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Curran Thesis Full.Pdf An exploration of the parallel evolution of iridescent structural colour in Heliconius butterflies Emma V. Curran A thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy The University of Sheffield Faculty of Science Department of Animal and Plant Sciences Submission Date September 2018 2 Abstract Understanding how selection interacts with genetic variation to produce biodiversity is a central theme in evolutionary biology. Many studies have taken advantage of the rich diversity of colouration in animals to tackle this, as colour is both ecologically relevant and a clearly visible phenotype. This has carried over into the ‘omics’ era, with plenty of studies addressing evolutionary questions by examining the genomics of colouration in natural populations. These studies tend to focus on discrete colour variation and pigmentation. However, most phenotypic variation is continuous, and little is known about the genetics of structural colour. Heliconius butterflies display warning colouration that boasts both striking diversity, alongside near-perfect convergence between mimetic species. Repeated evolution of pigment colour patterns is driven by the repeated use of a small set of genes. On the western slopes of the Andes, convergent iridescence has also evolved between the co-mimics Heliconius erato and Heliconius melpomene, which appears to vary continuously. In this thesis I (1) describe clinal variation in iridescence across hybrid zones between iridescent and non-iridescent subspecies of H. erato and H. melpomene and highlight a common selective agent (mimetic warning colouration), yet different migration-selection balance between the species. 2) I demonstrate a striking difference in levels of population structure between the co-mimics across their hybrid zones. However, in both species variation in iridescence is independent of population structure and is maintained by selection despite gene flow. (3) I describe the genetic architecture of iridescence in Heliconius, for the first time, using association mapping. Lack of power to estimate genetic architecture for H. melpomene prevented a thorough between-species comparison. However, I find potential evidence of overlapping genomic regions responsible for variation in iridescence. This thesis lays the groundwork for future research narrowing down the genetic underpinnings of iridescence in this system. 3 Acknowledgements First and foremost, I would like to thank my supervisor Nicola Nadeau for her unwavering support, expertise and guidance throughout the PhD. I have had the privilege of working with her from the start of her research on iridescence, and I have learnt an enormous amount in that time. It has been quite an adventure, and not only because of those 5 weeks in the jungle. I am also grateful to the other PhD students in the group, Mel Brien, who I’ve had the pleasure of being labmates with for most of my PhD, and Juan Enciso, who begun by helping us with our fieldwork in Colombia, and who is now studying in the equally exotic Sheffield. I am very fortunate to have worked on a study system with such a collaborative and adventurous spirit as the Heliconius community, whom I thank for interesting discussions and important butterflies. Our collaboration with Andrew Parnell and colleagues has been hugely enjoyable – thanks for guiding us biologists through the unfamiliar world of physics and for letting us play with cool machines. This thesis has benefitted greatly from discussions at joint meetings with the Nosil, Christin and Butlin lab groups. I am grateful to Carly Lynsdale, Sean Stankowski, and Roger Butlin for their valuable comments and discussions on various chapters of this thesis. I am also grateful to Rachel Tucker for her support during lab work. The process of carrying out a PhD can be daunting, so I feel very fortunate to have done it alongside such a brilliant group of PhD students in the department. I am grateful for their friendship and for many lost hours at Interval. I’m particularly thankful for the support of my housemates and good friends James Ord and Rob Goodsell, and also Emma Hughes and Patrick English for taking me in during the last couple of months of my PhD, and for making a stressful time an awful lot easier. Finally, I am grateful for my family and their endless encouragement and support (be it emotional, financial, Sunday dinner related, or otherwise), and without whom none of this would have been possible. 4 Table of Contents Abstract ......................................................................................................................................... 3 Acknowledgements ...................................................................................................................... 4 1: General Introduction ............................................................................................................... 8 1.1 Genetics of colour patterns in natural populations ............................................................ 9 1.1.1 Structural colouration ................................................................................................. 10 1.1.1 Continuous colour variation ....................................................................................... 12 1.2 Repeated evolution.......................................................................................................... 14 1.3 The Heliconius butterflies ............................................................................................... 16 1.4 Outline of thesis chapters ................................................................................................ 20 1.5 A note on contributions made to this thesis ................................................................... 21 1.6 Appendices ...................................................................................................................... 22 2: Clines in iridescent structural colour in the Müllerian mimics Heliconius erato and Heliconius melpomene ................................................................................................................ 23 2.1 Summary ........................................................................................................................ 23 2.2 Introduction ..................................................................................................................... 24 2.3 Materials and methods ................................................................................................... 27 2.3.1 Collection of butterfly samples ................................................................................... 27 2.3.2 Phenotypic measurements ........................................................................................... 31 2.3.3 Estimation of ‘yellow bar’ allele frequencies ............................................................ 33 2.3.4 Geographic cline analysis .......................................................................................... 34 2.3.5 Estimating strength of selection .................................................................................. 36 2.4 Results ............................................................................................................................. 37 2.4.1 Phenotypic variation .................................................................................................. 37 2.4.2 Geographic cline analysis .......................................................................................... 41 2.4.3 Estimating strength of selection .................................................................................. 48 2.5 Discussion ....................................................................................................................... 49 2.6 Conclusions ..................................................................................................................... 54 3: Quantitative trait divergence is independent of genetic structure across parallel hybrid zones in Heliconius erato and Heliconius melpomene ............................................................ 56 3.1 Summary ........................................................................................................................ 56 3.2 Introduction ..................................................................................................................... 57 3.3 Materials and methods ................................................................................................... 60 3.3.1 Butterfly specimens ..................................................................................................... 60 3.3.2 Sequencing data .......................................................................................................... 61 3.3.3 Population structure ................................................................................................... 62 3.3.4 Population differentiation .......................................................................................... 63 3.3.5 Cline analysis .............................................................................................................. 64 5 3.4 Results ........................................................................................................................... 66 3.4.1 Population Structure ................................................................................................. 66 3.4.2 Genomic differentiation and isolation
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