Genome-wide evidence for speciation with gene flow in Heliconius butterflies

Simon H. Martin, Kanchon K. Dasmahapatra, Nicola J. Nadeau, Camilo Salazar, James R. Walters, Fraser Simpson, Mark Blaxter, Andrea Manica, James Mallet, Chris D. Jiggins

Resultado de la investigación: Contribución a RevistaArtículo

234 Citas (Scopus)

Resumen

Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on wholegenome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Mu llerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time. © 2013 Martin et al.
Idioma originalEnglish (US)
Páginas (desde-hasta)1817-1828
Número de páginas12
PublicaciónGenome Research
Volumen23
N.º11
DOI
EstadoPublished - ene 1 2013

Huella dactilar

Butterflies
Gene Flow
Genome
Sympatry
Reproductive Isolation
Geography
Linkage Disequilibrium
Chromosomes
Alleles
Population

Citar esto

Martin, S. H., Dasmahapatra, K. K., Nadeau, N. J., Salazar, C., Walters, J. R., Simpson, F., ... Jiggins, C. D. (2013). Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research, 23(11), 1817-1828. https://doi.org/10.1101/gr.159426.113
Martin, Simon H. ; Dasmahapatra, Kanchon K. ; Nadeau, Nicola J. ; Salazar, Camilo ; Walters, James R. ; Simpson, Fraser ; Blaxter, Mark ; Manica, Andrea ; Mallet, James ; Jiggins, Chris D. / Genome-wide evidence for speciation with gene flow in Heliconius butterflies. En: Genome Research. 2013 ; Vol. 23, N.º 11. pp. 1817-1828.
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abstract = "Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on wholegenome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40{\%} of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Mu llerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time. {\circledC} 2013 Martin et al.",
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Martin, SH, Dasmahapatra, KK, Nadeau, NJ, Salazar, C, Walters, JR, Simpson, F, Blaxter, M, Manica, A, Mallet, J & Jiggins, CD 2013, 'Genome-wide evidence for speciation with gene flow in Heliconius butterflies', Genome Research, vol. 23, n.º 11, pp. 1817-1828. https://doi.org/10.1101/gr.159426.113

Genome-wide evidence for speciation with gene flow in Heliconius butterflies. / Martin, Simon H.; Dasmahapatra, Kanchon K.; Nadeau, Nicola J.; Salazar, Camilo; Walters, James R.; Simpson, Fraser; Blaxter, Mark; Manica, Andrea; Mallet, James; Jiggins, Chris D.

En: Genome Research, Vol. 23, N.º 11, 01.01.2013, p. 1817-1828.

Resultado de la investigación: Contribución a RevistaArtículo

TY - JOUR

T1 - Genome-wide evidence for speciation with gene flow in Heliconius butterflies

AU - Martin, Simon H.

AU - Dasmahapatra, Kanchon K.

AU - Nadeau, Nicola J.

AU - Salazar, Camilo

AU - Walters, James R.

AU - Simpson, Fraser

AU - Blaxter, Mark

AU - Manica, Andrea

AU - Mallet, James

AU - Jiggins, Chris D.

PY - 2013/1/1

Y1 - 2013/1/1

N2 - Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on wholegenome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Mu llerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time. © 2013 Martin et al.

AB - Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on wholegenome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Mu llerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time. © 2013 Martin et al.

U2 - 10.1101/gr.159426.113

DO - 10.1101/gr.159426.113

M3 - Article

VL - 23

SP - 1817

EP - 1828

JO - Genome Research

JF - Genome Research

SN - 1088-9051

IS - 11

ER -

Martin SH, Dasmahapatra KK, Nadeau NJ, Salazar C, Walters JR, Simpson F y otros. Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research. 2013 ene 1;23(11):1817-1828. https://doi.org/10.1101/gr.159426.113