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Reproductive Biology of Teleost Fishes




Reproductive Biology of Teleost Fishes

Robert J. Wootton, Carl Smith

ISBN: 978-1-118-89139-1 October 2014 Wiley-Blackwell 496 Pages

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Reproductive Biology of Teleost Fishes is the first integrated review of the reproductive biology of the bony fishes, which are the most species-rich and diversified group of vertebrates. Teleosts display remarkable variation in their modes of reproduction, and this volume is intended to provide a framework for understanding the remarkable reproductive diversity of this group. It describes their reproductive biology using, wherever possible, phylogenetic analyses and life-history theory as a means to interpret the information. The book addresses the genetic, physiological, behavioural, ecological, evolutionary and applied aspects of teleost reproduction in a comparative framework that emphasises the adaptive basis of reproductive diversity.

Reproductive Biology of Teleost Fishes provides a comprehensive synthesis of fish reproduction that will be of great interest to life scientists, particularly ecologists, evolutionary biologists, physiologists and advanced undergraduates, postgraduates and research workers requiring a comprehensive overview of fish reproduction. The book is suitable for courses in fish biology and ecology, reproductive physiology and reproductive genetics. It also addresses applied questions and will be of value for courses on fisheries science and aquaculture. Libraries in all universities and research establishments where biological sciences, fisheries science and aquaculture are studied and taught should have several copies of this important book on their shelves.

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

“I was very impressed by this book, even if it does not delve deeply into the mathematics of evolutionary theory applied to the topics.”  (Environ Biol Fish, 1 September 2015)