Diversification of complex butterfly wing patterns by repeated regulatory evolution of a<i>Wnt</i>ligand

Martin, Arnaud; Papa, Riccardo; Nadeau, Nicola J.; Hill, Ryan I.; Counterman, Brian A.; Halder, Georg; Jiggins, Chris D.; Kronforst, Marcus R.; Long, Anthony D.; McMillan, W. Owen; Reed, Robert D.

doi:10.1073/pnas.1204800109

Cited by 245 publications

(297 citation statements)

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“…Some of the most convincing data for the genetic and evolutionary control of colour patterns were obtained from different species or spontaneous mutants within species of Drosophila and some butterflies [12][13][14][15][16][17][18][19][20][21][22] . In those reports, various genetic changes that contributed to phenotypic differences within or between species were identified; however, the phenomena by which a single locus (gene) can produce multiple phenotypic traits are largely unknown 22 .…”

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The transcription factor Apontic-like controls diverse colouration pattern in caterpillars

et al. 2014

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Genetic polymorphisms underlie the convergent and divergent evolution of various phenotypes. Diverse colour patterns on caterpillars, which are ecologically important, are good models for understanding the molecular backgrounds of phenotypic diversity. Here we show that a single evolutionarily conserved gene apontic-like (apt-like) encoding for a putative transcription factor accounts for the silkworm p locus, which causes at least 15 different larval markings involved in branch-like markings and eye-spot formation. The expression of apt-like and melanin synthesis genes are upregulated in association with pigmented areas of marking mutants Striped (p S ) and normal ( þ p ) but not in the non-marking allele plain (p). Functional analyses, ectopic expression, RNAi and TALEN, demonstrate that apt-like causes melanin pigmentation in a cell-autonomous manner. These results suggest that variation in p alleles is caused by the differential expression of the gene apt-like which induces targeted elevation of gene expressions in the melanin synthesis pathway.

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The transcription factor Apontic-like controls diverse colouration pattern in caterpillars

et al. 2014

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“…This work joins a flurry of recent genomic work on mimicry in P. polytes and other butterflies [2][3][4][5][6] , which together bring us much closer to understanding how mimicry works.…”

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confidence: 67%

New genomes clarify mimicry evolution

Mallet

2015

Nat Genet

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“…WntA is expressed in the final larval instar where it shows diverse expression patterns associated with black regions in the centre of the forewing (figure 2). Additional evidence for the role of WntA comes from heparin injection into wing tissue of developing Heliconius pupae, which leads to changes in adult wing pattern comparable with genetic effects of Ac [36,37]. Heparin binds Wnt family ligands and promotes their mobility through tissue, and although its effects are not specific to WntA, the combination of genetic mapping, morphogen experiments and expression studies builds a compelling case for the role of WntA in forewing patterning.…”

Section: The Pattern Locus and Wnt Signallingmentioning

confidence: 99%

“…R. Soc. B 372: 20150485 [35,36,38,59]. Similarly, it has been used to remove white bands when distantly related L. arthemis mimics Battus philenor [37].…”

Section: Why Hotspot Genes?mentioning

confidence: 99%

“…WntA was identified as the functional gene at this locus through a combination of genetic linkage mapping using RAD-seq, a population genetic signal of divergence, and differences in expression patterns in developing wings [35][36][37][38]. WntA is expressed in the final larval instar where it shows diverse expression patterns associated with black regions in the centre of the forewing (figure 2).…”

Section: The Pattern Locus and Wnt Signallingmentioning

confidence: 99%

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Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

Jiggins¹,

Wallbank²,

Hanly³

2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. A major challenge is to understand how conserved gene regulatory networks control the wonderful diversity of form that we see among animals and plants. Butterfly wing patterns are an excellent example of this diversity. Butterfly wings form as imaginal discs in the caterpillar and are constructed by a gene regulatory network, much of which is conserved across the holometabolous insects. Recent work in Heliconius butterflies takes advantage of genomic approaches and offers insights into how the diversification of wing patterns is overlaid onto this conserved network. WntA is a patterning morphogen that alters spatial information in the wing. Optix is a transcription factor that acts later in development to paint specific wing regions red. Both of these loci fit the paradigm of conserved protein-coding loci with diverse regulatory elements and developmental roles that have taken on novel derived functions in patterning wings. These discoveries offer insights into the 'Nymphalid Ground Plan', which offers a unifying hypothesis for pattern formation across nymphalid butterflies. These loci also represent 'hotspots' for morphological change that have been targeted repeatedly during evolution. Both convergent and divergent evolution of a great diversity of patterns is controlled by complex alleles at just a few genes. We suggest that evolutionary change has become focused on one or a few genetic loci for two reasons. First, pre-existing complex cis-regulatory loci that already interact with potentially relevant transcription factors are more likely to acquire novel functions in wing patterning. Second, the shape of wing regulatory networks may constrain evolutionary change to one or a few loci. Overall, genomic approaches that have identified wing patterning loci in these butterflies offer broad insight into how gene regulatory networks evolve to produce diversity.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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Diversification of complex butterfly wing patterns by repeated regulatory evolution of aWntligand

Cited by 245 publications

References 52 publications

The transcription factor Apontic-like controls diverse colouration pattern in caterpillars

The transcription factor Apontic-like controls diverse colouration pattern in caterpillars

New genomes clarify mimicry evolution

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

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