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The Repeatability of Evolution; Colour Pattern Control in Heliconius Butterflies

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The Repeatability of Evolution; Colour Pattern Control in Heliconius Butterflies The repeatability of evolution; colour pattern control in Heliconius butterflies Jake Morris Doctor of Philosophy University of York Biology December, 2016 Abstract Heliconius butterflies are found across the neo-tropics, with bright aposematic colour patterns. These Müllerian mimics show striking colour pattern convergence across species, while paradoxically showing striking diversity within species. Thus Heliconius wing patterns have become an excellent system for understanding the repeatability of evolution. This work has identified a number of genes that appear to be involved in colour pattern control across species, such as optix and cortex, which respectively control red and yellow pattern elements. However, this work has only looked at the genetic basis of colour pattern in a small number of species, and primarily focuses on just two; H. melpomene and H. erato. I first use a population genomics approach to try to identify whether optix controls the hindwing rays phenotype in two poorly studied species; H. demeter and H. aoede. I identify both divergence associated with colour pattern at this optix, as well as another putative colour pattern control locus in H. aoede, the ommochrome pathway gene cardinal. Further, I use Quantitative trait loci analysis to explore the genetics of colour pattern in H. melpomene, confirming WntA as the gene controlling the ‘broken band’ phenotype and I identify a locus associated with red-orange pigmentation, while also exploring the role of minor effect loci in quantitative colour pattern variation. Finally, I use the natural diversity at two hybrid zones, in conjunction with phylogenetic discordance at mimicry loci, to identify putative regulatory enhancers associated with colour pattern shifts, investigate introgression across species at this fine genetic scale, and the possible role of colour pattern introgression in Heliconius speciation. This work reveals both interesting cases of convergent genetic evolution, independent genetic evolution and introgression, showing that a variety of evolutionary processes have shaped Heliconius mimicry across species. 2 Contents Abstract ........................................................................................................................................................ 2 Contents ....................................................................................................................................................... 3 List of tables ............................................................................................................................................... 7 List of figures ............................................................................................................................................. 8 Acknowledgments ............................................................................................................................... 12 Declaration .............................................................................................................................................. 14 1. Heliconius: colour pattern diversity and convergence ........................................... 15 1.1.1 Evolution: progress and paradigms ........................................................................ 15 1.1.2 Rapid improvements in technology ........................................................................ 16 1.1.3 Expanding model species .......................................................................................... 17 1.2 Convergent evolution........................................................................................................ 18 1.2.1 Convergent genetic evolution ................................................................................. 18 1.2.2 Parallel evolution: a special case of convergence ................................................ 20 1.2.3 Introgression ............................................................................................................... 21 1.3 The Heliconius radiation .................................................................................................... 22 1.3.1 Ecology and mimicry.................................................................................................. 22 1.3.2 The Nymphalid groundplan ..................................................................................... 24 1.3.3 Convergent genetics of Heliconius wing patterns ................................................ 25 1.3.4 Modulation of mimicry .............................................................................................. 27 1.3.5 Heliconius mimicry and speciation with gene flow .............................................. 29 1.4 Conclusion ........................................................................................................................... 30 2. Population genomics of a multi-species mimetic hybrid zone .......................... 32 2.1 Introduction ......................................................................................................................... 32 2.2 Methodology ........................................................................................................................ 38 2.2.1 Test dataset ................................................................................................................. 38 3 2.2.2 De novo assembly ........................................................................................................ 39 2.2.3 Finding fixed differences ........................................................................................... 40 2.2.4 De novo assembly quality metrics............................................................................ 41 2.2.5 H. aoede and H. demeter sample collection and sequencing ............................. 41 2.2.6 De novo assembly analyses ........................................................................................ 42 2.2.7 Reference genome analyses ..................................................................................... 42 2.2.8 Fixed differences across analyses ........................................................................... 43 2.2.9 Permutation tests of significance ............................................................................ 44 2.2.10 Short range PCR amplicon sequencing ................................................................. 44 2.2.11 Characterising regions of divergence .................................................................... 47 2.3 Results ................................................................................................................................... 48 2.3.1 H. melpomene test dataset analyses ........................................................................ 48 2.3.2 Divergence across the Heliconius aoede genome ................................................ 51 2.3.3 Divergence across the Heliconius demeter genome ............................................ 54 2.3.4 Short range PCR amplicon sequencing ................................................................. 57 2.3.5 Characterising regions of divergence .................................................................... 61 2.4 Discussion ............................................................................................................................ 67 2.4.1 Patterns of divergence .............................................................................................. 67 2.4.2 Cardinal; ancient gene, novel function? .................................................................. 70 2.4.3 Repeated evolution at the rays locus ..................................................................... 73 2.4.4 Conservation across subspecies ............................................................................. 73 2.4.5 Serine proteases ......................................................................................................... 74 2.4.6 Conclusion ................................................................................................................... 75 3. The genetics of diversity: the dennis-rayed mimicry ring of H. melpomene 77 3.1 Introduction ......................................................................................................................... 77 3.2 Methodology ........................................................................................................................ 83 3.2.1 Crossing experiments ............................................................................................... 83 3.2.2 Sample preservation and sequencing ..................................................................... 83 3.2.3 Segregation of phenotypic variation....................................................................... 84 4 3.2.4 Forewing band shape ................................................................................................. 85 3.2.5 Linkage map construction ........................................................................................ 86 3.2.6 QTL analysis ................................................................................................................ 89 3.3 Results ................................................................................................................................... 92 3.3.1 Segregation of phenotypic variation....................................................................... 92 3.3.2 The linkage map .........................................................................................................
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