Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan-Amazonian diversification of a lowland primateby Jessica W. Lynch Alfaro, Jean P. Boubli, Fernanda P. Paim, Camila C. Ribas, Maria Nazareth F. da Silva, Mariluce R. Messias, Fabio Röhe, Michelle P. Mercês, José S. Silva Júnior, Claudia R. Silva, Gabriela M. Pinho, Gohar Koshkarian, Mai T.T. Nguyen, Maria L. Harada, Rafael M. Rabelo, Helder L. Queiroz, Michael E. Alfaro, Izeni P. Farias

Molecular Phylogenetics and Evolution

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Year
2015
DOI
10.1016/j.ympev.2014.09.004
Subject
Molecular Biology / Ecology, Evolution, Behavior and Systematics / Genetics

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Accepted Manuscript

Biogeography of squirrel monkeys (genus Saimiri): south-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate

J.W. Lynch Alfaro, J.P. Boubli, F.P. Paim, C.C. Ribas, M. Nazareth, M. Messias,

F. Röhe, M.P. Mercês, J.d.S.e Silva Jr., C.R. Silva, G.M. Pinho, G. Koshkarian,

M.T.T. Nguyen, M.L. Harada, R.M. Rabelo, H.L. Queiroz, M.E. Alfaro, I. Farias

PII: S1055-7903(14)00316-9

DOI: http://dx.doi.org/10.1016/j.ympev.2014.09.004

Reference: YMPEV 5014

To appear in: Molecular Phylogenetics and Evolution

Received Date: 1 October 2013

Revised Date: 2 August 2014

Accepted Date: 9 September 2014

Please cite this article as: Lynch Alfaro, J.W., Boubli, J.P., Paim, F.P., Ribas, C.C., Nazareth, M., Messias, M.,

Röhe, F., Mercês, M.P., Silva, J.d.S.e Jr., Silva, C.R., Pinho, G.M., Koshkarian, G., Nguyen, M.T.T., Harada, M.L.,

Rabelo, R.M., Queiroz, H.L., Alfaro, M.E., Farias, I., Biogeography of squirrel monkeys (genus Saimiri): southcentral Amazon origin and rapid pan-Amazonian diversification of a lowland primate, Molecular Phylogenetics and

Evolution (2014), doi: http://dx.doi.org/10.1016/j.ympev.2014.09.004

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. 1

Biogeography of squirrel monkeys (genus Saimiri): south-central Amazon origin and rapid pan-Amazonian diversification of a lowland primate

J. W. Lynch Alfaro1,2,*, J. P. Boubli3,4, F. P. Paim5, C. C. Ribas4, M. Nazareth4, M.

Messias6, F. Röhe 7, M. P. Mercês8, J. d. S. e Silva Jr. 8, C. R. Silva9, G. M. Pinho10, G.

Koshkarian11, M. T. T. Nguyen11, M. L. Harada12, R. M. Rabelo4,5, H. L. Queiroz5, M. E.

Alfaro11, I. Farias10 1Institute for Society and Genetics, University of California, Los Angeles, CA, United

States jlynchalfaro@ucla.edu 2Department of Anthropology, University of California, Los Angeles, CA, United States 3

School of Environment and Life Sciences, University of Salford, UK

J.P.Boubli@salford.ac.uk 4Instituto Nacional de Pesquisas da Amazonia (INPA), Manaus, AM, Brazil camilaribas@gmail.com, mndasilva@gmail.com 5Instituto de Desenvolvimento Sustentável Mamirauá, Estrada do Bexiga 2584, cep: 69470-000, Tefé, AM Brazil fernanda@Mamirauá.org.br, rmrabelo@gmail.com, helder@Mamirauá.org.br 6Universidade Federal de Rondônia, UNIR, Porto Velho, Rondônia, RO, Brazil; and

Rede Bionorte - Projeto CONBio – Amazônia

Meridional. messias.malu@gmail.com 7Wildlife Conservation Society, Manaus, Brazil fabio@gmail.com 8Museu Paraense Emilio Goeldi, Belém, Brazil cazuza.junior@gmail.com, michelleMercês@yahoo.com.br 9

Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá (IEPA), Macapa,

Amapa, AP, Brazil crsilva.ap@gmail.com 10Universidade Federal do Amazonas UFAM, Manaus, AM, Brazil gabriela.m.pinho@gmail.com, izeni@evoamazon.net 11Department of Ecology and Evolutionary Biology, University of California, Los

Angeles, CA, United States gohark1989@ucla.edu, mttn.pro@gmail.com, michaelalfaro@ucla.edu 12Universidade Federal do Pará, Belém, PA, Brazil harada@ufpa.com.br *corresponding author: Jessica Lynch Alfaro, 1321 Rolfe Hall, Institute for Society and

Genetics, University of California--Los Angeles, Los Angeles CA 90095, USA, (310) 463-1409, jlynchalfaro@ucla.edu 2

HIGHLIGHTS *Modern Saimiri origin was the south-central Amazon, in Rondônia and Inambari centers *The Amazon River has limited squirrel monkey dispersal over the last 1 million years *Pleistocene river formation and climate fluctuations affected Saimiri speciation *Late Pleistocene glacial cycles and human intervention have caused secondary contact *Saimiri mitochondrial DNA phylogeny is discordant with Gothic vs. Roman division 3

ABSTRACT

The squirrel monkey, Saimiri, is a pan-Amazonian Pleistocene radiation. We use statistical phylogeographic methods to create a mitochondrial DNA-based timetree for 118 squirrel monkey samples across 68 localities spanning all Amazonian centers of endemism, with the aim of better understanding (1) the effects of rivers as barriers to dispersal and distribution; (2) the area of origin for modern Saimiri; (3) whether ancestral

Saimiri was a lowland lake-affiliated or an upland forest taxa; and (4) the effects of

Pleistocene climate fluctuation on speciation. We also use our topology to help resolve current controversies in Saimiri taxonomy and species relationships. The Rondônia and

Inambari centers in the southern Amazon were recovered as the most likely areas of origin for Saimiri. The Amazon River proved a strong barrier to dispersal, and squirrel monkey expansion and diversification was rapid, with all speciation events estimated to occur between 1.4 and 0.6 Ma, predating the last three glacial maxima and eliminating climate extremes as the main driver of squirrel monkey speciation. Saimiri expansion was concentrated first in central and western Amazonia, which according to the "Young

Amazon" hypothesis was just becoming available as floodplain habitat with the draining of the Amazon Lake. Squirrel monkeys also expanded and diversified east, both north and south of the Amazon, coincident with the formation of new rivers. This evolutionary history is most consistent with a Young Amazon Flooded Forest Taxa model, suggesting

Saimiri has always maintained a lowland wetlands niche and was able to greatly expand its range with the transition from a lacustrine to a riverine system in Amazonia. Saimiri vanzolinii was recovered as the sister group to one clade of Saimiri ustus, discordant with the traditional Gothic versus Roman morphological division of squirrel monkeys. We 4 also found paraphyly within each of the currently recognized species: S. sciureus, S. ustus, and S. macrodon. We discuss evidence for taxonomic revision within the genus