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The Genetics and Evolution of Iridescent Structural Colour in Heliconius Butterflies

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The Genetics and Evolution of Iridescent Structural Colour in Heliconius Butterflies The genetics and evolution of iridescent structural colour in Heliconius butterflies Melanie N. Brien 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 & Plant Sciences Submission Date August 2019 1 2 Abstract The study of colouration has been essential in developing key concepts in evolutionary biology. The Heliconius butterflies are well-studied for their diverse aposematic and mimetic colour patterns, and these pigment colour patterns are largely controlled by a small number of homologous genes. Some Heliconius species also produce bright, highly reflective structural colours, but unlike pigment colour, little is known about the genetic basis of structural colouration in any species. In this thesis, I aim to explore the genetic basis of iridescent structural colour in two mimetic species, and investigate its adaptive function. Using experimental crosses between iridescent and non-iridescent subspecies of Heliconius erato and Heliconius melpomene, I show that iridescent colour is a quantitative trait by measuring colour variation in offspring. I then use a Quantitative Trait Locus (QTL) mapping approach to identify loci controlling the trait in the co-mimics, finding that the genetic basis is not the same in the two species. In H. erato, the colour is strongly sex-linked, while in H. melpomene, we find a large effect locus on chromosome 3, plus a number of putative small effect loci in each species. Therefore, iridescence in Heliconius is not an example of repeated gene reuse. I then show that both iridescent colour and pigment colour are sexually dimorphic in H. erato and H. sara, pointing to differing selection pressures on the sexes. Structural colour, and to a lesser extent pigment colour, are condition dependent, suggesting the trait could be used as a signal of condition in mate choice. Together this work provides an understanding of the evolution of structural colour in Heliconius, in terms of its genetic control and its function as a signal and mimetic warning pattern. 3 Acknowledgements Firstly, I would like to thank my supervisor Nicola Nadeau for the opportunity to work on this project and for her ongoing support and guidance for more than four years. It has been an amazing project to be involved with, in no small part due to her supervision, and I have learnt so much. Thanks to my wonderful fellow lab members, Emma Curran, Juan Enciso-Romero and Vicky Lloyd, for making this project so enjoyable and for many breaks for cake during thesis writing. I am fortunate to be part of a supportive group of PhD students in the Animal & Plant Sciences department, and to have friends in Sheffield and further afield who are always willing to help, or just go to the pub. A large part of this thesis was possible thanks to Patricio Salazar and Carlos Morochz, who organised field work in Mashpi, and Gabriela Montejo-Kovacevich who allowed me to join her field trip across Ecuador. I am grateful to Andrew Parnell for sharing his expertise and ideas for the physics side of the project, and to Jon Slate, Roger Butlin and Pasi Rastas who all gave useful advice on analyses. Finally, thank you to my family for their endless support on this career path, especially when I said I was going to live in a jungle for three months. 4 Table of Contents Abstract ........................................................................................................................................ 3 Acknowledgements ...................................................................................................................... 4 1. General Introduction .............................................................................................................. 9 1.1 The study of structural colouration: mechanisms and functions ......................................... 9 1.2 Sexual selection and condition dependence of colour traits.............................................. 13 1.3 Structural colour in the Heliconius butterflies .................................................................. 15 1.4 Repeatability of colour pattern genetics ............................................................................ 19 1.5 Outline of thesis ................................................................................................................ 21 1.6 Contributions made to this thesis ...................................................................................... 22 2. Using phenotypic variation in crosses to explore the genetic basis of iridescent colour in Heliconius erato and Heliconius melpomene ........................................................................... 23 2.1 Summary ........................................................................................................................... 23 2.2. Introduction ...................................................................................................................... 24 2.3 Methods ............................................................................................................................. 27 2.3.1 Crossing Experiments ................................................................................................ 27 2.3.2 Phenotypic Analysis ................................................................................................... 29 2.4 Results ............................................................................................................................... 32 2.4.1 Colour variation in Heliconius erato ......................................................................... 32 2.4.2 Colour variation in Heliconius melpomene ............................................................... 39 2.5 Discussion ......................................................................................................................... 45 2.6 Supplementary Information .............................................................................................. 49 3. Investigating the genetic basis of iridescent structural colour in the co-mimics Heliconius erato and Heliconius melpomene using Quantitative Trait Locus mapping ..................................................................................................................................................... 53 3.1 Summary ........................................................................................................................... 53 3.2 Introduction ....................................................................................................................... 54 3.3 Methods ............................................................................................................................. 57 3.3.1 Experimental cross design and phenotyping .............................................................. 57 3.3.2 DNA extraction and sequencing ................................................................................. 59 3.3.3 Sequence data processing .......................................................................................... 59 3.3.4 Genetic map construction .......................................................................................... 60 3.3.5 Quantitative Trait Locus mapping ............................................................................. 61 3.4 Results ............................................................................................................................... 63 3.4.1 Genetic map construction .......................................................................................... 63 5 3.4.2 Mapping Cr and Yb/Sb genotypes .............................................................................. 65 3.4.3 QTL scans for iridescent colour in H. erato .............................................................. 67 3.4.4 QTL scans for iridescent colour in H. melpomene .................................................... 72 3.4.5 Comparison of maternal alleles ................................................................................. 77 3.5 Discussion ......................................................................................................................... 80 3.6 Supplementary Information .............................................................................................. 85 4. Condition dependence and sexual dimorphism of Heliconius structural and pigment colour ........................................................................................................................................ 103 4.1 Summary ......................................................................................................................... 103 4.2 Introduction .................................................................................................................... 104 4.3 Methods .......................................................................................................................... 107 4.3.1 Butterfly specimens .................................................................................................. 107 4.3.2 Thermal stress experiments ...................................................................................... 108 4.3.3 Optical Reflectance Spectroscopy ............................................................................ 108 4.3.4 Analysis of spectral data .......................................................................................... 110 4.3.5
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