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

Abstract 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 th...

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Published in:Molecular Biology and Evolution
Main Authors: 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
Other Authors: Russo, Claudia, Deutsche Forschungsgemeinschaft, Heisenberg program, Natural Environment Research Council, Institut Polaire Français Paul Emile Victor, Terres Australes et Antarctiques Françaises, Mohamed bin Zayed Species Conservation Fund and the Brian Mason Scientific and Technical Trust, Chatham Islands, Falkland Islands Government, Government of South Georgia and the South Sandwich Islands, Animal Ethic Committee of the Institut Polaire Français Paul Emile Victor, Préfet des Terres Australes et Antarctiques Françaises, Animal Ethics Committee of Charles Sturt University, New Zealand Department of Conservation, New Island Conservation Trust, Antarctic Research Trust
Format: Article in Journal/Newspaper
Language:English
Published: Oxford University Press (OUP) 2019
Subjects:
Online Access:http://dx.doi.org/10.1093/molbev/msz090
http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msz090/28790181/msz090.pdf
http://academic.oup.com/mbe/article-pdf/36/8/1671/29001242/msz090.pdf
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spelling croxfordunivpr:10.1093/molbev/msz090 2023-12-31T10:01:22+01:00 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 Russo, Claudia Deutsche Forschungsgemeinschaft Heisenberg program Natural Environment Research Council Institut Polaire Français Paul Emile Victor Terres Australes et Antarctiques Françaises Mohamed bin Zayed Species Conservation Fund and the Brian Mason Scientific and Technical Trust Chatham Islands Falkland Islands Government Government of South Georgia and the South Sandwich Islands Animal Ethic Committee of the Institut Polaire Français Paul Emile Victor Préfet des Terres Australes et Antarctiques Françaises Animal Ethics Committee of Charles Sturt University New Zealand Department of Conservation New Island Conservation Trust Antarctic Research Trust 2019 http://dx.doi.org/10.1093/molbev/msz090 http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msz090/28790181/msz090.pdf http://academic.oup.com/mbe/article-pdf/36/8/1671/29001242/msz090.pdf en eng Oxford University Press (OUP) http://creativecommons.org/licenses/by-nc/4.0/ Molecular Biology and Evolution volume 36, issue 8, page 1671-1685 ISSN 0737-4038 1537-1719 Genetics Molecular Biology Ecology, Evolution, Behavior and Systematics journal-article 2019 croxfordunivpr https://doi.org/10.1093/molbev/msz090 2023-12-06T08:36:34Z Abstract 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. Article in Journal/Newspaper Antarc* Antarctic Antarctic prion Pachyptila desolata Oxford University Press (via Crossref) Molecular Biology and Evolution 36 8 1671 1685
institution Open Polar
collection Oxford University Press (via Crossref)
op_collection_id croxfordunivpr
language English
topic Genetics
Molecular Biology
Ecology, Evolution, Behavior and Systematics
spellingShingle Genetics
Molecular Biology
Ecology, Evolution, Behavior and Systematics
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
topic_facet Genetics
Molecular Biology
Ecology, Evolution, Behavior and Systematics
description Abstract 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.
author2 Russo, Claudia
Deutsche Forschungsgemeinschaft
Heisenberg program
Natural Environment Research Council
Institut Polaire Français Paul Emile Victor
Terres Australes et Antarctiques Françaises
Mohamed bin Zayed Species Conservation Fund and the Brian Mason Scientific and Technical Trust
Chatham Islands
Falkland Islands Government
Government of South Georgia and the South Sandwich Islands
Animal Ethic Committee of the Institut Polaire Français Paul Emile Victor
Préfet des Terres Australes et Antarctiques Françaises
Animal Ethics Committee of Charles Sturt University
New Zealand Department of Conservation
New Island Conservation Trust
Antarctic Research Trust
format Article in Journal/Newspaper
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
title 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_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_sort additive traits lead to feeding advantage and reproductive isolation, promoting homoploid hybrid speciation
publisher Oxford University Press (OUP)
publishDate 2019
url http://dx.doi.org/10.1093/molbev/msz090
http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msz090/28790181/msz090.pdf
http://academic.oup.com/mbe/article-pdf/36/8/1671/29001242/msz090.pdf
genre Antarc*
Antarctic
Antarctic prion
Pachyptila desolata
genre_facet Antarc*
Antarctic
Antarctic prion
Pachyptila desolata
op_source Molecular Biology and Evolution
volume 36, issue 8, page 1671-1685
ISSN 0737-4038 1537-1719
op_rights http://creativecommons.org/licenses/by-nc/4.0/
op_doi https://doi.org/10.1093/molbev/msz090
container_title Molecular Biology and Evolution
container_volume 36
container_issue 8
container_start_page 1671
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