University of Wollongong Research Online

University of Wollongong Thesis Collection 1954-2016 University of Wollongong Thesis Collections

2008

The evolution of colour polymorphism in the painted dragon, pictus

Mo Healey University of Wollongong

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Recommended Citation Healey, Mo, The evolution of colour polymorphism in the painted dragon, Ctenophorus pictus, PhD thesis, School of Biological Sciences, University of Wollongong, 2008. http://ro.uow.edu.au/theses/71

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Abstract

Abstract: Many studies of colour polymorphism across a range of taxa have shown that morphs proliferate by operating different reproductive tactics. To investigate whether this is the case with our model , the Australian painted dragon Ctenophorus pictus, we characterised a number of morph-specific traits. We demonstrate that red-headed males beat yellow-headed males in staged contests for females and that this is linked to what appears to be a convention of red dominance in male-male interactions set very early in ontogeny, long before colouration has developed. Red dominance was also observed in the field, where red males have territories with higher perch density and begin their territory defense three weeks before yellow males in some years. Red males also have higher testosterone levels than yellow males, which may provide a potential proximate link to the behavioural differences between them. In female choice experiments on single males of different colours, females did not preferentially associate with a particular morph. However, when females were allowed to choose between pairs of males of the same versus different colours, they preferred to associate with male pairs that were polymorphic. We suggest that this may be the result of selection arising from polyandrous mating benefits and show experimentally that polyandry results in increased hatching success. Sperm competition trials in the lab showed that although yellow males copulated for a shorter period of time, they sired three times as many offspring as red males. Our mating experiments also showed that yellow males had significantly larger testes in relation to body condition than red males and that sperm storage played a highly significant role in male reproductive success. These morph-specific differences are indicative of different reproductive strategies, with red males being more coercive or better mate guarders than yellow males, whilst yellow males may employ a sneaker type strategy to gain matings. However, we could not verify the distinct differences in morph-specific reproductive tactics in the wild that we would have predicted from our trials in captivity. For example, inherent red dominance could result in yellow males being marginalised to poorer quality territories in terms of access to females, food, perch sites or shade. However, with a territory acquisition experiment in the wild, we found no significant effect of colour category per se, although on average red males

1 Abstract

remained closer to the release sites (our proxy for territory acquisition ability) than yellow males. We would also predict ongoing disruptive selection on space use, with red males defending well-defined territories and yellow males having larger and more loosely defined territories. Selection analysis showed that selection on space use in a natural population was not disruptive in either of the two years studied. Thus, divergence of male reproductive strategies in our model species does not seem to be related to differences in space use or territoriality. If yellow males employ a sneaker strategy, we would expect them to sire more offspring per copulation and have a greater proportion of offspring from clutches with mixed paternity. However, we show that the frequency of mixed paternity in the wild is low (< 20 %), and that all morphs on average have the same number of offspring sired per year. A contributing factor to this difference in results could be habitat constraints on the evolution and expression of morph-specific behaviour and their evolutionary divergence in painted dragons. Habitat heterogeneity in our population (along a man- made fire trail) may be too low to allow each morph to exploit their optimal strategies, and we show that polyandry is significantly more common on territories where vigilance opportunities are relatively poorer. Painted dragons are also polymorphic in bib colour. Red males with a bib are in better body condition than red males that lack a bib, which contrasts sharply to yellow males, in which males with a bib are in poorer condition than yellow males that lack a bib. In a field experiment we found that males without a bib lost within- clutch paternity significantly more often to rivals than bibbed males. We increased the work load of males and compared ‘loaded’ males against controls with respect to how they maintained body mass during the mating season. Unexpectedly, bibbed males consistently lost more body weight across all treatments and controls. Thus, higher quality signalers may be more efficient at converting signals into fitness, in spite of higher marginal costs. During the last three months we have managed to stimulate cryptic females to express their underlying colouration using testosterone implants, and we are currently collecting data that could allow us to elucidate the genetic inheritance of this fascinating colour polymorphism.

2 Acknowledgements

Acknowledgements: Blimey, where do I start when it comes to saying thank you to all the people who have contributed to the existence of this thesis? I should begin at the beginning, with my super, supervisor, mentor, slave driver, supporter, genius and friend, Mats Olsson. Thank you for inspiring, motivating, teaching and pushing me to become more than I thought I could be. I also want to thank Rick Shine, because he started the proverbial sphere in motion to begin with by indulging a cocky pommy woman with no funding and a somewhat obsessive nature for long enough to introduce me to Mats. The other key person is my wonderful sister, Sue, who is always there for me and has been standing next to me on many occasions when I have needed her warmth, wise words and endless support, thanks Sue you’re ace. Big kisses to our Mark and our Alan, and all the Healey clan, especially my gorgeous niece Penny who inspires me with her strength in the face of a challenge. I also got loads of support and love and laughs from a group of brilliant friends, especially Nat, Kym, Frenchie, Lozza, Col and Damo, Craig and Monica and the precious bump, Tanya, Marty and Ali, Nic, Bec, all the quiz team and Mils and Zec, I love the lot of yerse. Thanks to the rest of the crew in the Olsson lab, for laughs, discussion, great dinner parties and too much cake and coffee, Bea and Thomas, Troy, James and the gigglers and Tobias and Caroline. I get really sad when I think that I won’t be living out in Yathong Nature Reserve for my usual three months this year, mostly because I will miss Ern and Gerry Snaith so very much. Gerry for her gritty determination and soft heart, and Ern, who has treated me like his own, he has looked after me and worried about me and spoilt me and respected me. Without him Yathong would have been much dustier and hotter and tougher. Thanks for everything Ern, especially the ice pops on those stinkin hot days! Thanks also to Gerry Swan for being an unreal herper and teaching me how to noose like a pro and for those long days when the work load seemed insurmountable, thank you for keeping going with me and keeping those numbers up! I should also thank Parks and Wildlife for allowing me to spend so much time out in that stunningly beautiful and intensely magical place, I have been very, very privileged to be able to live and work out there. Thanks too, to all the rangers who

3 Acknowledgements have enriched Yathong quarters with many nights of cold beers, burnt sausages, tall stories and old and treasured memories. Thanks to the ARC for funding this great gig and Wollongong Uni for being a lovely place to work. I also want to acknowledge my gorgeous, funny, intriguing, noble and courageous painted dragon . So long and sorry about all that noosing. I have loved working on this amazing project, it has been a huge adventure and I have had some incredible experiences. I honestly cannot believe just how much I have learnt over this last three years and it has ignited a strong desire to learn more and more and more. At the risk of being morbid, I have to say that I wish my mum and dad were around to see this, they would be so chuffed! They would also not be surprised that the kid who annoyed everyone by constantly saying “but I think there is more to life than this” was right………

4 Table of Contents

ACKNOWLEDGEMENTS______3

ABSTRACT______1

INTRODUCTION ______8

WHAT DRIVES AND MAINTAINS THE EVOLUTION OF COLOUR POLYMORPHISM?______8 Alternative tactics and frequency dependent selction ______8 Other examples of frequency dependent selection______13 Intra-sexual selection______13 Inter- ______16 Natural selection ______13 PROXIMATE MECHANISMS ______22 Sex hormones ______22 Genetic considerations______26 Phenotypic plasticity ______28 THE STUDY SPECIES ______29 THESIS OUTLINE ______30 REFERENCES______35 CHAPTER ONE: SEEING RED: MORPH-SPECIFIC CONTEST SUCCESS, AND SURVIVAL RATES, IN A COLOUR–POLYMORPHIC AGAMID LIZARD ______53 METHODS______55 Study species ______55 Staged interactions between different coloured adult males in semi-natural enclosures _____ 56 Contest duration in re-painted adult males ______56 Colour-dependent contest success in painted sub-adult novice, males ______57 Male release experiment into the wild ______57 RESULTS______58 Staged interactions between different coloured adult males in semi-natural enclosures _____ 58 Contest duration in re-painted adult males ______58 Colour-dependent contest success in painted sub-adult, novice males ______59 Male survival in mono-versus polymorphic release triads ______59 DISCUSSION______59 ACKNOWLEDGEMENTS ______61 REFERENCES ______62 CHAPTER TWO: VARIETY IS THE SPICE OF LIFE: FEMALE LIZARDS CHOOSE TO ASSOCIATE WITH COLOUR-POLYMORPHIC MALE DYADS.______65

ABSTRACT ______65 INTRODUCTION ______65 MATERIALS AND METHODS______68 Female preference trials on single males in an enclosure in the wild ______68 Female preference trials on male dyads in the lab ______69 Female mating experiments in the laboratory: offspring viability______70 Release experiment in the wild______71 RESULTS ______72 Female preference trials on single males ______72 Female preference trials on male dyads ______72 Female mating experiments in the laboratory: offspring viability______72 Release experiment in the wild______72 DISCUSSION______73 ACKNOWLEDGEMENTS ______75 REFERENCES ______76

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CHAPTER THREE: TERRITORY ACQUISITION IN A POLYMORPHIC LIZARD–AN EXPERIMENTAL APPROACH______79

INTRODUCTION ______79 METHODS ______81 Study species ______81 Study site ______82 Field experiment on territory acquisition ______82 RESULTS ______85 Territory quality______85 Field experiment on territory acquisition ______85 DISCUSSION______89 ACKNOWLEDGEMENTS ______90 REFERENCES ______90 CHAPTER FOUR: SELECTION ON SPACE USE IN A POLYMORPHIC LIZARD______93

INTRODUCTION ______94 MATERIALS AND METHODS ______95 RESULTS AND DISCUSSION ______98 ACKNOWLEDGEMENTS ______100 REFERENCES ______100 CHAPTER FIVE: AFTERNOON T: TESTOSTERONE LEVEL IS HIGHER IN RED THAN YELLOW MALE POLYCHROMATIC LIZARDS ______102

ABSTRACT ______102 INTRODUCTION ______102 METHODS ______104 Model species ______104 Assay of Plasma Testosterone and Corticosterone ______104 RESULTS ______105 DISCUSSION______107 ACKNOWLEDGEMENTS ______109 REFERENCES ______109 CHAPTER SIX: MATING SYSTEM VARIATION AND MORPH FLUCTUATIONS IN A POLYMORPHIC LIZARD ______112

ABSTRACT ______112 INTRODUCTION ______112 MATERIALS AND METHODS______115 RESULTS ______119 DISCUSSION______125 CHAPTER SEVEN: SPERM COMPETITION IN A POLYCHROMATIC LIZARD ______131

ABSTRACT ______131 INTRODUCTION ______131 METHODS ______133 Field protocol______133 Husbandry and mating protocol ______133 Molecular paternity assignment______136 RESULTS ______137 Male body and relative testis size ______137 Male probability of paternity ______139 DISCUSSION______142 ACKNOWLEDGEMENTS ______144 REFERENCES ______144

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CHAPTER EIGHT: SONS ARE MADE FROM OLD STORES: SPERM STORAGE EFFECTS ON SEX RATIO IN A LIZARD______146

INTRODUCTION ______146 MATERIALS AND METHODS______147 Field and laboratory procedures ______148 Paternity assignment and statistical analyses ______148 RESULTS ______149 DISCUSSION ______149 CHAPTER NINE: CONDITION-DEPENDENT, MULTIPLE SIGNALLING IN AN AUSTRALIAN LIZARD ______153

ABSTRACT ______153 INTRODUCTION ______153 METHODS ______154 Field protocol______154 Statistical methods ______155 RESULTS ______155 DISCUSSION______158 ACKNOWLEDGEMENTS ______159 REFERENCES ______159 CHAPTER TEN: TESTING THE QUALITY OF A CARRIER: A FIELD EXPERIMENT ON LIZARD SIGNALERS ______159

ABSTRACT ______161 METHODS ______163 Field protocol______163 Field Experiment 2007______164 Surgical Implantation ______164 Statistical methods ______165 RESULTS ______166 Mating system and bib status in 2000 and 2005 ______166 Mass loss: effects of head color, bib, and treatment ______166 DISCUSSION______168 ACKNOWLEDGEMENTS ______170 LITERATURE CITED ______170 APPENDIX ONE: FREE RADICALS RUN IN LIZARD FAMILIES ______173

INTRODUCTION ______173 MATERIALS AND METHODS______175 RESULTS ______176 APPENDIX TWO: VITAMIN E DOES NOT ELEVATE SURVIVAL IN FREE-RANGING LIZARDS ______181

MATERIALS AND METHODS______183 RESULTS ______184 DISCUSSION ______185 ACKNOWLEDGEMENTS ______186 LITERATURE CITED ______186

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