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Evolution of Reproductive Traits in Sharks and Rays

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Evolution of Reproductive Traits in Sharks and Rays EVOLUTION OF REPRODUCTIVE TRAITS IN SHARKS AND RAYS A thesis submitted to the University of Manchester for the degree of Doctor of Philosophy (PhD) in the School of Medical Sciences, Faculty of Biology, Medicine and Health 2018 AMY ROWLEY FACULTY OF BIOLOGY, MEDICINE AND HEALTH 2 Contents LIST OF FIGURES 6 LIST OF TABLES 9 LIST OF APPENDICES 12 GENERAL ABSTRACT 13 DECLARATION 14 COPYRIGHT STATEMENT 15 ACKNOWLEDGEMENTS 16 1. GENERAL INTRODUCTION 19 1.1 SEXUAL SELECTION 19 1.2 SPERM COMPETITION 22 1.3 CRYPTIC FEMALE CHOICE AND SEXUAL CONFLICT 33 1.4 OUTSTANDING QUESTIONS IN HOW SPERM COMPETITION INFLUENCES THE EVOLUTION OF REPRODUCTIVE TRAITS 34 1.4.1 SPERM NUMBER 35 1.4.2 SPERM MORPHOLOGY 36 1.4.3 SPERM VARIANCE 37 1.4.4 GENITAL MORPHOLOGY 38 1.5 STUDYING EVOLUTIONARY RESPONSES OF REPRODUCTIVE TRAITS TO SPERM COMPETITION 39 1.6 SPERM COMPETITION AND EVOLUTIONARY RESPONSE IN SEXUAL TRAITS IN ELASMOBRANCHS 39 1.6.1 ELASMOBRANCHS 40 1.6.2 SHARKS VS RAYS 41 1.6.3 REPRODUCTIVE BEHAVIOURS IN ELASMOBRANCHS 41 1.6.4 GENETIC MATING SYSTEMS 43 1.6.5 VARIATION IN REPRODUCTIVE TRAITS 46 1.7 REPRODUCTIVE VARIATION IN MALES 47 1.7.1 TESTES 47 1.7.2 SPERM MORPHOLOGY 48 1.7.3 CLASPERS 49 1.8 REPRODUCTIVE VARIATION IN FEMALES 50 1.8.1 REPRODUCTIVE MODE 50 1.8.2 FECUNDITY 51 1.8.3 SPERM STORAGE 52 1.9 CHALLENGES IN STUDYING ELASMOBRANCH REPRODUCTION 54 1.10 AIMS OF THE THESIS 55 1.11 REFERENCES 56 2. TESTES SIZE INCREASES WITH SPERM COMPETITION RISK AND INTENSITY IN BONY FISH AND SHARKS 72 2.1 ABSTRACT 73 2.2 INTRODUCTION 74 2.3 METHODS 76 3 2.3.1 DATA COLLECTION 76 2.3.2 PHYLOGENY 78 2.3.4 PHYLOGENETIC ANALYSES 79 2.4 RESULTS 81 2.4.1 VARIATION IN SPERM COMPETITION RISK AND INTENSITY AMONG FISHES 81 2.4.2 SPERM COMPETITION RISK, INTENSITY AND TESTICULAR INVESTMENT 83 2.5 DISCUSSION 87 2.6 ACKNOWLEDGMENTS 89 2.7 REFERENCES 89 CHAPTER 2: SUPPORTING INFORMATION 96 SUPPORTING INFORMATION REFERENCES 105 3. SPERM COMPETITION AND THE EVOLUTION OF TESTES ORGANISATION IN SHARKS AND RAYS 113 3.1 ABSTRACT 114 3.2 INTRODUCTION 115 3.3 METHODS 117 3.3.1 SAMPLE COLLECTION 117 3.3.2 HISTOLOGICAL PROCESSING 119 3.3.3 IMAGE ANALYSIS 119 3.3.4 ESTIMATING SPERM COMPETITION RISK 120 3.3.5 PHYLOGENETIC ANALYSES 121 3.4 RESULTS 123 3.5 DISCUSSION 132 3.6 ACKNOWLEDGMENTS 136 3.7 REFERENCES 137 CHAPTER 3: SUPPORTING INFORMATION 142 SUPPORTING INFORMATION REFERENCES 143 4. SEXUAL SELECTION DRIVES DIVERGENT PATTERNS OF SELECTION ON SPERM FLAGELLUM LENGTH IN SHARKS AND RAYS 146 4.1 ABSTRACT 147 4.2 INTRODUCTION 148 4.3 METHODS 151 4.3.1 SAMPLE COLLECTION 151 4.3.2 SPERM ANALYSIS 152 4.3.3 PHYLOGENETIC LINEAR MODELS 154 4.3.4 COMPARING EVOLUTIONARY RATES 156 4.4 RESULTS 157 4.4.1 SPERM COMPETITION AND SPERM MORPHOLOGY 157 4.4.2 RATES OF EVOLUTION OF SPERM COMPONENTS 163 4.5 DISCUSSION 164 4.6 ACKNOWLEDGEMENTS 171 4.7 REFERENCES 172 CHAPTER 4: SUPPORTING INFORMATION 179 SUPPORTING INFORMATION REFERENCES 183 5. THE EVOLUTION OF WEAPONIZED GENITALS IN SHARKS 191 5.1 ABSTRACT 192 5.2 INTRODUCTION 193 4 5.3 METHODS 197 5.3.1 FIELD COLLECTED SAMPLES 197 5.3.2 LITERATURE COLLECTED DATA 197 5.3.3 COMPILING THE FINAL DATASET 199 5.3.4 PHYLOGENETIC ANALYSES 199 5.3.5 ANCESTRAL STATE RECONSTRUCTION 200 5.3.6 PHYLOGENETIC LINEAR MODELS 200 5.4 RESULTS 201 5.4.1 ANCESTRAL STATE RECONSTRUCTIONS AND THE GAINS AND LOSSES OF GENITAL APPENDAGES 201 5.4.2 PHYLOGENETIC LINEAR MODELS 204 5.5 DISCUSSION 208 5.6 ACKNOWLEDGMENTS 213 5.7 REFERENCES 214 CHAPTER 5: SUPPORTING INFORMATION 220 SUPPORTING INFORMATION REFERENCES 229 6. GENERAL CONCLUSION 238 6.1 THESIS SUMMARY 238 6.2 LIMITATIONS 245 6.3 FUTURE DIRECTIONS 248 6.4 REFERENCES 250 5 List of Figures Chapter 1: General introduction Figure 1.1: Summary of variation observed in male and female reproductive behaviours and how this variation influences the risk of sperm competition experienced by males ……………………………………………………………………………………….... 24 Figure 1.2: Comparison of a large guarding male and a smaller sneaking male in plainfin midshipman (Porichthys notatus), a species with two alternative male reproductive tactics. Testis size of a guarding and sneaking male demonstrating increased investment in testes in sneaking males ………………………………………………. 26 Figure 1.3: Diversity in genital morphology among cartilaginous fishes (sharks, skates, rays, sawfish and chimaeras) .……………………………………………………………………27 Figure 1.4: Variation in the percentage of litters sired by multiple males across shark and ray species ..………………………………………………………………………………………… 45 Figure 1.5: Variation in elasmobranch testes organisation in three shark and ray species, as illustrated by haematoxylin and eosin-stained histological testes sections ….………………………………………………………………………………………………………………………….48 Figure 1.6: Elasmobranch sperm ultrastructure. A single sperm cell from a nervous shark (Carachrinus cautus), with the components indicated and head coloured with the nuclear-binding stain DAPI ..……………………………………………………………………………49 Chapter 2: Testes size increases with sperm competition risk and intensity in bony fish and sharks Figure 2.1: Variation in sperm competition risk and intensity across fishes. Phylogenetic relationships between fish species in our dataset, with points representing the percentage of litters sired by multiple males for each species (risk), and the average number of sires per brood within each species (intensity) ……………………………………………………………………………………………………………………………..82 6 Figure 2.2: Relationships between testes mass relative to body size and (a) the percentage of litters sired by more than one male (sperm competition risk) and (b) the mean number of sires per brood (sperm competition intensity) across species. ……………………………………………………………………………………………………………………………. 86 Chapter 3: Sperm competition and the evolution of testes organisation in sharks and rays Figure 3.1: Variation in testes organisation traits across sharks and rays, as illustrated by haematoxylin and eosion-stained histological testes sections from (a) Ginglymostoma cirratum, (b) Mustelus asterias, (c) Chiloscyllium punctatum and (d) Scyliorhinus stellaris, shown at 20x magnification. …………………………………….……… 125 Figure 3.2: Traitgrams showing phenotypic divergence of (a) the proportion of sperm-producing tissue, (b) maximum follicle cross-sectional area and (c) body mass over time. ………………………………………………………………………………………………... 129 Figure 3.3: Relationships between testes mass corrected for body size (a proxy measure for sperm competition risk) and (a) the percentage of sperm-producing tissue within the testes and (b) maximum cross-sectional area of the seminiferous follicles across shark (black points) and ray (white points) species. …………………… 131 Chapter 4: Sexual selection drives divergent patterns of selection on sperm flagellum length in sharks and rays Figure 4.1: Sperm collection and variation in sperm morphology across sharks and rays. ………………………………………………………………………………………………………………….. 159 Figure 4.2: Associations between sperm morphological traits (plotted on a log- scale) and body size corrected testes mass, a proxy measure for sperm competition risk, in sharks (black points) and rays (white points) …………………………………………. 160 Figure 4.3: Rates of phenotypic evolution of sperm components in (a) sharks and (b) rays and (c) all elasmobranch species in our dataset. ……………………………………….. 164 7 Chapter 5: The evolution of weaponized genitals in sharks Figure 5.1: Variation in shark clasper morphology. …………………………………………… 196 Figure 5.2: Stochastic posterior probability density map of the presence or absence of clasper appendages in shark species, calculated from 1000 simulated phylogenies under an ‘all rates different’ (ARD) model of transitition probabilities. ……………. 203 Figure 5.3: Relationships between body length and clasper length (plotted on a log10-scale) across shark species, in species for which genital appendages are present (white points) and absent (black points) ……………………………………………... 208 Chapter 6: General conclusion No figures. 8 List of tables Chapter 1: General introduction No tables. Chapter 2: Testes size increases with sperm competition risk and intensity in bony fish and sharks Table 2.1: Phylogenetically controlled generalised least squares (PGLS) regressions between testes size and sperm competition risk/intensity …………………………………. 84 Table S2.1: Multiple paternity, body size and testes data collected for all n=34 fish species used in our analyses. ………………………………………………………………………………. 96 Chapter 3: Sperm competition and the evolution of testes organisation in sharks and rays Table 3.1: Evaluation of phylogenetic signal in the proportion of sperm-producing tissue within the testes and maximum cross-sectional area of the seminiferous follicles. …………………………………………………………………………………………………………..… 127 Table 3.2: Summary of model fits for Brownian motion (BM), single stationary peak (SSP, or single-optimum Ornstein-Uhlenbeck (OU) model), and accelerating/decelerating, where the change in rate is either exponential (ACDC exponential) or linear (ACDC linear), models of evolution for the percentage of seminiferous tissue within the testes (% Seminiferous tissue), the maximum cross- sectional area of the seminiferous follicles (Maximum follicle area), and adult body mass. ………………………………………………………………………….…………………………………….. 128 Table 3.3: Phylogenetically controlled linear regressions between testes organisation traits and testes mass in (a) sharks and (b) rays. ………………………….. 130 9 Table S3.1: Testes mass (g), body mass (g), mean percentage of sperm-producing tissue within the testes and maximum seminiferous follicle cross-sectional area for 18 shark and ray
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