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The Sexual Development of the Common Marmoset

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The Sexual Development of the Common Marmoset THE SEXUAL DEVELOPMENT OF THE COMMON MARMOSET MONKEY, CALLITHRIX JACCH(JS JACCH[JS by DAVID HOWARD ABBOTT Thesis submitted for /. the degree of Doctor of Philosophy at the University of Edinburgh March, 1979. To Angela --..'- •A - - - •. ,_-•• - •-- - - -- -- - - --•- • - - •---fl -- - - - • -:: Aj I TABLE OF CONTENTS Page ACKNOWLEDGEMENTS PUBLICATIONS ABSTRACT OF THESIS CHAPTER ONE: INTRODUCTION AND THE REVIEW OF LITERATURE 1 1.1 Introduction 1 1.2 The differentiation of male and female 1 1.2a The internal and external genitalia 1 1.2b The brain mechanisms regulating gonadal function 8 1 .2b(i) Mammals other than primates 8 1 .2b(ii) Primates (including man) 17 .1 .2c The brain centres controlling behaviour 22 1 .2c(i) Mammals other than primates 23 1 .2c(ii) Primates (including man) 31 1.3 The aims and scope of this study 39 CHAPTER TWO: MATERIALS AND METHODS )43 2.1 Animals 46 2.2 Management 46 2.2a Families 146 2.2b Peer groups and pairs 14.7 2.3 Observation room 14.7 2.3a Design 14.7 2.3b Construction 51 2.3c Routine use 51 2.3d Behavioural test conditions 52 24 Behavioural observation of families 52 2.4a Observation room 52 2.4b The observation schedules 52 T&BLE OF CONTENTS ... Cont. 2.4c Identification of animals 55 2.4d Behaviour recorded 55 204d(1) Social play behaviour 56 2.14.d(ii) Sexual behaviour 57 2.4d(ili) Aggressive and submissive behaviour 59 2.5 Behavioural observation of peer groups 59 2.5a Observational cages 59 2.5b Observation schedule 62 2.5c Identification of animals 63 2.5d Behaviour recorded 63 2.6 Behavioural observation of pairs of animals 66 2.7 Chance observations of behaviour 66 2.8 A computerised system for recording behaviour 66 2.8a The keyboard and tape deck 68 2.8b Encoding behaviour and animals 78 2.8c Decoding the recorded entries 78 2.8c(i) Calibration mode 81 2.8c(ii) Text mode 82 2.8c(iii) Event recording mode 82 2.8c(iv) Analogue mode 86 2.8d Transcription of recorded behaviour 86 2.9 A multi-pen recorder system for behaviour 89 2.10 Recording behaviour with abbreviated notes 92 2.11 Vaginal washings and the detection of inseminations 92 2.12 Collection of blood 95 2,13 Radioirnmunoassay for progesterone 95 2.13a Reagents 98 2.13b Assay procedure 99 TABLE OF CONTENTS ... Cont. Page 2.13b(i) Extraction of progesterone from plasma 99 2.13b(ii) Radioimrnunoassay 99 2013b(iii) Recovery 101 2,13c Inter- and intra-assay variation 102 2.13d Sensitivity 102 2.13e Calculations 102 2.14 Radloinimunoassay for oestradiol-1 7/? 103 2.15 Radioirnniunoassay for testosterone lOS 2.16 Validation of the steroid assays 108 2.17 Radioinimunoassay for luteinising hormone (Li) 110 2 .17a Reagents 111 2.17a(i) Buffers 2.17a(ii) Iodination of ratLH 112 2.17a(iii) Standards 112 2 .1 7a(iv) Antiserum 113 2.17b Assay procedure 113 2.17c Precision and sensitivity 114 2.17d Calculations 115 2.17e Validation of the LH assay us 2.18 Radioimrrrnnoassay for prolactin 117 2.18a Preparation of reagents 117 2.18b Assay procedure 119 2.18c Precision of the assay 120 2.18d Calculations 120 2.18e Validation of the prolactin assay 1120 2.19 Assay kit for cortisol 124 2.19a Contents of each kit 1:24 2.19b Reconstitution of the standards 125 TMLE OF CONTENTS ... Cont. 2.19c Assay procedure 125 2.19d Precision and sensitivity 128 2.19e Calculations 128 2.19f Validation of the assay - 128 2.20 Surgery 129 2.21 Surgical procedures 129 CHAPTER THREE: PATTERNS OF GROWTH AND PHYSICAL DEVELOPMENT 1 32 3.1 Introduction 133 3.2 Procedure 1 33 302a Body weight and knee-to-heel length 133 302b Pudendal pad and mammary glands 13)4 3.2c Testis volume 13)4 3.3 Results 13)4 3.3a Body weight and knee-to-heel length 13)4 3.3b Pudendal pad and mammary glands 136 303c Testis volume 1)42 3.4 Discussion 1)42 3.5 Chapter summary 1)47 CHAPTER FOUR: SEXUAL DEVELOPMENT: ENDOCRINOLOGY, REPRODUCTIVE BEHAVIOUR, FERTILITY AND BREEDING SUCCESS 1)48 4.1 Introduction 1)49 4.2 Procedure 150 4.2a Schedule of collection of plasma samples for radioirmmmoassay of hormone concentrations 150 2b Structure of the different social groups 152 )4.2c Observation schedules of the different social groups 1 53 4.2d Reproductive behaviour observed 15)4 TABLE OF CONTENTS ... Cont Page 4.2e Detection of pregnancies and spontaneous abortions 154 11..2f Evaluation of breeding success 155 4.3 Results 156 4.3a Changes in plasma hormone levels of young females 156 4.3b Changes in plasma hormone levels of young males 161 4.3c Reproductive behaviour and fertility 163 4.3d Breeding success of the different social groups and the different rates of spontaneous abortion 169 4.4 Discussion 171 24j4a Puberty 171 L.bb Endocrinological and behavioural aspects of female marmoset sexual development 175 4i4c Endocrinological and behavioural aspects of male marmoset sexual development 177 )4.)4d The contrasting development of sexual behaviour between monogamous and polygamous monkeys 178 4.4e The relationship between puberty, fertility and sexual maturity in marmoset monkeys 179 4.4f The effects of reproductive experience and different social groups on fertility and breeding success of marmoset monkeys 180 4.5 Chapter summary 181 CHAPTER FIVE: DOMINANT-SUBORDINATE RELATIONSHIPS AND THE REPRODUCTIVE SUCCESS OF YOUNG MARMOSET MONKEYS 183 5.1 Introduction 185 5.1a. Dominant-subordinate relationships and reproductive success in primate societies 185 5.1b Dominant-subordinate relationships and reproductive success in groups of marmosets and their close relatives, the tainarins 187 TABLE OF CONTENTS ... Cont. Page 5.2 General procedure 190 5.2a Structure of the social groups 190 5.2b Observation schedules 190 5,,2c Definition of dominant-subordinate interactions 191 5.2d Arrangement of dominant-subordinate interactions into a hierarchy 192 5.2e Description of pair-bonding behaviour in peer groups 193 5.2f Testing the ejaculatory response of male offspring in families and subordinate males in peer groups 194 5.2g Blood sampling and hormone assays 194 5.2h Pregnancy detection 194 5.3 Results S 194 5.3a Dominant-subordinate relationships among members of a family 194 5.3b Reproductive success in families 198 5.3c Dominant-subordinate relationships in newly-established peer groups 198 5.3d The contribution of each sex to the dominant-subordinate relationships in newly-established peer groups 206 - 5.3e Reduction of the frequency of dominant-subordinate interactions and the removal of subordinates from the peer groups 215 5.3f Dominant- subordinate relationships in well-established peer groups 217 5.39 Correlations of age, body weight, ear tuft colour and reproductive status with rank order 217 5.3h Pair-bonding behaviour 220 5.3i The reproductive success and break-up of the peer groups 226 TABLE OF CONTENTS ... Cont. Page 5.4 The relationship between female marmoset reproductive inhibition and their prolactin and cortisol levels 236 5.4a Procedure 236 5.4b Results 237 5.5 Discussion 242 5.5a Dominant-subordinate relationships in marmoset groups 242 5.5b The 'pair bond' and the monogamous breeding system of the marmoset 247 5.5c An analogy between families and peer groups of marmosets 249 5.5d Reproductive inhibition and the maintenance of the marmoset's monogamous breeding system 250 5,5e Female reproductive inhibition in marmosets in comparison with other species 253 5.6 Chapter summary 256 5.6a Family groups 256 5.6b Peer groups 257 5.6c General points 28 CHAPTER SIX: THE EFFECT OF NEONATAL EXPOSURE TO TESTOSTERONE ON THE DEVELOPMENT OF FEMALE MARMOSETS AND THE COMPARATIVE EFFECTS OF ORCHIDECTOMI AND OITARIECTONY 259 6.1 Introduction 261 6.2 Procedure 263 6.2a General methods 263 6.2b Testosterone and gonadectomy procedures 263 6.2c Blood sampling schedule 263 6.2d Families: Behaviour recorded and the statistical analysis 265 TABLE OF CONTENTS ... Cont. Page 6.2e Observation of peer groups and the behaviour recorded 266 6.2f Behavioural trials of unfamiliar animals; behaviour recorded and statistical analysis involved 266 6.3 Results 268 6.3a Testosterone dosage and the effects of experimental treatment on body weight 268 6.3b The effects of neonatal exposure to testosterone on female genitalia 268 6.3c The effects of ovariectoiny and orchidectomy on genital development 273 6.3d The effects of the neonatal treatments on pre-pubertal play behaviour 273 6.3e The effects of the neonatal treatments on behaviour in peer groups 277 6.3f The effects of the neonatal treatments on sexual behaviour 281 6.3f(i) Normal males, normal females and androgenized females 281 6.3f(ii) Normal females (born with a male co-twin) and normal females (born with a female co-twin) 287 6.3f(iii) Gonadectomized males and females and normal animals 287 6,3g The fertility of female marmosets exposed to neonatal testosterone 290 603h The effects of orchidectomy and ovariectomny on the pattern of Lii secretion in developing male and female marmosets 290 TABLE OF CONTENTS ... Cont. Page 6.4 Discussion 29 6J4a The consequences of postnatal differentiation in primates and Man 29 6i4b The effects of androgenization on growth, sexual development and fertility in female primates 300 6.4c The effects of androgenization on female playful and aggressive behaviour and the dimorphic characters of these behaviours 303 6.4d The effects of androgenization of female sexual behaviour and the consequences for postnatal differentiation in the marmoset 306 6.4e The effects of gonadectorny on the LII secretion of neonatal males 312 6.4f The different LII responses to gonadectomy of males and females before puberty 313 6.5 Summary 31 CHAPTER SEVEN: GENERAL DISCUSSION 316 7.1 General discussion 316 1EFEENCES 329 APPENDIX A 384 ACKNOWLEDGEMENTS I gratefully acknowledge all the staff members of the Medical Research Council Unit of Reproductive Biology, Edinburgh, for their interest in my work;.
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