Subspecies hybridization as a potential conservation tool in species reintroductions

Lilith J. Zecherle; Hazel J. Nichols; Shirli Bar-David; Richard P. Brown; Helen Hipperson; Gavin J. Horsburgh; Alan R. Templeton

doi:10.1111/eva.13191

Subspecies hybridization as a potential conservation tool in species reintroductions

Lilith J. Zecherle, Hazel J. Nichols, Shirli Bar-David, Richard P. Brown, Helen Hipperson, Gavin J. Horsburgh, Alan R. Templeton

Research output: Contribution to journal › Article › peer-review

Abstract

Reintroductions are a powerful tool for the recovery of endangered species. However, their long-term success is strongly influenced by the genetic diversity of the reintroduced population. The chances of population persistence can be improved by enhancing the population's adaptive ability through the mixing of individuals from different sources. However, where source populations are too diverse the reintroduced population could also suffer from outbreeding depression or unsuccessful admixture due to behavioural or genetic barriers. For the reintroduction of Asiatic wild ass Equus hemionus ssp. in Israel, a breeding core was created from individuals of two different subspecies (E. h. onager & E. h. kulan). Today the population comprises approximately 300 individuals and displays no signs of outbreeding depression. The aim of this study was a population genomic evaluation of this conservation reintroduction protocol. We used maximum likelihood methods and genetic clustering analyses to investigate subspecies admixture and test for spatial autocorrelation based on subspecies ancestry. Further, we analysed heterozygosity and effective population sizes in the breeding core prior to release and the current wild population. We discovered high levels of subspecies admixture in the breeding core and wild population, consistent with a significant heterozygote excess in the breeding core. Furthermore, we found no signs of spatial autocorrelation associated with subspecies ancestry in the wild population. Inbreeding and variance effective population size estimates were low. Our results indicate no genetic or behavioural barriers to admixture between the subspecies and suggest that their hybridization has led to greater genetic diversity in the reintroduced population. The study provides rare empirical evidence of the successful application of subspecies hybridization in a reintroduction. It supports use of intraspecific hybridization as a tool to increase genetic diversity in conservation translocations.

Original language	English
Pages (from-to)	1216-1224
Number of pages	9
Journal	Evolutionary Applications
Volume	14
Issue number	5
DOIs	https://doi.org/10.1111/eva.13191
State	Published - May 2021
Externally published	Yes

Bibliographical note

Funding Information:
We would like to thank the Israeli Nature and Parks authorities, The North of England Zoological Society (Chester Zoo), Wildlands Adventure Zoo Emmen, Zoo Rostock and Tiergarten Nürnberg for provision of the DNA samples, and Naama Shahar (Ben‐Gurion University of the Negev) and Georgios Zouganelis (Liverpool John Moores University) for their expertise and help with DNA extractions and shipment of samples. The laboratory work was performed at the NERC Biomolecular Analysis Facility at the University of Sheffield and supported be the UK Natural Environment Research Council. The genomic sequencing was carried out by Edinburgh Genomics, The University of Edinburgh. Edinburgh Genomics is partly supported through core grants from NERC (R8/H10/56), MRC (MR/K001744/1) and BBSRC (BB/J004243/1). The genomic and bioinformatic aspects of this research were funded by the Natural Environment Research Council Biomolecular Analysis Facility Grant (NBAF1073) awarded to HJN & RPB, and the research was also supported by a Humboldt Research Fellowship for Experienced Researchers and a Leverhulme International Academic Fellowship (IAF‐2018‐006) awarded to HJN. LJZ was supported by a PhD scholarship from Liverpool John Moores University. This is publication 1091 of the Mitrani Department of Desert Ecology.

Funding Information:
We would like to thank the Israeli Nature and Parks authorities, The North of England Zoological Society (Chester Zoo), Wildlands Adventure Zoo Emmen, Zoo Rostock and Tiergarten N?rnberg for provision of the DNA samples, and Naama Shahar (Ben-Gurion University of the Negev) and Georgios Zouganelis (Liverpool John Moores University) for their expertise and help with DNA extractions and shipment of samples. The laboratory work was performed at the NERC Biomolecular Analysis Facility at the University of Sheffield and supported be the UK Natural Environment Research Council. The genomic sequencing was carried out by Edinburgh Genomics, The University of Edinburgh. Edinburgh Genomics is partly supported through core grants from NERC (R8/H10/56), MRC (MR/K001744/1) and BBSRC (BB/J004243/1). The genomic and bioinformatic aspects of this research were funded by the Natural Environment Research Council Biomolecular Analysis Facility Grant (NBAF1073) awarded to HJN & RPB, and the research was also supported by a Humboldt Research Fellowship for Experienced Researchers and a Leverhulme International Academic Fellowship (IAF-2018-006) awarded to HJN. LJZ was supported by a PhD scholarship from Liverpool John Moores University. This is publication 1091 of the Mitrani Department of Desert Ecology.

Publisher Copyright:
© 2021 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

Keywords

conservation management
Equus hemionus
genetic admixture
reintroduction
subspecies hybridization

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
Agricultural and Biological Sciences (all)

Access to Document

10.1111/eva.13191

Cite this

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title = "Subspecies hybridization as a potential conservation tool in species reintroductions",

abstract = "Reintroductions are a powerful tool for the recovery of endangered species. However, their long-term success is strongly influenced by the genetic diversity of the reintroduced population. The chances of population persistence can be improved by enhancing the population's adaptive ability through the mixing of individuals from different sources. However, where source populations are too diverse the reintroduced population could also suffer from outbreeding depression or unsuccessful admixture due to behavioural or genetic barriers. For the reintroduction of Asiatic wild ass Equus hemionus ssp. in Israel, a breeding core was created from individuals of two different subspecies (E. h. onager & E. h. kulan). Today the population comprises approximately 300 individuals and displays no signs of outbreeding depression. The aim of this study was a population genomic evaluation of this conservation reintroduction protocol. We used maximum likelihood methods and genetic clustering analyses to investigate subspecies admixture and test for spatial autocorrelation based on subspecies ancestry. Further, we analysed heterozygosity and effective population sizes in the breeding core prior to release and the current wild population. We discovered high levels of subspecies admixture in the breeding core and wild population, consistent with a significant heterozygote excess in the breeding core. Furthermore, we found no signs of spatial autocorrelation associated with subspecies ancestry in the wild population. Inbreeding and variance effective population size estimates were low. Our results indicate no genetic or behavioural barriers to admixture between the subspecies and suggest that their hybridization has led to greater genetic diversity in the reintroduced population. The study provides rare empirical evidence of the successful application of subspecies hybridization in a reintroduction. It supports use of intraspecific hybridization as a tool to increase genetic diversity in conservation translocations.",

keywords = "conservation management, Equus hemionus, genetic admixture, reintroduction, subspecies hybridization",

author = "Zecherle, {Lilith J.} and Nichols, {Hazel J.} and Shirli Bar-David and Brown, {Richard P.} and Helen Hipperson and Horsburgh, {Gavin J.} and Templeton, {Alan R.}",

note = "Funding Information: We would like to thank the Israeli Nature and Parks authorities, The North of England Zoological Society (Chester Zoo), Wildlands Adventure Zoo Emmen, Zoo Rostock and Tiergarten N{\"u}rnberg for provision of the DNA samples, and Naama Shahar (Ben‐Gurion University of the Negev) and Georgios Zouganelis (Liverpool John Moores University) for their expertise and help with DNA extractions and shipment of samples. The laboratory work was performed at the NERC Biomolecular Analysis Facility at the University of Sheffield and supported be the UK Natural Environment Research Council. The genomic sequencing was carried out by Edinburgh Genomics, The University of Edinburgh. Edinburgh Genomics is partly supported through core grants from NERC (R8/H10/56), MRC (MR/K001744/1) and BBSRC (BB/J004243/1). The genomic and bioinformatic aspects of this research were funded by the Natural Environment Research Council Biomolecular Analysis Facility Grant (NBAF1073) awarded to HJN & RPB, and the research was also supported by a Humboldt Research Fellowship for Experienced Researchers and a Leverhulme International Academic Fellowship (IAF‐2018‐006) awarded to HJN. LJZ was supported by a PhD scholarship from Liverpool John Moores University. This is publication 1091 of the Mitrani Department of Desert Ecology. Funding Information: We would like to thank the Israeli Nature and Parks authorities, The North of England Zoological Society (Chester Zoo), Wildlands Adventure Zoo Emmen, Zoo Rostock and Tiergarten N?rnberg for provision of the DNA samples, and Naama Shahar (Ben-Gurion University of the Negev) and Georgios Zouganelis (Liverpool John Moores University) for their expertise and help with DNA extractions and shipment of samples. The laboratory work was performed at the NERC Biomolecular Analysis Facility at the University of Sheffield and supported be the UK Natural Environment Research Council. The genomic sequencing was carried out by Edinburgh Genomics, The University of Edinburgh. Edinburgh Genomics is partly supported through core grants from NERC (R8/H10/56), MRC (MR/K001744/1) and BBSRC (BB/J004243/1). The genomic and bioinformatic aspects of this research were funded by the Natural Environment Research Council Biomolecular Analysis Facility Grant (NBAF1073) awarded to HJN & RPB, and the research was also supported by a Humboldt Research Fellowship for Experienced Researchers and a Leverhulme International Academic Fellowship (IAF-2018-006) awarded to HJN. LJZ was supported by a PhD scholarship from Liverpool John Moores University. This is publication 1091 of the Mitrani Department of Desert Ecology. Publisher Copyright: {\textcopyright} 2021 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd",

year = "2021",

month = may,

doi = "10.1111/eva.13191",

language = "English",

volume = "14",

pages = "1216--1224",

journal = "Evolutionary Applications",

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AU - Bar-David, Shirli

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AU - Hipperson, Helen

AU - Horsburgh, Gavin J.

AU - Templeton, Alan R.

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N2 - Reintroductions are a powerful tool for the recovery of endangered species. However, their long-term success is strongly influenced by the genetic diversity of the reintroduced population. The chances of population persistence can be improved by enhancing the population's adaptive ability through the mixing of individuals from different sources. However, where source populations are too diverse the reintroduced population could also suffer from outbreeding depression or unsuccessful admixture due to behavioural or genetic barriers. For the reintroduction of Asiatic wild ass Equus hemionus ssp. in Israel, a breeding core was created from individuals of two different subspecies (E. h. onager & E. h. kulan). Today the population comprises approximately 300 individuals and displays no signs of outbreeding depression. The aim of this study was a population genomic evaluation of this conservation reintroduction protocol. We used maximum likelihood methods and genetic clustering analyses to investigate subspecies admixture and test for spatial autocorrelation based on subspecies ancestry. Further, we analysed heterozygosity and effective population sizes in the breeding core prior to release and the current wild population. We discovered high levels of subspecies admixture in the breeding core and wild population, consistent with a significant heterozygote excess in the breeding core. Furthermore, we found no signs of spatial autocorrelation associated with subspecies ancestry in the wild population. Inbreeding and variance effective population size estimates were low. Our results indicate no genetic or behavioural barriers to admixture between the subspecies and suggest that their hybridization has led to greater genetic diversity in the reintroduced population. The study provides rare empirical evidence of the successful application of subspecies hybridization in a reintroduction. It supports use of intraspecific hybridization as a tool to increase genetic diversity in conservation translocations.

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Subspecies hybridization as a potential conservation tool in species reintroductions

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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