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The Evolution and Socio-Ecology of Two Populations of the Vlei Rat Otomys Irroratus

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The Evolution and Socio-Ecology of Two Populations of the Vlei Rat Otomys Irroratus THE EVOLUTION AND SOCIO-ECOLOGY OF TWO POPULATIONS OF THE VLEI RAT OTOMYS IRRORATUS by Neville Pillay Submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy, in the Department of Biology, University of Natal 1993 Durban 1993 ii For Dineshree and the Chinee mouse gang. " Besides, Individualism has really the higher aim... " (The Picture of Dorian Gray: Oscar Wilde 1891) iii PREFACE This study was carried out in the Department of Biology, University of Natal, Durban, from March 1991 to December 1993, under the supervision of Professor J. Cooke and Dr K. Willan. This thesis represents original work by the author and has not been submitted in any form to another university. Where use was made of the work of others it has been duly acknowledged in the text. ~ . ----------- iv ACKNOWLEDGEMENTS I would like to thank Dr Ken Willan for his encouragement, able supervision and guidance during the early part of this study. Thanks to Ken for introducing me to the field of small mammal biology and helping me understand and interpret mammalian social evolution . Prof. John Cooke supervised the latter part of this project, and his guidance and patience are appreciated. Prof. Cooke and Prof. Waldo Meester patiently read earlier drafts of this work, and I remain eternally grateful to them. Prof. Anne Alexander read drafts of some of the behaviour-related chapters. Her comments have contributed gre tly tow rd improving int rpr tation 0 the data in these chapters. Thanks to members of the Speciation Group - Glen Campbell, Giancarlo Contrafatto, Janine Raubenheimer and Peter Taylor - for discussing with me the interpretation of various data. A special thanks to Giancarlo and Janine for allowing me access to unpublished material. Technical assistance was provided by Margaret du Plessis, Sergie Govender, Kay Govindsamy, Alan Grace, Reuben Ngubane, James Wesley-Smith and Peter Wright. Simon Shezi deserves special mention for tirelessly feeding and maintaining the animals and for providing magnificent support over so many years. Several people provided equipment which was vital for the execution of aspects of this study. They include Prof. Mike Perrin for sound recording equipment and a bat detector, v Prof. Gordon Maclean for sonographic equipment, and Prof. Norman Pammenter for a light meter. Dehn von Ahleveldt and Gavin MacDonald helped identify some of the plant specimens, and their contribution is acknowledged. Thanks to Dr Dave Rowe-Rowe of the Natal Parks Board and Rob Parker of Hans-Merensky (Karkloof) forests for providing rainfall data, and for permission to trap and conduct field work at Kamberg and Karkloof respectively. Rob provided some of the animals used in this study. A number of people helped with the field work, of whom Clare, Sumita, Ana-Maria, Thirusha, Malcolm, Ramesh and Reuben deserve special praise. Financial support from the FRO and University of Natal is gratefully acknowledged. I thank my family for their support and encouragement. Finally, I owe special thanks to Dineshree Padiachy who provided not only incredible support , but who was my secretary, research assistant, proof-reader and shrink. vi ABSTRACT This work investigated two important evolutionary processes - speciation and adaptive variation - in two chromosomally-distinct allopatric Natal Midlands populations of the vlei rat Otomys irroratus. The two populations, at Kamberg and Karkloof, differ in the presence of a tandem fusion between chromosomes seven and 12 in the Kamberg karyotype. Speciation studies considered possible reproductive isolating mechanisms. In studies of adaptive variation, socio-ecological characteristics of both populations were investigated. Data on breeding and postnatal development provided evidence of post-zygotic barriers. Interpopulation pairs had reduced breeding success compared to intrapopulation pairs, and some hybrids died before weaning. Surviving hybrids had reduced growth rates, and almost all were sterile. In tests of pre-mating reproductive isolation, ethological barriers were emphasized. Individuals preferred same-population mates, suggesting the existence of mate recognition, which was achieved by means of population-specific courtship behaviour and communication, particularly olfactory, tactile and visual cues. No evidence of population-specific acoustic signals was found, although acoustic cues were associated with agonistic interaction, complementing other communicatory cues to promote increased aggression during interpopulation pairings. Laboratory studies of behaviour and morphology and field work (trapping and habitat assessment) provided information about socio-ecological parameters. The Kamberg habitat was vii harsher than the Karkloof one, as revealed by differences in seasonal and spatial availability of food and·cover. Cover was the key determinant of the level of sociability of both populations. Sparse, patchy cover selected for a partially communal social system in Kamberg o. irroratus: females were intrasexually tolerant and males were intrasexually highly aggressive. This, in conjunction with male-biased sexual dimorphism, implied that mating was polygynous. Abundant, uniform cover selected for a dispersed social system in Karkloof o. irroratus: females were intrasexually less tolerant than males. Ritualized aggression between males and a low degree of male-biased sexual dimorphism suggested that male may hav overlapping hom rang s in nature and that mating is promiscuous. Females possibly mated with dominant males, however. Contrasting social systems suggest that adaptation to local environmental circumstances has occurred in allopatry, and that Kamberg and Karkloof o. irroratus are undergoing adaptive speciation. Post-zygotic and pre-mating reproductive barriers appear to have evolved independently in both populations, and could potentially impede gene flow between the populations should they become sympatric. The presence of the tandem fusion in the Kamberg karyotype which, together with genetically-determined factors, may have caused hybrid sterility, suggests that this population is a chromosomally-determined incipient sibling species. viii CONTENTS Page PREFACE iii ACKNOWLEDGEMENTS iv ABSTRACT vi CONTENTS viii LIST OF TABLES x LIST OF FIGURES xiv CHAPTER 1 INTRODUCTION 1 Motivation for the study 1 Approach to the study 9 General biology of o. irroratus 12 Modes of speciation in o. irroratus 15 Socio-ecology 17 Arrangement of the thesis 19 CHAPTER 2 GENERAL METHODS 20 Introduction 20 Terminology 20 Field studies 21 Captive studies 22 Data analysis 23 CHAPTER 3 BREEDING AND POSTNATAL DEVELOPMENT 25 Introduction 25 Materials and methods 26 Results 29 Discussion 35 Conclusions 38 CHAPTER 4 CHOICE AND OLFACTORY DISCRIMINATION TESTS 40 Introduction 40 Methods 42 Results 47 Discussion 50 Conclusions 55 ix CHAPTER 5 INTRA- AND INTERPOPULATION MALE-FEMALE ENCOUNTERS 57 Introduction 57 Materials and methods 59 Re suLts 61 Discussion 70 Conclusions 76 CHAPTER 6 AUDITORY COMMUNICATION 77 Introduction 77 Materials and methods 78 Results 80 Discussion 87 CHAPTER 7 POPULATION-SPECIFIC HABITAT CHARACTERISTICS AND POPULATION ECOLOGY 93 Introduction 93 Materials and methods 94 Results 104 Discussion 111 uCHAPTER 8 SOCIAL STRUCTURE 125 Introduction 125 Materials and methods 129 Results 135 Discussion 141 CHAPTER 9 GENERAL DISCUSSION AND CONCLUSIONS 155 Introduction 155 Socio-ecology 155 Speciation and reproductive isolation 166 Evolutionary considerations 170 Conclusions 176 SUMMARY 184 REFERENCES 190 x LIST OF TABLES Page Chapter 3: Breeding and postnatal development 1. Reproductive data in respect of intrapopulation, interpopulation, backcross and hybrid-cross pairings. 30 2. Timing of the onset of postnatal developmental events for progeny resulting from intra- and interpopulation pairings. 30 3. Von Bertalanffy growth equations for increase in body mass of males and females resulting from intra- and interpopulation pairings. 34 Chapter 4: Choice and olfactorY discrimination tests 1. Mean number of visits to compartments adjacent to homotype and heterotype individuals by test animalS, for the first hour of testing. 48 2. Mean number of minutes spent in compartments adjacent to homotype and heterotype individuals by test animals, during three time periods. 48 3. Mean number of visits to test units with odours of homotype and heterotype individuals by test animals, for the first hour of testing. Sl Chapter 5: Intra- nd int rpopulation mal - emale encounters 1. Behaviour patterns identified in encounters and the equivalent behaviour patterns for rodent species in other studies. 62 xi 2. Mean frequencies of behaviour patterns for male Kamberg and Karkloof o. irroratus during ·t h e first 20 min of intrapopulation encounters. 64 3 . Mean frequencies of behaviour patterns for female Kamberg and Karkloof o. irroratus during the first 20 min of intrapopulation encounters. 65 Chapter 6: Auditory communication 1. Mean values of the parameters describing the acoustic signals produced by Kamberg and Karkloof individuals. 81 2. Median numbers of acoustic signals produced during male-female intra- and interpopulation encounters. 88 Chapter 7: Population-specific habitat characteristics and population ecology 1. Plant species present at the Kamberg and Karkloof study areas. 98 2. Abundance and distribution of O. irroratus at the Kamberg and Karkloof trap-sites during summer, autumn and winter. 105 3 . Overall and adult sex ratio and percentage sexually active adult animals at the Kamberg and
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