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Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation

Speciation through homoploid hybridization (HHS) is considered extremely rare in animals. This is mainly because the establishment of reproductive isolation as a product of hybridization is uncommon. Additionally, many traits are underpinned by polygeny and/or incomplete dominance, where the hybrid...

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Autores principales: Masello, Juan F, Quillfeldt, Petra, Sandoval-Castellanos, Edson, Alderman, Rachael, Calderón, Luciano, Cherel, Yves, Cole, Theresa L, Cuthbert, Richard J, Marin, Manuel, Massaro, Melanie, Navarro, Joan, Phillips, Richard A, Ryan, Peter G, Shepherd, Lara D, Suazo, Cristián G, Weimerskirch, Henri, Moodley, Yoshan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6657733/
https://www.ncbi.nlm.nih.gov/pubmed/31028398
http://dx.doi.org/10.1093/molbev/msz090
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author Masello, Juan F
Quillfeldt, Petra
Sandoval-Castellanos, Edson
Alderman, Rachael
Calderón, Luciano
Cherel, Yves
Cole, Theresa L
Cuthbert, Richard J
Marin, Manuel
Massaro, Melanie
Navarro, Joan
Phillips, Richard A
Ryan, Peter G
Shepherd, Lara D
Suazo, Cristián G
Weimerskirch, Henri
Moodley, Yoshan
author_facet Masello, Juan F
Quillfeldt, Petra
Sandoval-Castellanos, Edson
Alderman, Rachael
Calderón, Luciano
Cherel, Yves
Cole, Theresa L
Cuthbert, Richard J
Marin, Manuel
Massaro, Melanie
Navarro, Joan
Phillips, Richard A
Ryan, Peter G
Shepherd, Lara D
Suazo, Cristián G
Weimerskirch, Henri
Moodley, Yoshan
author_sort Masello, Juan F
collection PubMed
description Speciation through homoploid hybridization (HHS) is considered extremely rare in animals. This is mainly because the establishment of reproductive isolation as a product of hybridization is uncommon. Additionally, many traits are underpinned by polygeny and/or incomplete dominance, where the hybrid phenotype is an additive blend of parental characteristics. Phenotypically intermediate hybrids are usually at a fitness disadvantage compared with parental species and tend to vanish through backcrossing with parental population(s). It is therefore unknown whether the additive nature of hybrid traits in itself could lead successfully to HHS. Using a multi-marker genetic data set and a meta-analysis of diet and morphology, we investigated a potential case of HHS in the prions (Pachyptila spp.), seabirds distinguished by their bills, prey choice, and timing of breeding. Using approximate Bayesian computation, we show that the medium-billed Salvin’s prion (Pachyptila salvini) could be a hybrid between the narrow-billed Antarctic prion (Pachyptila desolata) and broad-billed prion (Pachyptila vittata). Remarkably, P. salvini’s intermediate bill width has given it a feeding advantage with respect to the other Pachyptila species, allowing it to consume a broader range of prey, potentially increasing its fitness. Available metadata showed that P. salvini is also intermediate in breeding phenology and, with no overlap in breeding times, it is effectively reproductively isolated from either parental species through allochrony. These results provide evidence for a case of HHS in nature, and show for the first time that additivity of divergent parental traits alone can lead directly to increased hybrid fitness and reproductive isolation.
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spelling pubmed-66577332019-08-02 Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation Masello, Juan F Quillfeldt, Petra Sandoval-Castellanos, Edson Alderman, Rachael Calderón, Luciano Cherel, Yves Cole, Theresa L Cuthbert, Richard J Marin, Manuel Massaro, Melanie Navarro, Joan Phillips, Richard A Ryan, Peter G Shepherd, Lara D Suazo, Cristián G Weimerskirch, Henri Moodley, Yoshan Mol Biol Evol Discoveries Speciation through homoploid hybridization (HHS) is considered extremely rare in animals. This is mainly because the establishment of reproductive isolation as a product of hybridization is uncommon. Additionally, many traits are underpinned by polygeny and/or incomplete dominance, where the hybrid phenotype is an additive blend of parental characteristics. Phenotypically intermediate hybrids are usually at a fitness disadvantage compared with parental species and tend to vanish through backcrossing with parental population(s). It is therefore unknown whether the additive nature of hybrid traits in itself could lead successfully to HHS. Using a multi-marker genetic data set and a meta-analysis of diet and morphology, we investigated a potential case of HHS in the prions (Pachyptila spp.), seabirds distinguished by their bills, prey choice, and timing of breeding. Using approximate Bayesian computation, we show that the medium-billed Salvin’s prion (Pachyptila salvini) could be a hybrid between the narrow-billed Antarctic prion (Pachyptila desolata) and broad-billed prion (Pachyptila vittata). Remarkably, P. salvini’s intermediate bill width has given it a feeding advantage with respect to the other Pachyptila species, allowing it to consume a broader range of prey, potentially increasing its fitness. Available metadata showed that P. salvini is also intermediate in breeding phenology and, with no overlap in breeding times, it is effectively reproductively isolated from either parental species through allochrony. These results provide evidence for a case of HHS in nature, and show for the first time that additivity of divergent parental traits alone can lead directly to increased hybrid fitness and reproductive isolation. Oxford University Press 2019-08 2019-04-26 /pmc/articles/PMC6657733/ /pubmed/31028398 http://dx.doi.org/10.1093/molbev/msz090 Text en © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Masello, Juan F
Quillfeldt, Petra
Sandoval-Castellanos, Edson
Alderman, Rachael
Calderón, Luciano
Cherel, Yves
Cole, Theresa L
Cuthbert, Richard J
Marin, Manuel
Massaro, Melanie
Navarro, Joan
Phillips, Richard A
Ryan, Peter G
Shepherd, Lara D
Suazo, Cristián G
Weimerskirch, Henri
Moodley, Yoshan
Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation
title Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation
title_full Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation
title_fullStr Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation
title_full_unstemmed Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation
title_short Additive Traits Lead to Feeding Advantage and Reproductive Isolation, Promoting Homoploid Hybrid Speciation
title_sort additive traits lead to feeding advantage and reproductive isolation, promoting homoploid hybrid speciation
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6657733/
https://www.ncbi.nlm.nih.gov/pubmed/31028398
http://dx.doi.org/10.1093/molbev/msz090
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