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Low incidence of inbreeding in a long-lived primate population isolated for 75 years

ABSTRACT: When close relatives mate, offspring are expected to suffer fitness consequences due to inbreeding depression. Inbreeding has previously been quantified in two ways: using a sufficiently large panel of markers or deep and complete pedigrees over several generations. However, the applicatio...

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Autores principales: Widdig, Anja, Muniz, Laura, Minkner, Mirjam, Barth, Yvonne, Bley, Stefanie, Ruiz-Lambides, Angelina, Junge, Olaf, Mundry, Roger, Kulik, Lars
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5145906/
https://www.ncbi.nlm.nih.gov/pubmed/28018027
http://dx.doi.org/10.1007/s00265-016-2236-6
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author Widdig, Anja
Muniz, Laura
Minkner, Mirjam
Barth, Yvonne
Bley, Stefanie
Ruiz-Lambides, Angelina
Junge, Olaf
Mundry, Roger
Kulik, Lars
author_facet Widdig, Anja
Muniz, Laura
Minkner, Mirjam
Barth, Yvonne
Bley, Stefanie
Ruiz-Lambides, Angelina
Junge, Olaf
Mundry, Roger
Kulik, Lars
author_sort Widdig, Anja
collection PubMed
description ABSTRACT: When close relatives mate, offspring are expected to suffer fitness consequences due to inbreeding depression. Inbreeding has previously been quantified in two ways: using a sufficiently large panel of markers or deep and complete pedigrees over several generations. However, the application of both approaches is still limited by the challenge of compiling such data for species with long generation times, such as primates. Here, we assess inbreeding in rhesus macaques living on Cayo Santiago (Puerto Rico), a population genetically isolated since 1938, but descendant of a large set of presumably unrelated founders. Using comprehensive genetic data, we calculated inbreeding coefficients (F) for 2669 individuals with complete three generation pedigrees and 609 individuals with complete four generation pedigrees. We found that 0.79 and 7.39% of individuals had an F > 0 when using data from three and four generation pedigrees, respectively. No evidence of an increase in inbreeding over the study period (up to 23 years) was found. Furthermore, the observed mean relatedness of breeding pairs differed significantly from the distribution of parental relatedness expected as simulated based on previous reproductive data, suggesting that kin generally avoid breeding with each other. Finally, inbreeding was not a predictor of early mortality measured as survival until weaning and sexual maturation, respectively. Our results remain consistent with three estimators of inbreeding (standardized heterozygosity, internal relatedness, and homozygosity by loci) using up to 42 highly polymorphic microsatellites for the same set of individuals. Together, our results demonstrate that close inbreeding may not be prevalent even in populations isolated over long periods when mechanisms of inbreeding avoidance can operate. SIGNIFICANCE STATEMENT: When close relatives mate, offspring may suffer from such inbreeding, e.g., via lower survival and/or fertility. Using (i) a large panel of genetic markers and (ii) complete three or four generation pedigrees, respectively, we show that incidences of inbreeding in a long-lived primate population are rare, even after genetic isolation for 75 years. Moreover, our simulations suggest that kin in our population generally avoid breeding with each other. Finally, the few inbred individuals detected in our large sample did not suffer from lower survival. Given that many animal species face dramatic habitat loss combined with critical population declines, our study provides important implications for conservation biology in general and for population management in particular. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-016-2236-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-51459062016-12-23 Low incidence of inbreeding in a long-lived primate population isolated for 75 years Widdig, Anja Muniz, Laura Minkner, Mirjam Barth, Yvonne Bley, Stefanie Ruiz-Lambides, Angelina Junge, Olaf Mundry, Roger Kulik, Lars Behav Ecol Sociobiol Original Article ABSTRACT: When close relatives mate, offspring are expected to suffer fitness consequences due to inbreeding depression. Inbreeding has previously been quantified in two ways: using a sufficiently large panel of markers or deep and complete pedigrees over several generations. However, the application of both approaches is still limited by the challenge of compiling such data for species with long generation times, such as primates. Here, we assess inbreeding in rhesus macaques living on Cayo Santiago (Puerto Rico), a population genetically isolated since 1938, but descendant of a large set of presumably unrelated founders. Using comprehensive genetic data, we calculated inbreeding coefficients (F) for 2669 individuals with complete three generation pedigrees and 609 individuals with complete four generation pedigrees. We found that 0.79 and 7.39% of individuals had an F > 0 when using data from three and four generation pedigrees, respectively. No evidence of an increase in inbreeding over the study period (up to 23 years) was found. Furthermore, the observed mean relatedness of breeding pairs differed significantly from the distribution of parental relatedness expected as simulated based on previous reproductive data, suggesting that kin generally avoid breeding with each other. Finally, inbreeding was not a predictor of early mortality measured as survival until weaning and sexual maturation, respectively. Our results remain consistent with three estimators of inbreeding (standardized heterozygosity, internal relatedness, and homozygosity by loci) using up to 42 highly polymorphic microsatellites for the same set of individuals. Together, our results demonstrate that close inbreeding may not be prevalent even in populations isolated over long periods when mechanisms of inbreeding avoidance can operate. SIGNIFICANCE STATEMENT: When close relatives mate, offspring may suffer from such inbreeding, e.g., via lower survival and/or fertility. Using (i) a large panel of genetic markers and (ii) complete three or four generation pedigrees, respectively, we show that incidences of inbreeding in a long-lived primate population are rare, even after genetic isolation for 75 years. Moreover, our simulations suggest that kin in our population generally avoid breeding with each other. Finally, the few inbred individuals detected in our large sample did not suffer from lower survival. Given that many animal species face dramatic habitat loss combined with critical population declines, our study provides important implications for conservation biology in general and for population management in particular. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-016-2236-6) contains supplementary material, which is available to authorized users. Springer Berlin Heidelberg 2016-12-09 2017 /pmc/articles/PMC5145906/ /pubmed/28018027 http://dx.doi.org/10.1007/s00265-016-2236-6 Text en © The Author(s) 2017 Open Access This 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.
spellingShingle Original Article
Widdig, Anja
Muniz, Laura
Minkner, Mirjam
Barth, Yvonne
Bley, Stefanie
Ruiz-Lambides, Angelina
Junge, Olaf
Mundry, Roger
Kulik, Lars
Low incidence of inbreeding in a long-lived primate population isolated for 75 years
title Low incidence of inbreeding in a long-lived primate population isolated for 75 years
title_full Low incidence of inbreeding in a long-lived primate population isolated for 75 years
title_fullStr Low incidence of inbreeding in a long-lived primate population isolated for 75 years
title_full_unstemmed Low incidence of inbreeding in a long-lived primate population isolated for 75 years
title_short Low incidence of inbreeding in a long-lived primate population isolated for 75 years
title_sort low incidence of inbreeding in a long-lived primate population isolated for 75 years
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5145906/
https://www.ncbi.nlm.nih.gov/pubmed/28018027
http://dx.doi.org/10.1007/s00265-016-2236-6
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