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Edited by Dolph Schluter, University of British Columbia, Vancouver, BC, Canada, and approved November 29, 2017 (received for review October 4, 2017)
Significance
Hybridization between species can produce reproductively isolated lineages by combining parental genotypes in novel ways. Here, we used thousands of genetic markers to demonstrate that the recently rediscovered golden-crowned manakin represents an avian hybrid species from the Amazon basin. This hybrid species has a unique golden-colored crown patch used for display, which differs from the brilliant white coloration of the parental species. We used microscopy to demonstrate that, despite its unique coloration, the crown has intermediate color-producing morphological features at the nanoscale. We propose that these intermediate features disrupted the high reflectivity of the parental species, resulting in a dull hybrid population. Selection then sequestered carotenoids to the crown to compensate for its low reflectivity.
Abstract
Hybrid speciation is rare in vertebrates, and reproductive isolation arising from hybridization is infrequently demonstrated. Here, we present evidence supporting a hybrid-speciation event involving the genetic admixture of the snow-capped (Lepidothrix nattereri) and opal-crowned (Lepidothrix iris) manakins of the Amazon basin, leading to the formation of the hybrid species, the golden-crowned manakin (Lepidothrix vilasboasi). We used a genome-wide SNP dataset together with analysis of admixture, population structure, and coalescent modeling to demonstrate that the golden-crowned manakin is genetically an admixture of these species and does not represent a hybrid zone but instead formed through ancient genetic admixture. We used spectrophotometry to quantify the coloration of the species-specific male crown patches. Crown patches are highly reflective white (snow-capped manakin) or iridescent whitish-blue to pink (opal-crowned manakin) in parental species but are a much less reflective yellow in the hybrid species. The brilliant coloration of the parental species results from nanostructural organization of the keratin matrix feather barbs of the crown. However, using electron microscopy, we demonstrate that the structural organization of this matrix is different in the two parental species and that the hybrid species is intermediate. The intermediate nature of the crown barbs, resulting from past admixture appears to have rendered a duller structural coloration. To compensate for reduced brightness, selection apparently resulted in extensive thickening of the carotenoid-laden barb cortex, producing the yellow crown coloration. The evolution of this unique crown-color signal likely culminated in premating isolation of the hybrid species from both parental species.
Footnotes
- ↵1To whom correspondence may be addressed. Email: abarreguzm{at}gmail.com or jason.weir{at}utoronto.ca.
Author contributions: A.O.B.-G., A.A., and J.T.W. designed research; A.O.B.-G. and J.T.W. performed research; A.O.B.-G., A.A., and J.T.W. conducted field work; A.O.B.-G., M.D.S., and J.T.W. analyzed data; and A.O.B.-G. and J.T.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the National Center for Biotechnology Information GenBank database (accession nos. MG662263–MG662371) and the Sequence Read Archive (SRA) database (accession nos. SRR6370333–SRR6370542).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1717319115/-/DCSupplemental.
Published under the PNAS license.
- aDepartment of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
- bDepartment of Zoology, Museu Paráense Emílio Goeldi, Belém, Pará, 66040-170 Brazil;
- cDepartment of Biology, University of Ghent, 9000 Ghent, Belgium;
- dDepartment of Biological Sciences, University of Toronto Scarborough, Toronto, ON, Canada M1C 1A4
Edited by Dolph Schluter, University of British Columbia, Vancouver, BC, Canada, and approved November 29, 2017 (received for review October 4, 2017)
Significance
Hybridization between species can produce reproductively isolated lineages by combining parental genotypes in novel ways. Here, we used thousands of genetic markers to demonstrate that the recently rediscovered golden-crowned manakin represents an avian hybrid species from the Amazon basin. This hybrid species has a unique golden-colored crown patch used for display, which differs from the brilliant white coloration of the parental species. We used microscopy to demonstrate that, despite its unique coloration, the crown has intermediate color-producing morphological features at the nanoscale. We propose that these intermediate features disrupted the high reflectivity of the parental species, resulting in a dull hybrid population. Selection then sequestered carotenoids to the crown to compensate for its low reflectivity.
Abstract
Hybrid speciation is rare in vertebrates, and reproductive isolation arising from hybridization is infrequently demonstrated. Here, we present evidence supporting a hybrid-speciation event involving the genetic admixture of the snow-capped (Lepidothrix nattereri) and opal-crowned (Lepidothrix iris) manakins of the Amazon basin, leading to the formation of the hybrid species, the golden-crowned manakin (Lepidothrix vilasboasi). We used a genome-wide SNP dataset together with analysis of admixture, population structure, and coalescent modeling to demonstrate that the golden-crowned manakin is genetically an admixture of these species and does not represent a hybrid zone but instead formed through ancient genetic admixture. We used spectrophotometry to quantify the coloration of the species-specific male crown patches. Crown patches are highly reflective white (snow-capped manakin) or iridescent whitish-blue to pink (opal-crowned manakin) in parental species but are a much less reflective yellow in the hybrid species. The brilliant coloration of the parental species results from nanostructural organization of the keratin matrix feather barbs of the crown. However, using electron microscopy, we demonstrate that the structural organization of this matrix is different in the two parental species and that the hybrid species is intermediate. The intermediate nature of the crown barbs, resulting from past admixture appears to have rendered a duller structural coloration. To compensate for reduced brightness, selection apparently resulted in extensive thickening of the carotenoid-laden barb cortex, producing the yellow crown coloration. The evolution of this unique crown-color signal likely culminated in premating isolation of the hybrid species from both parental species.
- hybrid speciation
- structural color
- ornamentation
- Amazon
- Lepidothrix vilasboasi
Footnotes
- ↵1To whom correspondence may be addressed. Email: abarreguzm{at}gmail.com or jason.weir{at}utoronto.ca.
Author contributions: A.O.B.-G., A.A., and J.T.W. designed research; A.O.B.-G. and J.T.W. performed research; A.O.B.-G., A.A., and J.T.W. conducted field work; A.O.B.-G., M.D.S., and J.T.W. analyzed data; and A.O.B.-G. and J.T.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the National Center for Biotechnology Information GenBank database (accession nos. MG662263–MG662371) and the Sequence Read Archive (SRA) database (accession nos. SRR6370333–SRR6370542).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1717319115/-/DCSupplemental.
Published under the PNAS license.
Hybrid speciation in an Amazonian bird
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