The Gene Cortex Controls Mimicry and Crypsis in Butterflies and Moths Nicola J

Letter doi:10.1038/nature17961 The gene cortex controls mimicry and crypsis in butterflies and moths Nicola J. Nadeau1,2, Carolina Pardo-Diaz3, Annabel Whibley4,5, Megan A. Supple2,6, Suzanne V. Saenko4, Richard W. R. Wallbank2,7, Grace C. Wu8, Luana Maroja9, Laura Ferguson10, Joseph J. Hanly2,7, Heather Hines11, Camilo Salazar3, Richard M. Merrill2,7, Andrea J. Dowling12, Richard H. ffrench-Constant12, Violaine Llaurens4, Mathieu Joron4,13, W. Owen McMillan2 & Chris D. Jiggins2,7 The wing patterns of butterflies and moths (Lepidoptera) are pattern elements across many individuals from a wide diversity of diverse and striking examples of evolutionary diversification by colour pattern phenotypes (Fig. 2). natural selection1,2. Lepidopteran wing colour patterns are a key In three separate Heliconius species, our analysis consistently impli- innovation, consisting of arrays of coloured scales. We still lack a cated the gene cortex as being involved in adaptive differences in wing general understanding of how these patterns are controlled and colour pattern. In H. erato the strongest associations with the presence whether this control shows any commonality across the 160,000 of a yellow hindwing bar were centred around the genomic region moth and 17,000 butterfly species. Here, we use fine-scale mapping with population genomics and gene expression analyses to identify HeCr a gene, cortex, that regulates pattern switches in multiple species H. erato favorinus demophoon notabilis hydara emma lativita erato across the mimetic radiation in Heliconius butterflies. cortex belongs to a fast-evolving subfamily of the otherwise highly 3 amaryllis rosina bellula vulcanus cythera plesseni conserved fizzy family of cell-cycle regulators , suggesting that it H. HmYb probably regulates pigmentation patterning by regulating scale melpomene HmN cell development. In parallel with findings in the peppered moth amandus aglaope malleti thelxiopeia melpomene (Biston betularia)4, our results suggest that this mechanism is H. timareta common within Lepidoptera and that cortex has become a major thelxinoe timareta ﬂorencia target for natural selection acting on colour and pattern variation Other in this group of insects. silvaniforms H. pardalinus H. elevatus In Heliconius, there is a major effect locus, Yb, that controls a diver- HnP sity of colour pattern elements across the genus. It is the only locus H. numata in Heliconius that regulates all scale types and colours, including the silvana tarapotensis numata euphrasius elegans diversity of white and yellow pattern elements in the two co-mimics H. melpomene and H. erato, and whole-wing variation in black, yellow, illustris aurora isabellinus peeblesi arcuella bicoloratus ~100 5–7 Bigeye white, and orange/red elements in H. numata . In addition, genetic Myr variation underlying the Bigeye wing pattern mutation in Bicyclus any- Bicyclus anynana nana, melanism in the peppered moth, Biston betularia, and mela- Wild-type Bigeye carbonaria nism and patterning differences in the silkmoth, Bombyx mori, have all Biston betularia 8–10 Bm been localized to homologous genomic regions (Fig. 1). Therefore, typica carbonaria Ws this genomic region appears to contain one or more genes that act as major regulators of wing pigmentation and patterning across the Bombyx mori Lepidoptera. Previous mapping of this locus in H. erato, H. melpomene and Wild-type Bm Ws H. numata identified a genomic interval of about 1 Mb (refs 11–13) Figure 1 | A homologous genomic region controls a diversity of (Extended Data Table 1), which also overlaps with the 1.4-Mb region phenotypes across the Lepidoptera. Left, phylogenetic relationships29. containing the carbonaria locus in B. betularia9 and a 100-bp non- Right, chromosome maps with colour pattern intervals in grey; coloured 5,8–10 coding region containing the Ws mutation in B. mori10 (Fig. 1). We bars represent markers used to assign homology and the first and last used a population genomics approach to identify the single nucleotide genes from Fig. 2 are shown in red. In H. erato the HeCr locus controls the polymorphisms (SNPs) that were most strongly associated with phe- yellow hindwing bar phenotype (grey boxed races). In H. melpomene it controls both the yellow hindwing bar (HmYb, pink box) and the yellow notypic variation within the approximately 1-Mb Heliconius interval. forewing band (HmN, blue box). In H. numata it modulates black, yellow The diversity of wing patterning in Heliconius arises from divergence and orange elements on both wings (HnP), producing phenotypes that 7 at wing pattern loci , while convergent patterns generally involve the mimic butterflies in the genus Melinaea. Morphs/races of Heliconius 14–16 same loci and sometimes even the same alleles . We used this pat- species included in this study are shown with names. All images are by the tern of divergence and sharing to identify SNPs associated with colour authors or are in the public domain. 1Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN UK. 2Smithsonian Tropical Research Institute, Apartado Postal 0843-00153, Panamá, República de Panamá. 3Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Cra. 24 No 63C-69, Bogotá D.C., 111221, Colombia. 4Institut de Systématique, Evolution et Biodiversité (UMR 7205 CNRS, MNHN, UPMC, EPHE, Sorbonne Université), Museum National d’Histoire Naturelle, CP50, 57 rue Cuvier, 75005 Paris, France. 5Cell and Developmental Biology, John Innes Centre, Norwich, Norfolk NR4 7UH, UK. 6Research School of Biology, The Australian National University, 134 Linnaeus Way, Acton, ACT, 2601, Australia. 7Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK. 8Energy and Resources Group, University of California at Berkeley, California, 94720, USA. 9Department of Biology, Williams College, Williamstown, Massachusetts 01267, USA. 10Department of Zoology, University of Oxford, South Parks Rd, Oxford OX1 3PS, UK. 11Penn State University, 517 Mueller, University Park, Pennsylvania 16802, USA. 12School of Biosciences, University of Exeter in Cornwall, Penryn, Cornwall TR10 9FE, UK. 13Centre d’Ecologie Fonctionnelle et Evolutive (CEFE, UMR 5175 CNRS, Université de Montpellier, Université Paul-Valéry Montpellier, EPHE), 1919 route de Mende, 34293 Montpellier, France. 106 | NATURE | VOL 534 | 2 June 2016 © 2016 Macmillan Publishers Limited. All rights reserved LETTER RESEARCH a H. erato 8 6 P 10 4 –log 2 0 b 100 kb cortex HM00026 miRNAs HM00036 c d H. melpomene group 10 Genotype-by-phenotype association 8 P 6 10 4 –log 2 0 e 6 H. numata P 4 10 –log 2 0 inv1 inv2 Position Figure 2 | Association analyses across the genomic region known to silvaniform group with the yellow hindwing bar (red) and yellow forewing contain major colour pattern loci in Heliconius. a, Association in band (blue) (n = 49). e, Association in H. numata with the bicoloratus H. erato with the yellow hindwing bar (n = 45). Coloured SNPs are fixed morph (n = 26); inversion positions13 shown below. In all cases black or for a unique state in H. erato demophoon (orange) or H. erato favorinus dark coloured points are above the strongest associations found outside (purple). b, Genes in H. erato with direct homologues in H. melpomene. the colour pattern scaffolds (H. erato P = 1.63 × 10−5; H. melpomene Genes are in different colours with exons (coding and UTRs) connected P = 2.03 × 10−5 and P = 2.58 × 10−5 for hindwing bar and forewing band, by lines. Grey bars are transposable elements. c, H. melpomene genes and respectively; H. numata P = 6.81 × 10−6). P values are from score tests for transposable elements. Colours correspond to homologous H. erato genes association. and microRNAs30 are black. d, Association in the H. melpomene/timareta/ containing cortex (Fig. 2a). We identified 108 SNPs that were fixed for than coding. We found extensive transposable element variation one allele in H. erato favorinus, and fixed for the alternative allele in around cortex but it is unclear whether any of these are associated all individuals lacking the yellow bar; the majority of these SNPs were with phenotypic differences (Extended Data Fig. 3, Extended Data in introns of cortex (Extended Data Table 2). Fifteen SNPs showed a Table 4 and Supplementary Information). similar fixed pattern for H. erato demophoon, which also has a yellow Finally, large inversions at the P supergene locus in H. numata (Fig. 1) bar. These SNPs did not overlap with those in H. erato favorinus, con- are associated with different morphs13. There is a steep increase in sistent with the hypothesis that this phenotype evolved independently genotype-by-phenotype association at the breakpoint of inversion 1, in the two disjunct populations17. consistent with the role of these inversions in reducing recombination Previous work has suggested that alleles at the Yb locus are shared (Fig. 2e). However, the bicoloratus morph can recombine with all other between H. melpomene, the closely related species H. timareta, and morphs across one or the other inversion, permitting finer-scale asso- the more distantly related species H. elevatus, resulting in mimicry ciation mapping of this region. As in H. erato and H. melpomene, this among these species18. Across these species, the strongest associations analysis showed a narrow region of associated SNPs corresponding with the yellow hindwing bar phenotype were again found at cortex exactly to the cortex gene (Fig. 2e),

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