The origins of a novel butterfly wing patterning gene from within a family of conserved cell cycle regulators

A major challenge in evolutionary biology is to understand the origins of novel structures. The wing patterns of butterflies and moths are derived phenotypes unique to the Lepidoptera. Here we identify a gene that we name poikilomousa (poik), which regulates colour pattern switches in the mimetic Heliconius butterflies. Strong associations between phenotypic variation and DNA sequence variation are seen in three different Heliconius species, in addition to associations between gene expression and colour pattern. Colour pattern variants are also associated with differences in splicing of poik transcripts. poik is a member of the conserved fizzy family of cell cycle regulators. It belongs to a faster evolving subfamily, the closest functionally characterised orthologue being the cortex gene in Drosophila, a female germ-line specific protein involved in meiosis. poik appears to have adopted a novel function in the Lepidoptera and become a major target for natural selection acting on colour and pattern variation in this group.

[1]  M. J. Thompson,et al.  Supergenes and their role in evolution , 2014, Heredity.

[2]  Wei Zhang,et al.  doublesex is a mimicry supergene , 2014, Nature.

[3]  N. Patel,et al.  Multiple recent co-options of Optix associated with novel traits in adaptive butterfly wing radiations , 2014, EvoDevo.

[4]  Patricio A. Salazar,et al.  Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato , 2013, bioRxiv.

[5]  Simon H. Martin,et al.  Genome-wide evidence for speciation with gene flow in Heliconius butterflies , 2013, Genome research.

[6]  V. Valente,et al.  Ultrastructure and morphogenesis of the wing scales in Heliconius erato phyllis (Lepidoptera: Nymphalidae): what silvery/brownish surfaces can tell us about the development of color patterning? , 2013, Arthropod structure & development.

[7]  Camilo Salazar,et al.  Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies , 2013, Genome research.

[8]  C. Wiklund,et al.  Eyespot display in the peacock butterfly triggers antipredator behaviors in naïve adult fowl , 2012, Behavioral ecology : official journal of the International Society for Behavioral Ecology.

[9]  M. Dalíková,et al.  Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism , 2012, Heredity.

[10]  C. Jiggins,et al.  Partial Complementarity of the Mimetic Yellow Bar Phenotype in Heliconius Butterflies , 2012, PloS one.

[11]  Hongtao Yu,et al.  Structural analysis of human Cdc20 supports multisite degron recognition by APC/C , 2012, Proceedings of the National Academy of Sciences.

[12]  C. Jiggins,et al.  Adaptive Introgression across Species Boundaries in Heliconius Butterflies , 2012, PLoS genetics.

[13]  Simon H. Martin,et al.  Butterfly genome reveals promiscuous exchange of mimicry adaptations among species , 2012, Nature.

[14]  L. Cook,et al.  Selective bird predation on the peppered moth: the last experiment of Michael Majerus , 2012, Biology Letters.

[15]  James Mallet,et al.  Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  D. Barford Structural insights into anaphase-promoting complex function and mechanism , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  Robert D Reed,et al.  Wing patterning gene redefines the mimetic history of Heliconius butterflies , 2011, Proceedings of the National Academy of Sciences.

[18]  Camilo Salazar,et al.  Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry , 2011, Nature.

[19]  H. Nijhout,et al.  optix Drives the Repeated Convergent Evolution of Butterfly Wing Pattern Mimicry , 2011, Science.

[20]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[21]  Martin Goodson,et al.  Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. , 2011, Genome research.

[22]  M. Dalíková,et al.  Industrial Melanism in British Peppered Moths Has a Singular and Recent Mutational Origin , 2011, Science.

[23]  Grace C. Wu,et al.  Signatures of selection in loci governing major colour patterns in Heliconius butterflies and related species , 2010, BMC Evolutionary Biology.

[24]  Thomas J. Hardcastle,et al.  baySeq: Empirical Bayesian methods for identifying differential expression in sequence count data , 2010, BMC Bioinformatics.

[25]  G. Ast,et al.  Alternative splicing and evolution: diversification, exon definition and function , 2010, Nature Reviews Genetics.

[26]  W. Huber,et al.  which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets , 2011 .

[27]  Heiko Vogel,et al.  Characterization of a Hotspot for Mimicry: Assembly of a Butterfly Wing Transcriptome to Genomic Sequence at the Hmyb/sb Locus , 2022 .

[28]  Simon W. Baxter,et al.  Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in Heliconius erato , 2010, PLoS genetics.

[29]  Nicolien Pul,et al.  A Gene-Based Linkage Map for Bicyclus anynana Butterflies Allows for a Comprehensive Analysis of Synteny with the Lepidopteran Reference Genome , 2009, PLoS genetics.

[30]  C. Jiggins Ecological Speciation in Mimetic Butterflies , 2008 .

[31]  A. Vogler,et al.  Colour pattern specification in the Mocker swallowtail Papilio dardanus: the transcription factor invected is a candidate for the mimicry locus H , 2008, Proceedings of the Royal Society B: Biological Sciences.

[32]  T. Orr-Weaver,et al.  Developmental Role and Regulation of cortex, a Meiosis-Specific Anaphase-Promoting Complex/Cyclosome Activator , 2007, PLoS genetics.

[33]  T. Schüpbach,et al.  The Cdc20 (Fzy)/Cdh1-related protein, Cort, cooperates with Fzy in cyclin destruction and anaphase progression in meiosis I and II in Drosophila , 2007, Development.

[34]  James Mallet,et al.  A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies , 2006, PLoS biology.

[35]  A. Papanicolaou,et al.  Heliconius wing patterns: an evo-devo model for understanding phenotypic diversity , 2006, Heredity.

[36]  T. Venkatesh,et al.  rap gene encodes Fizzy-related protein (Fzr) and regulates cell proliferation and pattern formation in the developing Drosophila eye-antennal disc. , 2005, Developmental biology.

[37]  Sebastian Maurer-Stroh,et al.  The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. , 2005, Molecular cell.

[38]  C. Lehner,et al.  Completion of Mitosis Requires Neither fzr/rap nor fzr2, a Male Germline-Specific Drosophila Cdh1 Homolog , 2002, Current Biology.

[39]  M. Kirschner,et al.  Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex. , 2001, Genes & development.

[40]  Tehyen Chu,et al.  Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family , 2001, Genesis.

[41]  Durrell D. Kapan,et al.  Three-butterfly system provides a field test of müllerian mimicry , 2001, Nature.

[42]  P. Brakefield,et al.  Butterfly wing pattern mutants: developmental heterochrony and co-ordinately regulated phenotypes , 2000, Development Genes and Evolution.

[43]  W. Gehring,et al.  The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. , 2000, Development.

[44]  J. M. Scriber,et al.  GENETICS OF MIMICRY IN THE TIGER SWALLOWTAIL BUTTERFLIES, PAPILIO GLAUCUS AND P. CANADENSIS (LEPIDOPTERA: PAPILIONIDAE) , 1996, Evolution; international journal of organic evolution.

[45]  S. Artavanis-Tsakonas,et al.  The Drosophila cell cycle gene fizzy is required for normal degradation of cyclins A and B during mitosis and has homology to the CDC20 gene of Saccharomyces cerevisiae , 1995, The Journal of cell biology.

[46]  H. Nijhout,et al.  The development and evolution of butterfly wing patterns , 1991 .

[47]  J. Mallet The genetics of warning colour in Peruvian hybrid zones of Heliconius erato and H. melpomene , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[48]  N. Barton,et al.  STRONG NATURAL SELECTION IN A WARNING‐COLOR HYBRID ZONE , 1989, Evolution; international journal of organic evolution.

[49]  J. Mallet Hybrid zones of Heliconius butterflies in Panama and the stability and movement of warning colour clines , 1986, Heredity.

[50]  K. S. Brown,et al.  Genetics and the Evolution of Muellerian Mimicry in Heliconius Butterflies , 1985 .

[51]  C. Clarke,et al.  Super-genes and mimicry , 1960, Heredity.

[52]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[53]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[54]  L. Gilbert,et al.  Correlations of ultrastructure and pigmentation suggest how genes control development of wing scales of Heliconius butterflies , 1988, The Journal of Research on the Lepidoptera.

[55]  Yurii S. Aulchenko,et al.  BIOINFORMATICS APPLICATIONS NOTE doi:10.1093/bioinformatics/btm108 Genetics and population analysis GenABEL: an R library for genome-wide association analysis , 2022 .