The Evolutionary Ecology of Sex Change by David John Allsop Submitted for the Degree of Doctor of Philosophy The University of Edinburgh 2003 Contents List of Figures ..............................................................................................................1 List of Tables................................................................................................................1 Declaration ...................................................................................................................2 List of papers arising from this thesis ..........................................................................3 Acknowledgements......................................................................................................4 Abstract.......................................................................................................................6 Chapter 1. General Introduction ................................................................................7 1.1. Sex allocation...............................................................................................8 1.1.1. Fisher's Principle of equal investment .................................................9 1.1.2. Unequal sex ratios................................................................................9 1.1.3. Sex Change Theory............................................................................ 10 1.2. The Comparative Approach ....................................................................... 12 1.2.1. Allometry ........................................................................................... 13 1.2.2. Dimensionless analysis ...................................................................... 14 1.2.3. Dimensionless analysis in life history evolution................................ 14 1.2.4. Dimensionless invariants for sex change ........................................... 17 Chapter 2. Sex allocation in the sex changing marine goby Coryphopterus personatus on atoll fringing reefs. 19 2.1. Abstract ...................................................................................................... 19 2.2. Introduction................................................................................................ 20 2.3. Materials and methods ............................................................................... 23 2.3.1. Study Sites.......................................................................................... 23 2.3.2. Sample Collections & Basic Reef Ecology........................................ 23 2.3.3. Social Control of Sex Change Experiment ........................................ 26 2.3.4. Estimating Life History Variables for Natural Populations............... 26 2.3.5. Statistical analysis .............................................................................. 27 2.4. Results........................................................................................................ 28 2.4.1. Social Control of Sex Change Experiment ........................................ 29 2.4.2. Basic ecology and population density................................................ 30 2.4.3. Ecological factors and sex change ..................................................... 31 2.4.4. Sex ratio bias and the proportion of EMMs....................................... 33 2.5. Discussion .................................................................................................. 33 Chapter 3. Sex ratio evolution in sex changing animals.......................................... 37 3.1. Abstract ...................................................................................................... 37 3.2. Introduction................................................................................................ 38 3.2.1. Sex change theory .............................................................................. 40 3.3. Methods...................................................................................................... 42 3.3.1. Data collection ................................................................................... 42 3.3.2. Phylogenetic relationships ................................................................. 43 3.3.3. Statistical analyses ............................................................................. 44 3.4. Results and Discussion............................................................................... 46 3.4.1. Direction of sex change and the sex ratio .......................................... 49 3.4.2. Early maturers and the sex ratio......................................................... 52 3.4.3. Sex ratio bias: protogynous versus protandrous species.................... 55 3.5. Conclusions................................................................................................ 55 3.6. Appendix.................................................................................................... 57 Chapter 4. Constant relative age and size at sex change for sequentially hermaphroditic fish .................................................................................................... 64 4.1. Abstract ...................................................................................................... 64 4.2. Introduction................................................................................................ 65 4.3. Materials and methods ............................................................................... 67 4.3.1. Data collection ................................................................................... 67 4.3.2. Statistical analyses ............................................................................. 70 4.4. Results........................................................................................................ 72 4.4.1. Size invariant...................................................................................... 72 4.4.2. Age invariant...................................................................................... 74 4.5. Discussion .................................................................................................. 76 4.5.1. Sex change invariants in fish.............................................................. 76 4.5.2. Future directions................................................................................. 79 4.6. Conclusions................................................................................................ 79 4.7. Appendix.................................................................................................... 81 Chapter 5. Dimensionless invariants for the timing of gender switch in sex changing animals........................................................................................................ 84 5.1. Abstract ...................................................................................................... 84 5.2. Introduction................................................................................................ 85 5.3. Methodology .............................................................................................. 86 5.3.1. Data collection ................................................................................... 86 5.3.2. Statistical analyses ............................................................................. 87 5.4. Results and Discussion............................................................................... 88 5.5. Conclusions................................................................................................ 93 Chapter 6. General Discussion................................................................................. 94 6.1. Selection for sex change and alternative reproductive strategies............... 94 6.2. Sex ratio evolution for sex changers .......................................................... 95 6.3. Dimensionless Invariants for sex change................................................... 96 6.4. Concluding remarks ................................................................................... 99 Bibliography ........................................................................................................... 100 Appendix – published papers................................................................................ 117 The Evolutionary Ecology of Sex Change List of Figures Figure 1-1. The size advantage model for sex change............................................... 11 Figure 1-2. Average adult lifespan (E) versus age at maturity (a) for several taxa. .. 16 Figure 1-3. Adult body size distribution for male and female Pseudoanthias squamipinnis. ..................................................................................................... 17 Figure 2-1. Map of study area. The Belize Barrier Reef is demarked by the string of small islands (running N – S) to the west of the atolls. Study atolls are outlined in bold. ............................................................................................................... 24 Figure 2-2. Sex-size distribution for whole study population of C. personatus collected on atoll fringing reefs in Belize. Left of figure = frequency distribution, Right of figure = proportion male. Note the large overlap in size distribution between the two sexes. ................................................................... 28 Figure 2-3. Sex change is mediated by social environment (sex ratio) in a laboratory experiment.........................................................................................................