Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling

Richard W R Wallbank, Simon W. Baxter, Carolina Pardo-Diaz, Joseph J. Hanly, Simon H. Martin, James Mallet, Kanchon K. Dasmahapatra, Camilo Salazar, Mathieu Joron, Nicola Nadeau, W. Owen McMillan, Chris D. Jiggins

Resultado de la investigación: Contribución a RevistaArtículo

50 Citas (Scopus)

Resumen

© 2016 Wallbank et al.An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.
Idioma originalEnglish (US)
PublicaciónPLoS Biology
DOI
EstadoPublished - ene 15 2016

Huella dactilar

Heliconius
Butterflies
butterflies
Genetic Recombination
enhancer elements
Internal-External Control
adaptive radiation
introgression
Transcription Factors
transcription factors
Color
Genes
Genome
Radiation
Phenotype
phenotype
Biological Sciences
history
loci
genome

Citar esto

Wallbank, R. W. R., Baxter, S. W., Pardo-Diaz, C., Hanly, J. J., Martin, S. H., Mallet, J., ... Jiggins, C. D. (2016). Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling. PLoS Biology. https://doi.org/10.1371/journal.pbio.1002353
Wallbank, Richard W R ; Baxter, Simon W. ; Pardo-Diaz, Carolina ; Hanly, Joseph J. ; Martin, Simon H. ; Mallet, James ; Dasmahapatra, Kanchon K. ; Salazar, Camilo ; Joron, Mathieu ; Nadeau, Nicola ; McMillan, W. Owen ; Jiggins, Chris D. / Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling. En: PLoS Biology. 2016.
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abstract = "{\circledC} 2016 Wallbank et al.An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.",
author = "Wallbank, {Richard W R} and Baxter, {Simon W.} and Carolina Pardo-Diaz and Hanly, {Joseph J.} and Martin, {Simon H.} and James Mallet and Dasmahapatra, {Kanchon K.} and Camilo Salazar and Mathieu Joron and Nicola Nadeau and McMillan, {W. Owen} and Jiggins, {Chris D.}",
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Wallbank, RWR, Baxter, SW, Pardo-Diaz, C, Hanly, JJ, Martin, SH, Mallet, J, Dasmahapatra, KK, Salazar, C, Joron, M, Nadeau, N, McMillan, WO & Jiggins, CD 2016, 'Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling', PLoS Biology. https://doi.org/10.1371/journal.pbio.1002353

Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling. / Wallbank, Richard W R; Baxter, Simon W.; Pardo-Diaz, Carolina; Hanly, Joseph J.; Martin, Simon H.; Mallet, James; Dasmahapatra, Kanchon K.; Salazar, Camilo; Joron, Mathieu; Nadeau, Nicola; McMillan, W. Owen; Jiggins, Chris D.

En: PLoS Biology, 15.01.2016.

Resultado de la investigación: Contribución a RevistaArtículo

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AU - Wallbank, Richard W R

AU - Baxter, Simon W.

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AU - Hanly, Joseph J.

AU - Martin, Simon H.

AU - Mallet, James

AU - Dasmahapatra, Kanchon K.

AU - Salazar, Camilo

AU - Joron, Mathieu

AU - Nadeau, Nicola

AU - McMillan, W. Owen

AU - Jiggins, Chris D.

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N2 - © 2016 Wallbank et al.An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.

AB - © 2016 Wallbank et al.An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.

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