Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest

Autores
Oklander, Luciana Inés; Fernández, Gabriela Paula; Machado, Stela; Caputo, Mariela; Hirano, Zelinda M. B.; Rylands, Anthony B.; Neves, Leonardo G.; Mendes, Sérgio L.; Pacca, Luciana G.; de Melo, Fabiano R.; Mourthé, Italo; Freitas, Thales R. O.; Corach, Daniel; Jerusalinsky, Leandro; Bonatto, Sandro L.
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The brown howler, Alouatta guariba, endemic to the Atlantic Forest of Brazil and Argentina, is threatened by habitat loss and fragmentation, hunting, and its susceptibility to yellow fever. Two subspecies have been recognized, but their names, validity, and geographic ranges have been controversial. We obtained samples covering the species' entire distribution in Brazil and Argentina to clarify these issues by investigating their genetic diversity and structure and assessing their evolutionary history. We analyzed, for the first time, a set of ten microsatellite markers (N = 153), plus mitochondrial DNA (mtDNA) segments of the control region (N = 207) and cytochrome b gene (N = 116). The microsatellite data support two to three genetic clusters with biological significance. The southern populations (Argentina, Santa Catarina, and Rio Grande do Sul) presented a homogeneous genetic component, and populations from São Paulo (SP) to the north presented another component, although most presented ∼20% of the southern component. With K = 3, SP emerged as a third component while sharing some ancestry with Rio de Janeiro and Argentina. The mtDNA phylogenies revealed three main clades that diverged almost simultaneously around 250 thousand years ago (kya). Clades A and B are from central SP to the north and east, while clade C is from SP to the south and southwest. Samples from SP presented haplotypes in all three clades, sometimes in the same population. The demographic history of the species estimated with the Bayesian skyline plot of the mtDNA showed a strong expansion ∼40–20 kya and a strong reduction over the last ∼4–2 kya. Although the genetic clusters identified here deserve appropriate management strategies as conservation units, the absence of (i) concordance between the mtDNA and microsatellite data, (ii) reciprocal monophyly in the mtDNA, and (iii) clear-cut non-genetic diagnostic characters advises against considering them as different taxonomic entities. None of the previous taxonomic proposals were corroborated by our data. Our results elucidate the taxonomy of the Atlantic Forest brown howler, indicating it should be considered a monotypic species, A. guariba. We also clarify the evolutionary history of the species regarding its intraspecific genetic diversity, which is crucial information for its conservation and population management.
Fil: Oklander, Luciana Inés. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; Argentina
Fil: Fernández, Gabriela Paula. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina
Fil: Machado, Stela. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina
Fil: Caputo, Mariela. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina
Fil: Hirano, Zelinda M. B.. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rylands, Anthony B.. No especifíca;
Fil: Neves, Leonardo G.. No especifíca;
Fil: Mendes, Sérgio L.. Instituto Nacional da Mata Atlântica; Brasil
Fil: Pacca, Luciana G.. Instituto Chico Mendes de Conservação da Biodiversidade; Brasil
Fil: de Melo, Fabiano R.. Universidade Federal de Viçosa; Brasil
Fil: Mourthé, Italo. Pontificia Universidade Católica do Rio Grande do Sul; Brasil
Fil: Freitas, Thales R. O.. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Corach, Daniel. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Microbiología, Inmunología y Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Jerusalinsky, Leandro. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Bonatto, Sandro L.. Pontificia Universidade Católica do Rio Grande do Sul; Brasil
Materia
mtdna
microsatelite
Platyrrhini
primates
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/268759

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spelling Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic ForestOklander, Luciana InésFernández, Gabriela PaulaMachado, StelaCaputo, MarielaHirano, Zelinda M. B.Rylands, Anthony B.Neves, Leonardo G.Mendes, Sérgio L.Pacca, Luciana G.de Melo, Fabiano R.Mourthé, ItaloFreitas, Thales R. O.Corach, DanielJerusalinsky, LeandroBonatto, Sandro L.mtdnamicrosatelitePlatyrrhiniprimateshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The brown howler, Alouatta guariba, endemic to the Atlantic Forest of Brazil and Argentina, is threatened by habitat loss and fragmentation, hunting, and its susceptibility to yellow fever. Two subspecies have been recognized, but their names, validity, and geographic ranges have been controversial. We obtained samples covering the species' entire distribution in Brazil and Argentina to clarify these issues by investigating their genetic diversity and structure and assessing their evolutionary history. We analyzed, for the first time, a set of ten microsatellite markers (N = 153), plus mitochondrial DNA (mtDNA) segments of the control region (N = 207) and cytochrome b gene (N = 116). The microsatellite data support two to three genetic clusters with biological significance. The southern populations (Argentina, Santa Catarina, and Rio Grande do Sul) presented a homogeneous genetic component, and populations from São Paulo (SP) to the north presented another component, although most presented ∼20% of the southern component. With K = 3, SP emerged as a third component while sharing some ancestry with Rio de Janeiro and Argentina. The mtDNA phylogenies revealed three main clades that diverged almost simultaneously around 250 thousand years ago (kya). Clades A and B are from central SP to the north and east, while clade C is from SP to the south and southwest. Samples from SP presented haplotypes in all three clades, sometimes in the same population. The demographic history of the species estimated with the Bayesian skyline plot of the mtDNA showed a strong expansion ∼40–20 kya and a strong reduction over the last ∼4–2 kya. Although the genetic clusters identified here deserve appropriate management strategies as conservation units, the absence of (i) concordance between the mtDNA and microsatellite data, (ii) reciprocal monophyly in the mtDNA, and (iii) clear-cut non-genetic diagnostic characters advises against considering them as different taxonomic entities. None of the previous taxonomic proposals were corroborated by our data. Our results elucidate the taxonomy of the Atlantic Forest brown howler, indicating it should be considered a monotypic species, A. guariba. We also clarify the evolutionary history of the species regarding its intraspecific genetic diversity, which is crucial information for its conservation and population management.Fil: Oklander, Luciana Inés. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; ArgentinaFil: Fernández, Gabriela Paula. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; ArgentinaFil: Machado, Stela. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; ArgentinaFil: Caputo, Mariela. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; ArgentinaFil: Hirano, Zelinda M. B.. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Rylands, Anthony B.. No especifíca;Fil: Neves, Leonardo G.. No especifíca;Fil: Mendes, Sérgio L.. Instituto Nacional da Mata Atlântica; BrasilFil: Pacca, Luciana G.. Instituto Chico Mendes de Conservação da Biodiversidade; BrasilFil: de Melo, Fabiano R.. Universidade Federal de Viçosa; BrasilFil: Mourthé, Italo. Pontificia Universidade Católica do Rio Grande do Sul; BrasilFil: Freitas, Thales R. O.. Universidade Federal do Rio Grande do Sul; BrasilFil: Corach, Daniel. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Microbiología, Inmunología y Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Jerusalinsky, Leandro. Universidade Federal do Rio Grande do Sul; BrasilFil: Bonatto, Sandro L.. Pontificia Universidade Católica do Rio Grande do Sul; BrasilFrontiers Media2024-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/268759Oklander, Luciana Inés; Fernández, Gabriela Paula; Machado, Stela; Caputo, Mariela; Hirano, Zelinda M. B.; et al.; Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest; Frontiers Media; Frontiers in Genetics; 15; 12-2024; 1-221664-8021CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fgene.2024.1453005/fullinfo:eu-repo/semantics/altIdentifier/doi/10.3389/fgene.2024.1453005info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:22:07Zoai:ri.conicet.gov.ar:11336/268759instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-15 14:22:08.068CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
title Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
spellingShingle Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
Oklander, Luciana Inés
mtdna
microsatelite
Platyrrhini
primates
title_short Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
title_full Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
title_fullStr Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
title_full_unstemmed Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
title_sort Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest
dc.creator.none.fl_str_mv Oklander, Luciana Inés
Fernández, Gabriela Paula
Machado, Stela
Caputo, Mariela
Hirano, Zelinda M. B.
Rylands, Anthony B.
Neves, Leonardo G.
Mendes, Sérgio L.
Pacca, Luciana G.
de Melo, Fabiano R.
Mourthé, Italo
Freitas, Thales R. O.
Corach, Daniel
Jerusalinsky, Leandro
Bonatto, Sandro L.
author Oklander, Luciana Inés
author_facet Oklander, Luciana Inés
Fernández, Gabriela Paula
Machado, Stela
Caputo, Mariela
Hirano, Zelinda M. B.
Rylands, Anthony B.
Neves, Leonardo G.
Mendes, Sérgio L.
Pacca, Luciana G.
de Melo, Fabiano R.
Mourthé, Italo
Freitas, Thales R. O.
Corach, Daniel
Jerusalinsky, Leandro
Bonatto, Sandro L.
author_role author
author2 Fernández, Gabriela Paula
Machado, Stela
Caputo, Mariela
Hirano, Zelinda M. B.
Rylands, Anthony B.
Neves, Leonardo G.
Mendes, Sérgio L.
Pacca, Luciana G.
de Melo, Fabiano R.
Mourthé, Italo
Freitas, Thales R. O.
Corach, Daniel
Jerusalinsky, Leandro
Bonatto, Sandro L.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv mtdna
microsatelite
Platyrrhini
primates
topic mtdna
microsatelite
Platyrrhini
primates
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The brown howler, Alouatta guariba, endemic to the Atlantic Forest of Brazil and Argentina, is threatened by habitat loss and fragmentation, hunting, and its susceptibility to yellow fever. Two subspecies have been recognized, but their names, validity, and geographic ranges have been controversial. We obtained samples covering the species' entire distribution in Brazil and Argentina to clarify these issues by investigating their genetic diversity and structure and assessing their evolutionary history. We analyzed, for the first time, a set of ten microsatellite markers (N = 153), plus mitochondrial DNA (mtDNA) segments of the control region (N = 207) and cytochrome b gene (N = 116). The microsatellite data support two to three genetic clusters with biological significance. The southern populations (Argentina, Santa Catarina, and Rio Grande do Sul) presented a homogeneous genetic component, and populations from São Paulo (SP) to the north presented another component, although most presented ∼20% of the southern component. With K = 3, SP emerged as a third component while sharing some ancestry with Rio de Janeiro and Argentina. The mtDNA phylogenies revealed three main clades that diverged almost simultaneously around 250 thousand years ago (kya). Clades A and B are from central SP to the north and east, while clade C is from SP to the south and southwest. Samples from SP presented haplotypes in all three clades, sometimes in the same population. The demographic history of the species estimated with the Bayesian skyline plot of the mtDNA showed a strong expansion ∼40–20 kya and a strong reduction over the last ∼4–2 kya. Although the genetic clusters identified here deserve appropriate management strategies as conservation units, the absence of (i) concordance between the mtDNA and microsatellite data, (ii) reciprocal monophyly in the mtDNA, and (iii) clear-cut non-genetic diagnostic characters advises against considering them as different taxonomic entities. None of the previous taxonomic proposals were corroborated by our data. Our results elucidate the taxonomy of the Atlantic Forest brown howler, indicating it should be considered a monotypic species, A. guariba. We also clarify the evolutionary history of the species regarding its intraspecific genetic diversity, which is crucial information for its conservation and population management.
Fil: Oklander, Luciana Inés. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; Argentina
Fil: Fernández, Gabriela Paula. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina
Fil: Machado, Stela. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina
Fil: Caputo, Mariela. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina
Fil: Hirano, Zelinda M. B.. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Servicio de Huellas Digitales Genéticas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Rylands, Anthony B.. No especifíca;
Fil: Neves, Leonardo G.. No especifíca;
Fil: Mendes, Sérgio L.. Instituto Nacional da Mata Atlântica; Brasil
Fil: Pacca, Luciana G.. Instituto Chico Mendes de Conservação da Biodiversidade; Brasil
Fil: de Melo, Fabiano R.. Universidade Federal de Viçosa; Brasil
Fil: Mourthé, Italo. Pontificia Universidade Católica do Rio Grande do Sul; Brasil
Fil: Freitas, Thales R. O.. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Corach, Daniel. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Microbiología, Inmunología y Biotecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Jerusalinsky, Leandro. Universidade Federal do Rio Grande do Sul; Brasil
Fil: Bonatto, Sandro L.. Pontificia Universidade Católica do Rio Grande do Sul; Brasil
description The brown howler, Alouatta guariba, endemic to the Atlantic Forest of Brazil and Argentina, is threatened by habitat loss and fragmentation, hunting, and its susceptibility to yellow fever. Two subspecies have been recognized, but their names, validity, and geographic ranges have been controversial. We obtained samples covering the species' entire distribution in Brazil and Argentina to clarify these issues by investigating their genetic diversity and structure and assessing their evolutionary history. We analyzed, for the first time, a set of ten microsatellite markers (N = 153), plus mitochondrial DNA (mtDNA) segments of the control region (N = 207) and cytochrome b gene (N = 116). The microsatellite data support two to three genetic clusters with biological significance. The southern populations (Argentina, Santa Catarina, and Rio Grande do Sul) presented a homogeneous genetic component, and populations from São Paulo (SP) to the north presented another component, although most presented ∼20% of the southern component. With K = 3, SP emerged as a third component while sharing some ancestry with Rio de Janeiro and Argentina. The mtDNA phylogenies revealed three main clades that diverged almost simultaneously around 250 thousand years ago (kya). Clades A and B are from central SP to the north and east, while clade C is from SP to the south and southwest. Samples from SP presented haplotypes in all three clades, sometimes in the same population. The demographic history of the species estimated with the Bayesian skyline plot of the mtDNA showed a strong expansion ∼40–20 kya and a strong reduction over the last ∼4–2 kya. Although the genetic clusters identified here deserve appropriate management strategies as conservation units, the absence of (i) concordance between the mtDNA and microsatellite data, (ii) reciprocal monophyly in the mtDNA, and (iii) clear-cut non-genetic diagnostic characters advises against considering them as different taxonomic entities. None of the previous taxonomic proposals were corroborated by our data. Our results elucidate the taxonomy of the Atlantic Forest brown howler, indicating it should be considered a monotypic species, A. guariba. We also clarify the evolutionary history of the species regarding its intraspecific genetic diversity, which is crucial information for its conservation and population management.
publishDate 2024
dc.date.none.fl_str_mv 2024-12
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/268759
Oklander, Luciana Inés; Fernández, Gabriela Paula; Machado, Stela; Caputo, Mariela; Hirano, Zelinda M. B.; et al.; Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest; Frontiers Media; Frontiers in Genetics; 15; 12-2024; 1-22
1664-8021
CONICET Digital
CONICET
url http://hdl.handle.net/11336/268759
identifier_str_mv Oklander, Luciana Inés; Fernández, Gabriela Paula; Machado, Stela; Caputo, Mariela; Hirano, Zelinda M. B.; et al.; Phylogeography, taxonomy, and conservation of the endangered brown howler monkey, Alouatta guariba (Primates, Atelidae), of the Atlantic Forest; Frontiers Media; Frontiers in Genetics; 15; 12-2024; 1-22
1664-8021
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fgene.2024.1453005/full
info:eu-repo/semantics/altIdentifier/doi/10.3389/fgene.2024.1453005
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https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
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dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
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reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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