33 2.5.2 Clustering of environmentally transmitted parasites ................................................................ 35 2.5.3 Clustering of flea borne parasites ................................................................................................ 36 2.5.4 Lack of spatiotemporal analysis ................................................................................................... 37 2.5.5 Sample Size and Inference ............................................................................................................ 37 2.5.6 Overall conclusions ........................................................................................................................ 38 3 SPATIAL SCALING OF WITHIN-HOST COINFECTION INTERACTIONS ............. 40 3.1 Abstract ................................................................................................................................................... 40 3.2 Introduction .............................................................................................................................................. 41 3.2.1 Examples of coinfection in natural systems ............................................................................... 42 3.2.2 A natural model of coinfection: the wood mouse parasite system ......................................... 43 3.2.3 Aims and hypotheses ..................................................................................................................... 44 i 3.3 Methods ................................................................................................................................................... 44 3.3.1 Data .................................................................................................................................................. 44 3.3.2 Neighbourhood analysis ................................................................................................................ 46 3.3.3 Statistical Analysis .......................................................................................................................... 47 3.3.4 Accounting for treated animals .................................................................................................... 48 3.4 Results ..................................................................................................................................................... 49 3.4.1 Single parasite models .................................................................................................................... 49 3.4.2 Coinfection interaction models .................................................................................................... 49 3.4.3 Null Model Simulation .................................................................................................................. 52 3.5 Discussion ................................................................................................................................................ 53 3.5.1 Between host consequences of coinfection ............................................................................... 53 3.5.2 Methodological advance in the detection of coinfection interactions ................................... 54 3.5.3 Overall conclusions ........................................................................................................................ 56 4 SCALING OF COINFECTION INTERACTIONS ACROSS SOCIAL NETWORKS ..... 57 4.1 Abstract ................................................................................................................................................... 57 4.2 Introduction .............................................................................................................................................. 58 4.2.1 Assumptions of homogenous mixing and its limitations ......................................................... 58 4.2.2 Social network approaches and network features ..................................................................... 60 4.2.3 Network neighbourhood analysis and the spatial scale of coinfection interactions ............ 62 4.2.4 Aims and hypotheses ..................................................................................................................... 65 4.3 Methods ................................................................................................................................................... 65 4.3.1 Data .................................................................................................................................................. 65 4.3.2 Social Network Analysis ................................................................................................................ 66 4.3.3 Statistical models of individual network metrics ....................................................................... 66 4.3.4 Neighbourhood Analysis of Social Networks ........................................................................... 68 4.4 Results ..................................................................................................................................................... 69 4.4.1 Network structure over year and season ...................................................................................