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The gene cortex controls mimicry and crypsis in butterflies and moths

Abstract

The wing patterns of butterflies and moths (Lepidoptera) are diverse and striking examples of evolutionary diversification by natural selection1,2. Lepidopteran wing colour patterns are a key innovation, consisting of arrays of coloured scales. We still lack a general understanding of how these patterns are controlled and whether this control shows any commonality across the 160,000 moth and 17,000 butterfly species. Here, we use fine-scale mapping with population genomics and gene expression analyses to identify a gene, cortex, that regulates pattern switches in multiple species across the mimetic radiation in Heliconius butterflies. cortex belongs to a fast-evolving subfamily of the otherwise highly conserved fizzy family of cell-cycle regulators3, suggesting that it probably regulates pigmentation patterning by regulating scale cell development. In parallel with findings in the peppered moth (Biston betularia)4, our results suggest that this mechanism is common within Lepidoptera and that cortex has become a major target for natural selection acting on colour and pattern variation in this group of insects.

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Figure 1: A homologous genomic region controls a diversity of phenotypes across the Lepidoptera.
Figure 2: Association analyses across the genomic region known to contain major colour pattern loci in Heliconius.
Figure 3: Differential gene expression across the genomic region known to contain major colour pattern loci in H. melpomene.
Figure 4: In situ hybridizations of cortex in hindwings of final instar larvae.

Accession codes

Primary accessions

European Nucleotide Archive

GenBank/EMBL/DDBJ

Gene Expression Omnibus

NCBI Reference Sequence

Data deposits

Short read sequence data generated for this study are available from ENA (http://www.ebi.ac.uk/ena) under study accession PRJEB8011 and PRJEB12740 (see Supplementary Table 1 for previously published data accessions). The updated Cr contig is deposited in Genbank with accession KC469893.2. The assembled H. melpomene fosmid sequences are deposited in Genbank with accessions KU514430KU514438. The microarray data are deposited in GEO with accessions GSM1563402GSM1563497.

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Acknowledgements

We thank C. Saski for assembly of the H. erato BACs; M. Abanto and A. Tapia for assistance with raising butterflies; M. Chouteau, J. Morris and K. Dasmahapatra for providing larvae for in situ hybridizations; A. Morrison, R. Tetley, S. Carl and H. Wegener for assistance with laboratory work; S. Baxter for the H. melpomene fosmid libraries; and the governments of Colombia, Ecuador, Panama and Peru for permission to collect butterflies. This work was funded by a Leverhulme Trust award (RPG-2014-167), BBSRC (H01439X/1), ERC (SpeciationGenetics 339873), and NERC small project (MGF 280) grants to C.D.J., NSF grants (DEB 1257689, IOS 1052541) to W.O.M., an ERC starting grant (StG-243179) to M.J. and French National Agency for Research (ANR) grants to M.J. (ANR-12-JSV7-0005) and V.L. (ANR-13-JSV7-0003-01). N.J.N. is funded by a NERC fellowship (NE/K008498/1).

Author information

Authors and Affiliations

Authors

Contributions

N.J.N. performed the association analyses, 5′ RACE, RT–PCR and qRT–PCR and prepared the manuscript. N.J.N. and C.D.J. co-ordinated the research. C.P.-D. performed and analysed the microarray and RNA-seq experiments. A.W. performed the H. numata association analysis. M.A.S. assembled and annotated the HeCr BAC reference and the H. erato alignments. S.V.S. performed in situ hybridizations. R.W.R.W. performed the transgenic experiments and analysis of de novo assembled sequences and fosmids together with J.J.H. G.C.W. and L.F. initially identified splicing variants of cortex. L.M. performed crosses between H. melpomene races. H.H. screened the HeCr BAC library. C.S. and R.M.M. provided samples. A.J.D. contributed to the H. melpomene BAC sequencing and annotation. R.H.f.-C., M.J., V.L., W.O.M. and C.D.J. are PIs who obtained funding and led the project elements. All authors commented on the manuscript.

Corresponding authors

Correspondence to Nicola J. Nadeau or Chris D. Jiggins.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 H. melpomene race-associated cortex splicing variation.

a, Exons and splice variants of cortex in H. melpomene. Orientation is reversed with respect to Figs 2 and 4, with transcription going from left to right. SNPs showing the strongest associations with phenotype are shown with stars. b, Differential expression of two regions of cortex between whole hindwings of H. melpomene amaryllis and H. melpomene aglaope (n = 11 and n = 10, respectively). Box plots are standard (median; seventy-fifth and twenty-fifth percentiles; maximum and minimum excluding outliers (shown as discrete points)). ***P < 0.0001, *P < 0.05, Wilcoxon rank sum test. c, Expression of a cortex isoform lacking exon 3 is found in H. melpomene aglaope but not H. melpomene amaryllis hindwings. d, Expression of an isoform lacking exon 5 is found in H. melpomene rosina but not H. melpomene melpomene hindwings. Green triangles indicate predicted start codons and red triangles predicted stop codons, with usage dependent on which exons are present in the isoform. Schematics of the targeted exons are shown for each (q)RT–PCR product; black triangles indicate the positions of the primers used in the assay.

Source data

Extended Data Figure 2 Alignments of de novo assembled fragments containing the top associated SNPs from H. melpomene and related taxa short-read data.

Identified indels do not show stronger associations with phenotype that those seen at SNPs (as shown in Extended Data Table 2), although some near-perfect associations are seen in fragment C. Black regions, missing data; yellow boxes, individuals with a yellow hindwing bar; blue boxes, individuals with a yellow forewing band.

Extended Data Figure 3 Sequencing of long-range PCR products and fosmids spanning cortex.

a, Sequence read coverage from long-range PCR products across the cortex coding region from two H. melpomene races. b, Minor allele frequency difference from these reads between H. melpomene aglaope and H. melpomene amaryllis. Exons of cortex are indicated by boxes, numbered as in Extended Data Fig. 2. c, Alignments of sequenced fosmids overlapping cortex from three H. melpomene (H. m.) individuals of difference races. No major rearrangements are observed, nor any major differences in transposable element (TE) content between closely related races with different colour patterns (melpomene/rosina or amaryllis/aglaope). H. melpomene amaryllis and rosina have the same phenotype, but do not share any transposable elements that are not present in the other races. Hm_BAC, BAC reference sequence; Hm_mel, melpomene from new unpublished assembly of H. melpomene genome51; Hm_ros, rosina (two different alleles were sequenced from this individual); Hm_ama, amaryllis (two non-overlapping clones were sequenced from this individual); Hm_agla, aglaope (four clones were sequenced from this individual, of which two represent alternative alleles). Alignments were performed with Mauve;coloured bars represent homologous genomic regions. cortex is annotated in black above each clone. Variable transposable elements are shown as coloured bars below each clone: red, Metulj-like non-LTR; yellow, Helitron-like DNA; grey, other.

Extended Data Figure 4 Expression array results for additional stages.

Array results are related to Fig. 4. ag, Comparisons between races (H. melpomene plesseni and H. melpomene malleti) for three wing regions. hn, Comparisons between proximal and distal forewing regions for each race. Significance values (−log10P) are shown separately for genes in the HmYb region from the gene array (a, d, f, h, k, m) and for the HmYb tiling array (b, e, g, i, l, n) for day 1 (a, b, h, i), day 5 (d, e, k, l) and day 7 (f, g, m, n) after pupation. The level of expression difference (log fold change) for tiling probes showing significant differences (P ≤ 0.05) is shown for day 1 (c and j) with probes in known cortex exons shown in dark colours and probes elsewhere shown as pale colours. P values are based on FDR-adjusted t-statistics.

Source data

Extended Data Figure 5 Alternative splicing of cortex.

a, Amplification of the whole cortex coding region, showing the diversity of isoforms and variation between individuals. b, Differences in splicing of exon 3 between H. melpomene aglaope and H. melpomene amaryllis. Products amplified with a primer spanning the exon 2–4 junction at three developmental stages. The lower panel shows verification of this assay by amplification between exons 2 and 4 for the same final instar larval samples (replicated in Extended Data Fig. 2c). c, Lack of consistent differences between H. melpomene melpomene and H. melpomene rosina in splicing of exon 3. Top panel shows products amplified with a primer spanning the exon 2–4 junction; lower panel shows the same samples amplified between exons 2 and 4. d, Differences in splicing of exon 5 between H. melpomene melpomene and H. melpomene rosina. Products amplified with a primer spanning the exon 4–6 junction at three developmental stages. e, Subset of samples from d amplified with primers between exons 4 and 6 for verification (middle, 24-h pupae samples are replicated in Extended Data Fig. 2d). f, Lack of consistent differences between H. melpomene aglaope and H. melpomene amaryllis in splicing of exon 5. Products amplified with a primer spanning the exon 4–6 junction. g, H. melpomene cythera also expresses the isoform lacking exon 5, while a pool of six H. melpomene malleti individuals do not. h, Expression of the isoform lacking exon 5 from an F2 H. melpomene melpomene × H. melpomene rosina cross. Individuals homozygous or heterozygous for the H. melpomene rosina HmYb allele express the isoform while those homozygous for the H. melpomene melpomene HmYb allele do not. i, Allele-specific expression of isoforms with and without exon 5. Heterozygous individuals (indicated with blue and red stars) express only the H. melpomene rosina allele in the isoform lacking exon 5 (G at highlighted position), while they express both alleles in the isoform containing exon 5 (G/A at this position).

Extended Data Figure 6 Phylogeny of fizzy family proteins and effects of expressing cortex in the Drosophila wing.

a, Neighbour joining phylogeny of fizzy family proteins including functionally characterized proteins (in bold) from Saccharomyces cerevisiae, Homo sapiens and D. melanogaster as well as copies from the basal metazoan Trichoplax adhaerens and a range of annotated arthropod genomes (Daphnia pulex, Acyrthosiphon pisum, Pediculus humanus, Apis mellifera, Nasonia vitripennis, Anopheles gambiae and Tribolium castaneum) including the lepidoptera H. melpomene (in blue), D. plexippus and B. mori. Branch colours: dark blue, cdc20/fzy; light blue, rap; red, lepidopteran cortex. be, Ectopic expression of cortex in D. melanogaster. Drosophila cortex produces an irregular microchaete phenotype when expressed in the posterior compartment of the fly wing (c) whereas Heliconius cortex does not (d), when compared to no expression (b). A, anterior; P, posterior. Successful Heliconius cortex expression was confirmed by anti-HA immunohistochemistry in the last instar Drosophila larva wing imaginal disc (e, red), with DAPI staining in blue.

Extended Data Table 1 Genes in the Yb region and evidence for wing patterning control in Heliconius
Extended Data Table 2 Locations of fixed or above-background SNPs and differentially expressed (DE) tiling array probes
Extended Data Table 3 SNPs showing the strongest phenotypic associations in the H. melpomene/timareta/silvaniform comparison
Extended Data Table 4 Transposable elements (TEs) found within the Yb region

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Supplementary Information

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Supplementary Table 1

This file contains information on all individuals genotyped for the genotype-by-phenotype association analyses and study accessions for sequence read data. (XLSX 35 kb)

Supplementary Table 2

This file contains the information on all primers used. (XLSX 11 kb)

Supplementary Data 1

This file shows the alignment of fizzy family protein amino acid sequences, used to generate Extended Data Figure 6. (PDF 137 kb)

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Nadeau, N., Pardo-Diaz, C., Whibley, A. et al. The gene cortex controls mimicry and crypsis in butterflies and moths. Nature 534, 106–110 (2016). https://doi.org/10.1038/nature17961

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