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

[Display omitted] •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 cy...

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Published in:Molecular phylogenetics and evolution 2015-01, Vol.82, p.436-454
Main Authors: Lynch Alfaro, Jessica W., Boubli, Jean P., Paim, Fernanda P., Ribas, Camila C., Silva, Maria Nazareth F. da, Messias, Mariluce R., Röhe, Fabio, Mercês, Michelle P., Silva Júnior, José S., Silva, Claudia R., Pinho, Gabriela M., Koshkarian, Gohar, Nguyen, Mai T.T., Harada, Maria L., Rabelo, Rafael M., Queiroz, Helder L., Alfaro, Michael E., Farias, Izeni P.
Format: Article
Language:English
Subjects:
Animals
Bayes Theorem
Biological Evolution
Cebidae
DNA, Mitochondrial - genetics
Ecosystem
Models, Genetic
Phylogenetics
Phylogeny
Phylogeography
Pleistocene diversification
Refugia hypothesis
River barriers
Saimiri - classification
Sequence Analysis, DNA
South America
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Summary:[Display omitted] •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. 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 0.6Ma, 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 vs. Roman morphological division of squirrel monkeys. We 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
ISSN:1055-7903
1095-9513
DOI:10.1016/j.ympev.2014.09.004