Joanna Malukiewicz1,2, Reed A Cartwright3, Nelson H A Curi4, Jorge A Dergam5, Claudia S Igayara6, Silvia B Moreira7, Camila V Molina8,9, Patricia A Nicola10, Angela Noll11, Marcello Passamani12, Luiz C M Pereira13, Alcides Pissinatti7, Carlos R Ruiz-Miranda14, Daniel L Silva15, Anne C Stone16,17,18, Dietmar Zinner19,20,21, Christian Roos11,22. 1. Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany. jmalukiewicz@dpz.eu. 2. Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo, SP, Brazil. jmalukiewicz@dpz.eu. 3. School of Life Sciences and The Biodesign Institute, Arizona State University, Tempe, AZ, USA. 4. Ecologia, Epidemiologia e Medicina da Conservação, Departamento de Medicina Veterinária, Unilavras, Lavras, MG, Brazil. 5. Department of Animal Biology, Federal University of Viçosa, Viçosa, MG, Brazil. 6. Guarulhos Municipal Zoo, Guarulhos, SP, Brazil. 7. Centro de Primatologia do Rio de Janeiro, Guapimirim, RJ, Brazil. 8. Programa de Interunidades em Biotecnologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, SP, Brazil. 9. Scientific Platform Pasteur, Universidade de São Paulo, São Paulo, Brazil. 10. Programa de Pós-Graduação, Ciências da Saúde e Biológicas, Universidade Federal do Vale do São Francisco, Petrolina, PE, Brazil. 11. Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany. 12. Laboratório de Ecologia e Conservação de Mamíferos, Departamento de Biologia, Universidade Federal de Lavras, Lavras, MG, Brazil. 13. Centro de Conservação e Manejo de Fauna da Caatinga, Universidade Federal do Vale do São Francisco, Petrolina, PE, Brazil. 14. Laboratório das Ciências Ambientais, Centro de Biociências e Biotecnologia, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, RJ, Brazil. 15. Núcleo de Pesquisas em Ciências Biológicas - NUPEB, Federal University of Ouro Preto, Ouro Preto, MG, Brazil. 16. School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA. 17. Institute of Human Origins, Arizona State University, Tempe, AZ, USA. 18. Center for Evolution and Medicine, Arizona State University, Tempe, AZ, USA. 19. Cognitive Ethology Laboratory, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany. 20. Leibniz Science Campus Primate Cognition, Göttingen, Germany. 21. Department of Primate Cognition, Georg-August-University, Göttingen, Germany. 22. Gene Bank of Primates, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany.
Abstract
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.
BACKGROUND:Callithrixmarmosets 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.
Authors: Joanna Malukiewicz; Vanner Boere; Lisieux F Fuzessy; Adriana D Grativol; Jeffrey A French; Ita de Oliveira e Silva; Luiz C M Pereira; Carlos R Ruiz-Miranda; Yuri M Valença; Anne C Stone Journal: Am J Phys Anthropol Date: 2014-09-03 Impact factor: 2.868
Authors: Polina Perelman; Warren E Johnson; Christian Roos; Hector N Seuánez; Julie E Horvath; Miguel A M Moreira; Bailey Kessing; Joan Pontius; Melody Roelke; Yves Rumpler; Maria Paula C Schneider; Artur Silva; Stephen J O'Brien; Jill Pecon-Slattery Journal: PLoS Genet Date: 2011-03-17 Impact factor: 5.917
Authors: Steven L Chown; Kathryn A Hodgins; Philippa C Griffin; John G Oakeshott; Margaret Byrne; Ary A Hoffmann Journal: Evol Appl Date: 2014-12-09 Impact factor: 5.183
Authors: Knut Finstermeier; Dietmar Zinner; Markus Brameier; Matthias Meyer; Eva Kreuz; Michael Hofreiter; Christian Roos Journal: PLoS One Date: 2013-07-16 Impact factor: 3.240
Authors: Denise Monnerat Nogueira; Rodrigo Salles de Carvalho; Andréa Maria de Oliveira; Thiago Silva de Paula; Daniel Gomes Pereira; Alcides Pissinatti; Silvia de Oliveira Loiola; Elizeu Fagundes Carvalho; Dayse Aparecida Silva; Helena Godoy Bergallo; Ana Maria Dos Reis Ferreira Journal: Sci Rep Date: 2022-01-27 Impact factor: 4.379
Authors: Mareike C Janiak; Felipe E Silva; Robin M D Beck; Dorien de Vries; Lukas F K Kuderna; Nicole S Torosin; Amanda D Melin; Tomàs Marquès-Bonet; Ian B Goodhead; Mariluce Messias; Maria N F da Silva; Iracilda Sampaio; Izeni P Farias; Rogerio Rossi; Fabiano R de Melo; João Valsecchi; Tomas Hrbek; Jean P Boubli Journal: Mol Ecol Date: 2022-06-20 Impact factor: 6.622