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Mitogenomic Phylogeny of Callithrix with Special Focus on Human Transferred Taxa

View ORCID ProfileJoanna Malukiewicz, Reed A. Cartwright, Nelson H.A. Curi, Jorge A. Dergam, Claudia S. Igayara, Silvia B. Moreira, Camila V. Molina, Patricia A. Nicola, Angela Noll, Marcello Passamani, Luiz C.M. Pereira, Alcides Pissinatti, Carlos R. Ruiz-Miranda, Daniel L. Silva, Anne C. Stone, Dietmar Zinner, Christian Roos
doi: https://doi.org/10.1101/2020.08.12.247692
Joanna Malukiewicz
1Primate Genetics Laboratory, German Primate Research Center, Leibniz Institute for Primate Research, Göttingen, Germany
2Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo, SP, Brazil
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  • ORCID record for Joanna Malukiewicz
  • For correspondence: jmalukiewicz@dpz.eu
Reed A. Cartwright
3School of Life Sciences and The Biodesign Institute, Arizona State University, Tempe AZ, USA
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Nelson H.A. Curi
4Ecologia, Epidemiologia e Medicina da Conservação, Departamento de Medicina Veterinária, Unilavras, Lavras, MG Brazil
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Jorge A. Dergam
5Department of Animal Biology, Federal University of Viçosa, Viçosa, MG Brazil
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Claudia S. Igayara
6Guarulhos Municipal Zoo, Guarulhos, SP, Brazil
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Silvia B. Moreira
7Centro de Primatologia do Rio de Janeiro, Guapimirim, RJ, Brazil
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Camila V. Molina
8Programa de Interunidades em Biotecnologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP Brazil
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Patricia A. Nicola
9Programa de Pós-Graduação, Ciências da Saúde e Biológicas, Universidade Federal do Vale do São Francisco, Petrolina, PE, Brazil
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Angela Noll
1Primate Genetics Laboratory, German Primate Research Center, Leibniz Institute for Primate Research, Göttingen, Germany
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Marcello Passamani
10Laboratório de Ecologia e Conservação de Mamíferos, Departamento de Biologia, Universidade, Federal de Lavras, Lavras, MG, Brazil
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Luiz C.M. Pereira
11Centro de Conservação e Manejo de Fauna da Caatinga, Universidade Federal do Vale do São Francisco, Petrolina PE, Brazil
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Alcides Pissinatti
7Centro de Primatologia do Rio de Janeiro, Guapimirim, RJ, Brazil
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Carlos R. Ruiz-Miranda
12Laboratorio das Ciências Ambientais, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes RJ,, Brazil
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Daniel L. Silva
13Núcleo de Pesquisas em Ciências Biológicas - NUPEB, Federal University of Ouro Preto, Ouro Preto, MG, Brazil
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Anne C. Stone
14School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA
15Institute of Human Origins, Arizona State University, Tempe, Arizona, USA
16Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, USA
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Dietmar Zinner
17Cognitive Ethology Laboratory, German Primate Research Center, Leibniz Institute for Primate Research, Göttingen, Germany
18Leibniz Science Campus Primate Cognition, Göttingen, Germany
19Department of Primate Cognition, Georg-August-University, Göttingen, Germany
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Christian Roos
1Primate Genetics Laboratory, German Primate Research Center, Leibniz Institute for Primate Research, Göttingen, Germany
20Gene Bank of Primates, German Primate Research Center, Leibniz Institute for Primate Research, Göttingen, Germany
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Abstract

Background Callithrix marmosets are a relatively young non-human primate radiation, whose phylogeny is not yet full 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 in this study to reconstruct a robust Callithrix phylogeny and divergence time estimates, as well as identify autochthonous and allochthonous Callithrix mitogenome lineages across Brazil. 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 mtDNA genomes to analyze five Callithrix species in total.

Results We report the complete sequence and organization of the C. aurita mtDNA genome. Phylogenetic analyses showed that C. aurita was the first to diverge within Callithrix 3.54 million years ago (MYA), while C. jacchus and C. penicillata lineages diverged most recently 0.5 MYA 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 geographic 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 allochtonous 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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • cartwright{at}asu.edu, nelsoncuri{at}hotmail.com, dergam{at}ufv.br, claudiaigayara{at}uol.com.br, silviabm.inea{at}gmail.com, camolina.vet{at}gmail.com, patricia.nicola{at}univasf.edu.br, anoll{at}dpz.eu, mpassamani{at}ufla.br, luiz.pereira{at}univasf.edu.br, alcidespissinatti{at}gmail.com, cruiz{at}uenf.br, silvadaniellucas{at}gmail.com, acstone{at}asu.edu, dzinner{at}gwdg.de, croos{at}dpz.eu

  • https://github.com/Callithrix-omics/Callithrix_mtDNA

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Mitogenomic Phylogeny of Callithrix with Special Focus on Human Transferred Taxa
Joanna Malukiewicz, Reed A. Cartwright, Nelson H.A. Curi, Jorge A. Dergam, Claudia S. Igayara, Silvia B. Moreira, Camila V. Molina, Patricia A. Nicola, Angela Noll, Marcello Passamani, Luiz C.M. Pereira, Alcides Pissinatti, Carlos R. Ruiz-Miranda, Daniel L. Silva, Anne C. Stone, Dietmar Zinner, Christian Roos
bioRxiv 2020.08.12.247692; doi: https://doi.org/10.1101/2020.08.12.247692
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Mitogenomic Phylogeny of Callithrix with Special Focus on Human Transferred Taxa
Joanna Malukiewicz, Reed A. Cartwright, Nelson H.A. Curi, Jorge A. Dergam, Claudia S. Igayara, Silvia B. Moreira, Camila V. Molina, Patricia A. Nicola, Angela Noll, Marcello Passamani, Luiz C.M. Pereira, Alcides Pissinatti, Carlos R. Ruiz-Miranda, Daniel L. Silva, Anne C. Stone, Dietmar Zinner, Christian Roos
bioRxiv 2020.08.12.247692; doi: https://doi.org/10.1101/2020.08.12.247692

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