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A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact

BACKGROUND: Much of the debate over the evolutionary consequences of hybridization on genetic divergence and speciation results from the breakdown or reinforcement of reproductive barriers in secondary hybrid zones. Among hybrid populations established for different lengths of time following seconda...

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Autores principales: Liao, Wan-Jin, Zhu, Bi-Ru, Li, Yue-Fei, Li, Xiao-Meng, Zeng, Yan-Fei, Zhang, Da-Yong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6404273/
https://www.ncbi.nlm.nih.gov/pubmed/30841907
http://dx.doi.org/10.1186/s12862-019-1399-y
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author Liao, Wan-Jin
Zhu, Bi-Ru
Li, Yue-Fei
Li, Xiao-Meng
Zeng, Yan-Fei
Zhang, Da-Yong
author_facet Liao, Wan-Jin
Zhu, Bi-Ru
Li, Yue-Fei
Li, Xiao-Meng
Zeng, Yan-Fei
Zhang, Da-Yong
author_sort Liao, Wan-Jin
collection PubMed
description BACKGROUND: Much of the debate over the evolutionary consequences of hybridization on genetic divergence and speciation results from the breakdown or reinforcement of reproductive barriers in secondary hybrid zones. Among hybrid populations established for different lengths of time following secondary contact, stronger reproductive barriers are generally expected to occur in zones with longer contact. However, in plants no detailed investigation of recent and ancient zones of secondary contact has been conducted despite the importance of such a comparative study. Here, we compare pre- and postzygotic reproductive barriers between two closely related oak species, Quercus mongolica and Q. liaotungensis, in such a situation. RESULTS: The recorded flowering times of both species overlapped in both contact zones. The fruit set at 10 and 30 days after interspecific hand pollination was not significantly lower than that after intraspecific pollination whenever Q. mongolica or Q. liaotungensis comprised the maternal parents in both populations. These results indicated that neither prezygotic phenological barriers nor interspecific incompatibility could have resulted in the reproductive isolation between the two species in both hybrid zones. However, the proportion of hybrid seeds produced by both species in the ancient zone was significantly lower than that recorded in the recent zone of secondary contact. In addition, the proportion of hybrid seeds simulated to form, assuming both random mating and an absence of postpollination barriers, was significantly higher than that detected in the ancient contact zone but not in the recent contact zone. These results suggest stronger early-acting postzygotic isolation between the two oak species in the ancient relative to the recent contact zone. CONCLUSIONS: Our comparative study demonstrated that postzygotic barriers during seed maturity were the main contributing factor to total reproductive isolation, particularly in the ancient contact zone, which aided species delimitation. In the recently formed secondary contact zone, pre- and postzygotic barriers were not well developed, and a high frequency of natural hybridization was evident. To our knowledge this study provides the first comparison of reproductive isolation between the ancient and recent secondary contact zones in plants and helps to clarify the evolutionary consequences of hybridization in a temporal context. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1399-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-64042732019-03-18 A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact Liao, Wan-Jin Zhu, Bi-Ru Li, Yue-Fei Li, Xiao-Meng Zeng, Yan-Fei Zhang, Da-Yong BMC Evol Biol Research Article BACKGROUND: Much of the debate over the evolutionary consequences of hybridization on genetic divergence and speciation results from the breakdown or reinforcement of reproductive barriers in secondary hybrid zones. Among hybrid populations established for different lengths of time following secondary contact, stronger reproductive barriers are generally expected to occur in zones with longer contact. However, in plants no detailed investigation of recent and ancient zones of secondary contact has been conducted despite the importance of such a comparative study. Here, we compare pre- and postzygotic reproductive barriers between two closely related oak species, Quercus mongolica and Q. liaotungensis, in such a situation. RESULTS: The recorded flowering times of both species overlapped in both contact zones. The fruit set at 10 and 30 days after interspecific hand pollination was not significantly lower than that after intraspecific pollination whenever Q. mongolica or Q. liaotungensis comprised the maternal parents in both populations. These results indicated that neither prezygotic phenological barriers nor interspecific incompatibility could have resulted in the reproductive isolation between the two species in both hybrid zones. However, the proportion of hybrid seeds produced by both species in the ancient zone was significantly lower than that recorded in the recent zone of secondary contact. In addition, the proportion of hybrid seeds simulated to form, assuming both random mating and an absence of postpollination barriers, was significantly higher than that detected in the ancient contact zone but not in the recent contact zone. These results suggest stronger early-acting postzygotic isolation between the two oak species in the ancient relative to the recent contact zone. CONCLUSIONS: Our comparative study demonstrated that postzygotic barriers during seed maturity were the main contributing factor to total reproductive isolation, particularly in the ancient contact zone, which aided species delimitation. In the recently formed secondary contact zone, pre- and postzygotic barriers were not well developed, and a high frequency of natural hybridization was evident. To our knowledge this study provides the first comparison of reproductive isolation between the ancient and recent secondary contact zones in plants and helps to clarify the evolutionary consequences of hybridization in a temporal context. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1399-y) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-06 /pmc/articles/PMC6404273/ /pubmed/30841907 http://dx.doi.org/10.1186/s12862-019-1399-y Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Liao, Wan-Jin
Zhu, Bi-Ru
Li, Yue-Fei
Li, Xiao-Meng
Zeng, Yan-Fei
Zhang, Da-Yong
A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact
title A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact
title_full A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact
title_fullStr A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact
title_full_unstemmed A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact
title_short A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact
title_sort comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6404273/
https://www.ncbi.nlm.nih.gov/pubmed/30841907
http://dx.doi.org/10.1186/s12862-019-1399-y
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