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Determinants of Reproductive Status and Mate Choice in Captive Colonies of the Naked Mole-Rat, Heterocephalus Glaber

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Determinants of Reproductive Status and Mate Choice in Captive Colonies of the Naked Mole-Rat, Heterocephalus Glaber DETERMINANTS OF REPRODUCTIVE STATUS AND MATE CHOICE IN CAPTIVE COLONIES OF THE NAKED MOLE-RAT, HETEROCEPHALUS GLABER FRANK M. CLARKE A thesis submitted in fulfillment of the requirements of University of London for the degree of Doctor of Philosophy OCTOBER 1998 ProQuest Number: 10609357 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a com plete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest ProQuest 10609357 Published by ProQuest LLC(2017). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States C ode Microform Edition © ProQuest LLC. ProQuest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106- 1346 I declare that I have conducted the work in this thesis, that I have composed this thesis, that all the quotations and sources of information have been acknowledged and that this work has not previously been accepted in an application for a degree. Frank Clarke Abstract Naked mole-rats are small, fossorial, cooperatively breeding rodents with a high reproductive skew. Wild colonies contain around 80 individuals and reproduction is monopolised by a single female, the 'queen', and one to three males. This study investigates the hormonal, behavioural, and genetic correlates of dominance and breeding status in captive colonies. I examine the relationship between dominance rank, reproductive status, and urinary testosterone and cortisol levels, and try to determine whether physiological and behavioural parameters can be used as predictors of succession by experimentally removing breeders. Additionally, Y-maze choice tests were used to investigate kin recognition and female mate choice. Colony social structure is characterised by a linear dominance hierarchy with male and female rank correlated with body weight, age, and testosterone levels. Rank appears the most important determinant of reproductive status. Queens are generally the highest ranking colony member and breeding males the highest ranking males. Both are succeeded by the next highest ranking individuals. Queen succession results in an increase in body weight of colony members, the reproductive activation of one or more females, and often intense dominance-related aggression by females. In contrast, male-male competition over breeding rights is low. This result is interpreted in terms of 'skew theory' and female mate choice. No evidence for a simple relationship between social status and the 'stress' hormone cortisol was found. Furthermore, cortisol does not appear to be causally implicated in suppression of subordinate reproduction. Females discriminate between conspecifics on the basis of familiarity, not through detection of genetic similarity, and discrimination is dependant on their reproductive status. Whereas queens prefer unfamiliar males as mates, reproductively inactive females fail to discriminate. Preferences are interpreted as inbreeding avoidance. Thus, the genetic relationship of males to queens is an important determinant of reproductive status in males. DEDICATION To my mum, Grace, who encouraged my love of natural history from a very young age, and made all this possible. ACKNOWLEDGMENTS This work was supported by a Biotechnology and Biological Research Council studentship reference no. 94316743. The research was carried out at the Institute of Zoology, part of the Zoological Society of London. The B.B.S.R.C. also contributed towards the costs of visiting South Africa, carrying out collaborative research at the University of Cape Town, and of speaking at die Symposium for Southern African Zoology Pretoria 1996. This study was covered by Home Office project license PPL/3897. A very special thanks to Chris for being incredibly patient and understanding supervisor. He needed to be! Also, thanks Chris for inspiring me - that one can have a life and be a scientist! Thanks also to my sub-supervisors, Mike Bruford and Linda Partridge. Mike, your unsympathetic approach to student problems stopped us dwelling on our worries - we know as a student you had it 100 times worse. Thanks Linda for your (very) critical analysis of my first year report, which gave me a kick up the ass and put me on the right track. Not forgetting the mole-rats themselves. I have gained an deep insight into their lives which has proved more fascinating than watching the most outrageous soap opera, and with the same high drama - sex, infidelity, incest, fighting and murder. Many thanks to all my friends, family, and workmates who made life as a Ph.D student tolerable - even enjoyable at times. A special mention goes to the following people. Kofi, A1 and Ulrich for their friendship and supports, and for the endless philosophical discussions about the meaning of life. Tom Kyffin for his friendship and excellent mole-rat illustrations. Fellow workfriends Dada, Rob, Kath Jeffries, and fellow suffering Ph.D. students - Michelle, Tamsin, Trevor and Steve. All the London Techno Soundsystems and free party people who provided a much needed distraction from work. I would also like to thank the following people who for their support and help. Roger Downie and Felicity Huntingford (University of Glasgow), for the use of Zoology departmental facilities. Mandy Donaldson and technicians at medical endocrinology unit, Hammersmith Hospital, for providing me with radioactive label. Jennifer Jarvis (UCT) and Nigel Bennett (Pretoria University) for making my stay in South Africa so enjoyable and productive. Daphne Green for patiently answering many questions on assays (with patently obvious answers) and by risking life and limb by sharing the same laboratory with me. Elizabeth for help with The Observer and SPSS. Mark Beaumont and Stuart Bearshop for statistical advice and all those who read earlier drafts of this thesis. On behalf of the mole-rats I would like to thank the following people. Selwyn Mundy for keeping a roof over their heads and providing them with a burrow system any self respecting rodent would give their incisors for. Mike Lovett and the other animal technicians at the Institute of Zoology for meals on wheels and their expert care and attention. Tony Sainsbury and the other veterinary staff at the Zoological Society of London for excellent medical care. CONTENTS 1. INTRODUCTION 1.1 PHYLOGENY 1 1.2 MORPHOLOGY 1 1.3 ECOLOGY & DEMOGRAPHY 2 1.4 SOCIAL ORGANISATION 3 1.4.1 The eusociality continuum 3 1.4.2 Reproductive division of labour 5 1.4.3 Reproductive suppression 6 1.4.4 Overlap of generations 7 1.4.5 Cooperative care of young 7 1.4.6 Division of labour among helpers 8 1.4.7 Inbreeding and inbreeding avoidance 9 1.4.8 Evolution of eusociality & cooperative breeding in mole-rats 12 1.4.9 Reproductive skew 14 1.5 DETERMINANTS OF REPRODUCTIVE STATUS 18 1.5.1 Dominance rank, size and age 18 1.5.2 Dominance hierarchies 19 1.5.3 Dominance, aggression and androgens 20 1.5.4 Benefits of being dominant 22 1.5.5 Dominance, social stress and reproduction 23 1.6 KIN RECOGNITION 25 1.6.1 Recognition cues 26 1.6.2 Recognition mechanisms 27 1.6.3 MHC and kin recognition 29 1.7 MATE CHOICE 30 1.7.1 Choice for genetic benefits 30 1.7.2 Dissassortative mating in mammals 31 1.8 RESEARCH AIMS 33 2. GENERAL METHODS 2.1 HOUSING AND HUSBANDRY 38 2.2 BEHAVIOURAL RECORDING 40 2.2.1 Sampling method 40 2.2.2 Ethogram 41 2.2.3 Recording method 43 2.3 COLLECTION OF BODY FLUIDS 44 2.3.1 Urine sampling 44 2.3.2 Blood sampling 44 2.4 HORMONE DETERMINATION 45 2.4.1 Creatinine determination 45 2.4.2 Testosterone assay 47 2.4.3 Progesterone assay 50 2.4.4 Cortisol assay 53 2.4.5 Luteinising hormone assay 56 3. HORMONAL AND BEHAVIOURAL CORRELATES OF FEMALE DOMINANCE AND REPRODUCTIVE STATUS 3.1 INTRODUCTION 60 3.2 METHODS AND MATERIALS 62 3.3 RESULTS 65 3.3.1 Pre-queen removal 65 3.3.2 Post-queen removal 68 3.4 DISCUSSION 73 4. HORMONAL AND BEHAVIOURAL CORRELATES OF MALE DOMINANCE AND REPRODUCTIVE STATUS 4.1 INTRODUCTION 77 4.2 METHODS AND MATERIALS 79 4.3 RESULTS 82 4.3.1 Before breeding male removal 82 4.3.2 Breeding male removal (1) 82 4.3.3 Breeding male removal (2) 88 4.4 DISCUSSION 91 5. FUNCTION OF SHOVING 5.1 INTRODUCTION 94 5.2 METHODS AND MATERIALS 96 5.3 RESULTS 98 5.3.1 Before breeder removal 98 5.3.2 After queen removal 106 5.3.3 After breeding male removal 109 5.3.4 Urinary hormone levels 110 5.4 DISCUSSION 111 6. KIN RECOGNITION AND FEMALE MATE CHOICE 6.1 INTRODUCTION 117 6.2 METHODS AND MATERIALS 119 6.3 RESULTS 124 6.3.1 Female reproductive status 124 6.3.2 Odour preference for familiarity 125 6.3.3 Odour preference for relatedness 126 6.3.4 Social preference for familiarity 127 6.3.5 Social preference for relatedness 127 6.3.6 Mate choice 128 6.4 DISCUSSION 131 7. DISPERSAL 7.1 INTRODUCTION 137 7.2 METHODS AND MATERIALS 139 7.3 RESULTS 142 7.3.1 Identification of dispersers 142 7.3.2 Transfer experiment 144 7.4 DISCUSSION 145 8. GENERAL DISCUSSION 147 REFERENCES 157 vii LIST OF FIGURES Typical layout of laboratory burrow systems. 39 Mean body weight of males and females as a function of dominance rank in colony Nl, colony O, and colony NN before queen removal. 66 Female urinary testosterone levels (mean ± s.d.) as a function of dominance rank in colony Nl, colony O, and colony NN before queen removal.
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