Reproductive Biology of Teleost Fishes

Preface xvii Acknowledgements xix Abbreviations and acronyms xxi 1 Introduction 1 Introduction 1 Reproductive modes of the teleosts 2 Gender systems of teleosts 2 Spawning dynamics 4 Modes of fertilisation 5 Mating systems 5 Secondary sexual characteristics 6 Parental care 6 Reproductive guilds 6 Reproductive diversity in teleosts: an explanatory framework 6 Phylogenetic relationships of the teleosts 8 Life-history theory 9 Aims of the volume 11 2 Sex determination 13 Introduction 13 Genotypic sex determination 14 Monofactorial genotypic sex determination 14 Multifactorial genotypic sex determination 20 Polyfactorial (polygenic) genotypic sex determination 20 Environmental sex determination 21 Evolution of sex-determining mechanisms 26 3 Sex differentiation 31 Introduction 31 Embryology of the gonads 32 Origin and migration of primordial germ cells 33 Sex differentiation in the gonadal anlagen 35 Initial differentiation of the gonads 36 Initial differentiation of ovaries 38 Initial differentiation of testes 38 Genetic control of early gonadal differentiation 40 Synthesis 42 4 Gametogenesis 45 Introduction 46 Structure of ovaries 48 Gross morphology of the ovaries 48 Development of female gonoducts 51 Oogenesis 52 Oogonial proliferation and oogonial nest formation 53 Chromatin nucleolus stage 53 Primary growth 54 Secondary growth – vitellogenesis 55 Vitellogenin and the zona pellucida proteins 56 Polarity of the oocyte 58 Oocyte maturation 58 Ovulation 60 Atresia 60 Fertilisation 62 Genetic control of oogenesis 64 Dynamics of oocyte development 65 Spawning dynamics and fecundity 66 Structure of the testes 66 Gross morphology of a testis 66 Development of male gonoducts 69 Accessory structures associated with the testes and gonoducts 70 Spermatogenesis 71 Spermatocysts 71 Sertoli cells 71 Stages of spermatogenesis within a spermatogenic spermatocyst 73 Differentiated spermatogonia 73 Primary spermatocysts 73 Secondary spermatocysts 73 Spermatids 74 Spermiation and capacitation 75 Types of spermatozoa 76 Structure and phylogenetic distribution 76 Spermatozoa viability 77 Genetic control of spermatogenesis 79 Dynamics of spermatogenesis 79 Quantitative analysis of sperm production 80 5 Endocrinology of reproduction 81 Introduction 82 Brain–pituitary–gonad reproductive axis in vertebrates 83 Levels of analysis 85 Gonadal steroids 86 Sex steroid synthesis 86 Sex steroid receptors 87 Endocrine control of oogenesis 88 Oogonial proliferation and primary growth 88 Secondary growth: vitellogenesis 89 Maturation and ovulation 90 Endocrine control of oogenesis in species with batch spawning 91 Endocrine control of spermatogenesis 93 Spermatogonial proliferation 95 Initiation of meiosis and formation of spermatocysts 95 Spermiation 96 Patterns of spawning in relation to spermatogenesis 96 The pituitary and the gonadotrophins 98 Brain–pituitary relationship 98 Gonadotrophs and gonadotrophins 99 Gonadotrophin receptors 100 Hypothalamic control of the pituitary 101 Gonadotrophin-releasing hormone 101 Functions of gonadotrophin-releasing hormone 102 Gonadotrophin-releasing hormone receptors 102 Distribution of gonadotrophin-releasing hormone neurons in the brain 103 Role of dopamine as an inhibitor of reproduction 104 Role of other brain factors in the control of gonadotrophs 105 Feedback control in the brain–pituitary–gonad reproductive axis 106 A provisional model for the control of the developmental dynamics of ovaries and testes 109 Puberty in teleosts 109 Physiological control of puberty 110 Interactions between growth and reproductive axes 113 Endocrines, behaviour and secondary sexual characteristics 116 Four model species 117 Role of endocrines in regulation of reproductive behaviour 118 Sensory systems 118 Central integrative systems 118 Motor systems 120 Endocrines and secondary sex characteristics 120 Effect of social interactions on reproductive endocrines 121 Role of pheromones in reproductive interactions 122 Endocrine-disrupting chemicals 123 Conclusions 125 6 Environmental control of reproduction 127 Introduction 128 Seasonal patterns of reproduction 128 Global seasonal patterns 128 Ultimate factors 129 Proximate factors 130 Spawning seasonality in freshwater systems 130 Spawning seasonality in marine species 132 Lunar-related reproductive cycles 134 Intertidal spawners 135 Coral reef spawners 135 Freshwater spawners 136 Diel reproductive cycles 136 Multiple environmental cycles 136 Endogenous cycles and reproductive activity 137 Proximate factors 138 Photoperiod and temperature 139 Lunar-related and tidal cycles 143 Rainfall, flooding and other cues 143 Social factors as cues 144 Stress and reproduction 144 Neuroendocrine mechanisms mediating environmental effects 147 Food as a proximate factor 150 Feeding and capital breeders 151 Feeding and income breeders 154 Feeding and skipped spawnings 155 Physiological basis for the effect of feeding on reproduction 156 Conclusions 157 7 Migration, territoriality and spawning site selection 159 Introduction 160 Migration 160 Terms and definitions 161 Migratory patterns associated with reproduction 162 Adaptive significance of reproductive migrations 164 Energetic costs of migration 166 Survival costs of migration 167 Physiological adaptations associated with migration 167 Mechanisms of orientation and homing during spawning migrations 168 Control of timing of migration 171 Human impacts on migration 172 Territoriality 173 The concept of territoriality and definitions 174 Adaptive significance of territoriality 174 Cost–benefit analysis and evolutionary stable strategy 174 Aggression and territoriality 175 Patterns of occurrence of territoriality 176 Establishment and maintenance of territories 180 Physiological basis of territoriality 182 Energetic costs of territoriality 184 Genetic basis of territoriality 184 Territoriality and population dynamics 185 Spawning site selection 188 Sites for reproduction 188 Site selection without habitat modification 188 Site preparation 189 Site excavation 189 Site preparation and young brooded elsewhere 190 Site preparation and eggs buried 191 Excavation of shelters and tunnels 192 Nest construction 193 Terrestrial spawning sites 195 Cues used in spawning site selection 197 Spawning symbioses 197 Conclusions 200 8 Mating systems and sexual selection 201 Introduction 202 Classification of mating systems 203 Sexual selection and theories of mate choice 204 Direct intersexual selection 205 Indirect intersexual selection 206 Good genes 207 Compatible genes 207 Antagonistic genes 209 Arbitrary mate choice 210 Fisherian selection 210 Sensory bias 211 Male mate choice and female ornaments 212 Mutual mate choice and the ‘double process’ of sexual selection 214 Mate choice copying 216 Intrasexual selection 216 The interaction of intra- and intersexual selection 218 The strength of sexual selection and the operational sex ratio 218 Courtship 219 Functions of courtship 219 Mate identification and attraction 219 Mate stimulation, mating synchrony and appeasement 220 Maintenance of pair bonds 221 Ornaments and signals in courtship 221 Visual 222 Body size 222 Morphological trait size 223 Colour 224 UV reflectance 224 Display behaviour 225 Auditory 226 Olfaction and gustation 227 Tactile, electrical and other cues 228 Multiple cues 228 Sexual signals and reproductive isolation 229 Fertilisation 231 Sperm competition 231 Cost of sperm production 231 Risk and intensity of sperm competition 232 Sperm competition avoidance 234 Pre-oviposition ejaculation 234 Seminal fluid composition 235 Sperm capacitation and motility 235 Ejaculate size and ejaculation frequency 236 External fertilisation 237 Internal fertilisation 238 Quasi-internal fertilisation 239 Male mating polymorphisms 240 Causal factors 242 Floaters, sneakers, streakers, pirates, parasites, fighters and the bourgeoisie 243 Male mating polymorphism and sperm competition 244 Guarder male response to non-guarders 244 Female response to alternative male mating phenotypes 244 Female mating polymorphisms 245 Sexual conflict 246 Phylogenetic history and mating system evolution 249 9 Parental care 251 Introduction 252 Definition of care 252 Distribution of parental care 252 Modes of parental care 253 Protection from predators and disturbance 253 Protection from hypoxia and desiccation 253 Protection from pathogens 255 Nutrition 256 External bearing 257 Internal bearing 261 Costs of parental care 262 Cost to parental survival 262 Cost to number of offspring produced 264 Sex role reversal and parental care 265 Phenotypic plasticity in care 266 Number of offspring 266 Offspring age 267 Offspring quality 267 Food availability 268 Parental age 268 Availability of alternative mates 268 Helper care systems 269 Alloparental care 270 Sneaky mating and egg dumping 270 Egg stealing, kidnapping and nest takeovers 271 Brood parasitism 271 Cooperative care 273 Misdirected care 274 Filial cannibalism 274 Evolution of parental care 276 10 Unusual reproductive modes 281 Introduction 282 Viviparity in teleosts 282 Systematic distribution of viviparity in teleosts 283 Internal fertilisation 283 Lecithotrophy and matrotrophy 286 Ovarian modifications in viviparity 287 Testis modification in viviparity 289 Gestation 289 Timing of events 289 Embryonic nutrition 290 Superfetation 291 Endocrine control of viviparity 292 Evolution of viviparity and matrotrophy 292 Male viviparity in the Syngnathidae 295 Unisexual teleosts 298 Systematic distribution of unisexual biotypes in teleosts 299 Cyprinodontiformes 300 Poeciliid unisexuals 300 Poeciliid unisexuals: Poecilia formosa 300 Poeciliid unisexuals: Poeciliopsis 300 Atheriniformes 301 Cypriniformes 301 Phoxinus eos-neogaeus 302 Tropidophoxinellus alburnoides 302 Carassius gibelio 302 Cobitis 303 Problems posed by unisexual teleosts 303 Developmental 303 Evolutionary implications 304 Hermaphroditism in teleosts 305 Phylogenetic distribution of hermaphroditism in teleosts 306 Gonadal organisation in hermaphroditic fishes 308 Endocrinology of reproduction in hermaphroditic species 309 Simultaneous hermaphrodites 312 Self-fertilisation 312 Cross-fertilisation 313 Sequential hermaphrodites 313 Protogyny 314 Protandry 315 Serial change 315 Adaptive significance of hermaphroditism 316 Why are hermaphrodites found in teleosts? 319 Deep-sea anglerfish dwarf males: quasi-hermaphroditism 320 11 Reproduction and life-history evolution 323 Introduction 324 Life-history variables 324 Size and age at maturity 325 Fecundity and clutch size 325 Egg and offspring size 327 Incubation time 331 Reproductive lifespan 333 Parental care 333 Other life-history traits 333 Basic concepts in life-history theory 334 Trade-offs 334 Costs of reproduction 334 Measuring the costs of reproduction 335 Evidence of costs of reproduction 336 Reproductive effort 338 Demographic models of life-history evolution 339 Measures of fitness 340 Predictions of demographic models 341 Empirical studies of life-history evolution 342 Habitat invasion 344 Environmental gradients 346 Habitat templet model 347 Dimensionless variables and life-history invariants 350 Plasticity of life-history traits 351 Constraints on life-history evolution 353 Alternative life-history strategies 354 Conclusions 356 12 Reproduction, fisheries and aquaculture 357 Introduction 358 Reproduction and fisheries management 358 Stock–recruitment relationships and reproduction 358 Reproductive traits and population dynamics 362 Age at maturity 362 Fecundity 363 Mode of reproduction and susceptibility to overexploitation 364 The impact of fisheries on reproductive traits 365 Age and size structure 365 Population sex ratio 368 Population size and density 370 Fisheries-induced evolution 372 Control of reproduction in aquaculture 373 Facilitating reproduction 374 Environmental manipulation 374 Endocrine manipulation 375 Sexual dysfunction in cultivated fishes 376 Sexual dysfunction in females 376 Sexual dysfunction in males 378 Preservation of gametes 378 Suppressing reproduction 379 Monosex production 379 Endocrine manipulation 380 Production of female monosex lines 381 Production of male monosex lines 382 Gynogenesis 383 Androgenesis 385 Hybridisation 385 Sterilisation 386 Mechanical, immunological, chemical and irradiation techniques 386 Hybridisation 387 Polyploidy 387 13 Coda 389 References 391 Systematic index 451 Subject index 463