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Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa

BACKGROUND: Callithrix marmosets are a relatively young primate radiation, whose phylogeny is not yet fully resolved. These primates are naturally para- and allopatric, but three species with highly invasive potential have been introduced into the southeastern Brazilian Atlantic Forest by the pet tr...

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Autores principales: Malukiewicz, Joanna, Cartwright, Reed A., Curi, Nelson H. A., Dergam, Jorge A., Igayara, Claudia S., Moreira, Silvia B., Molina, Camila V., Nicola, Patricia A., Noll, Angela, Passamani, Marcello, Pereira, Luiz C. M., Pissinatti, Alcides, Ruiz-Miranda, Carlos R., Silva, Daniel L., Stone, Anne C., Zinner, Dietmar, Roos, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8025498/
https://www.ncbi.nlm.nih.gov/pubmed/33823806
http://dx.doi.org/10.1186/s12864-021-07533-1
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author Malukiewicz, Joanna
Cartwright, Reed A.
Curi, Nelson H. A.
Dergam, Jorge A.
Igayara, Claudia S.
Moreira, Silvia B.
Molina, Camila V.
Nicola, Patricia A.
Noll, Angela
Passamani, Marcello
Pereira, Luiz C. M.
Pissinatti, Alcides
Ruiz-Miranda, Carlos R.
Silva, Daniel L.
Stone, Anne C.
Zinner, Dietmar
Roos, Christian
author_facet Malukiewicz, Joanna
Cartwright, Reed A.
Curi, Nelson H. A.
Dergam, Jorge A.
Igayara, Claudia S.
Moreira, Silvia B.
Molina, Camila V.
Nicola, Patricia A.
Noll, Angela
Passamani, Marcello
Pereira, Luiz C. M.
Pissinatti, Alcides
Ruiz-Miranda, Carlos R.
Silva, Daniel L.
Stone, Anne C.
Zinner, Dietmar
Roos, Christian
author_sort Malukiewicz, Joanna
collection PubMed
description BACKGROUND: Callithrix marmosets are a relatively young primate radiation, whose phylogeny is not yet fully resolved. These primates are naturally para- and allopatric, but three species with highly invasive potential have been introduced into the southeastern Brazilian Atlantic Forest by the pet trade. There, these species hybridize with each other and endangered, native congeners. We aimed here to reconstruct a robust Callithrix phylogeny and divergence time estimates, and identify the biogeographic origins of autochthonous and allochthonous Callithrix mitogenome lineages. We sequenced 49 mitogenomes from four species (C. aurita, C. geoffroyi, C. jacchus, C. penicillata) and anthropogenic hybrids (C. aurita x Callithrix sp., C. penicillata x C. jacchus, Callithrix sp. x Callithrix sp., C. penicillata x C. geoffroyi) via Sanger and whole genome sequencing. We combined these data with previously published Callithrix mitogenomes to analyze five Callithrix species in total. RESULTS: We report the complete sequence and organization of the C. aurita mitogenome. Phylogenetic analyses showed that C. aurita was the first to diverge within Callithrix 3.54 million years ago (Ma), while C. jacchus and C. penicillata lineages diverged most recently 0.5 Ma as sister clades. MtDNA clades of C. aurita, C. geoffroyi, and C. penicillata show intraspecific geographic structure, but C. penicillata clades appear polyphyletic. Hybrids, which were identified by phenotype, possessed mainly C. penicillata or C. jacchus mtDNA haplotypes. The biogeographic origins of mtDNA haplotypes from hybrid and allochthonous Callithrix were broadly distributed across natural Callithrix ranges. Our phylogenetic results also evidence introgression of C. jacchus mtDNA into C. aurita. CONCLUSION: Our robust Callithrix mitogenome phylogeny shows C. aurita lineages as basal and C. jacchus lineages among the most recent within Callithrix. We provide the first evidence that parental mtDNA lineages of anthropogenic hybrid and allochthonous marmosets are broadly distributed inside and outside of the Atlantic Forest. We also show evidence of cryptic hybridization between allochthonous Callithrix and autochthonous C. aurita. Our results encouragingly show that further development of genomic resources will allow to more clearly elucidate Callithrix evolutionary relationships and understand the dynamics of Callithrix anthropogenic introductions into the Brazilian Atlantic Forest. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07533-1.
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spelling pubmed-80254982021-04-08 Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa Malukiewicz, Joanna Cartwright, Reed A. Curi, Nelson H. A. Dergam, Jorge A. Igayara, Claudia S. Moreira, Silvia B. Molina, Camila V. Nicola, Patricia A. Noll, Angela Passamani, Marcello Pereira, Luiz C. M. Pissinatti, Alcides Ruiz-Miranda, Carlos R. Silva, Daniel L. Stone, Anne C. Zinner, Dietmar Roos, Christian BMC Genomics Research Article BACKGROUND: Callithrix marmosets are a relatively young primate radiation, whose phylogeny is not yet fully resolved. These primates are naturally para- and allopatric, but three species with highly invasive potential have been introduced into the southeastern Brazilian Atlantic Forest by the pet trade. There, these species hybridize with each other and endangered, native congeners. We aimed here to reconstruct a robust Callithrix phylogeny and divergence time estimates, and identify the biogeographic origins of autochthonous and allochthonous Callithrix mitogenome lineages. We sequenced 49 mitogenomes from four species (C. aurita, C. geoffroyi, C. jacchus, C. penicillata) and anthropogenic hybrids (C. aurita x Callithrix sp., C. penicillata x C. jacchus, Callithrix sp. x Callithrix sp., C. penicillata x C. geoffroyi) via Sanger and whole genome sequencing. We combined these data with previously published Callithrix mitogenomes to analyze five Callithrix species in total. RESULTS: We report the complete sequence and organization of the C. aurita mitogenome. Phylogenetic analyses showed that C. aurita was the first to diverge within Callithrix 3.54 million years ago (Ma), while C. jacchus and C. penicillata lineages diverged most recently 0.5 Ma as sister clades. MtDNA clades of C. aurita, C. geoffroyi, and C. penicillata show intraspecific geographic structure, but C. penicillata clades appear polyphyletic. Hybrids, which were identified by phenotype, possessed mainly C. penicillata or C. jacchus mtDNA haplotypes. The biogeographic origins of mtDNA haplotypes from hybrid and allochthonous Callithrix were broadly distributed across natural Callithrix ranges. Our phylogenetic results also evidence introgression of C. jacchus mtDNA into C. aurita. CONCLUSION: Our robust Callithrix mitogenome phylogeny shows C. aurita lineages as basal and C. jacchus lineages among the most recent within Callithrix. We provide the first evidence that parental mtDNA lineages of anthropogenic hybrid and allochthonous marmosets are broadly distributed inside and outside of the Atlantic Forest. We also show evidence of cryptic hybridization between allochthonous Callithrix and autochthonous C. aurita. Our results encouragingly show that further development of genomic resources will allow to more clearly elucidate Callithrix evolutionary relationships and understand the dynamics of Callithrix anthropogenic introductions into the Brazilian Atlantic Forest. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07533-1. BioMed Central 2021-04-06 /pmc/articles/PMC8025498/ /pubmed/33823806 http://dx.doi.org/10.1186/s12864-021-07533-1 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Malukiewicz, Joanna
Cartwright, Reed A.
Curi, Nelson H. A.
Dergam, Jorge A.
Igayara, Claudia S.
Moreira, Silvia B.
Molina, Camila V.
Nicola, Patricia A.
Noll, Angela
Passamani, Marcello
Pereira, Luiz C. M.
Pissinatti, Alcides
Ruiz-Miranda, Carlos R.
Silva, Daniel L.
Stone, Anne C.
Zinner, Dietmar
Roos, Christian
Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa
title Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa
title_full Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa
title_fullStr Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa
title_full_unstemmed Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa
title_short Mitogenomic phylogeny of Callithrix with special focus on human transferred taxa
title_sort mitogenomic phylogeny of callithrix with special focus on human transferred taxa
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8025498/
https://www.ncbi.nlm.nih.gov/pubmed/33823806
http://dx.doi.org/10.1186/s12864-021-07533-1
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