Molecular phylogenetic inference of the howler monkey radiation (Primates: Alouatta )
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ORIGINAL ARTICLE
Molecular phylogenetic inference of the howler monkey radiation (Primates: Alouatta) Esmeralda D. Doyle1 · Ivan Prates1,2 · Iracilda Sampaio3 · Celia Koiffmann4 · Wilson Araujo Silva Jr.5 · Ana Carolina Carnaval1,6 · Eugene E. Harris7 Received: 22 February 2020 / Accepted: 3 August 2020 © Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2020
Abstract Howler monkeys (Alouatta), comprising between nine and 14 species and ranging from southern Mexico to northern Argentina, are the most widely distributed platyrrhines. Previous phylogenetic studies of howlers have used chromosomal and morphological characters and a limited number of molecular markers; however, branching patterns conflict between studies or remain unresolved. We performed a new phylogenetic analysis of Alouatta using both concatenated and coalescent-based species tree approaches based on 14 unlinked non-coding intergenic nuclear regions. Our taxon sampling included five of the seven South American species (Alouatta caraya, Alouatta belzebul, Alouatta guariba, Alouatta seniculus, Alouatta sara) and the two recognized species from Mesoamerica (Alouatta pigra, Alouatta palliata). Similarly to previous studies, our phylogenies supported a Mesoamerican clade and a South American clade. For the South American howlers, both methods recovered the Atlantic Forest endemic A. guariba as sister to all remaining South American species, albeit with moderate support. Moreover, we found no support for the previously proposed sister relationship between A. guariba and A. belzebul. For the first time, a clade composed of A. sara and A. caraya was identified. The relationships among the other South American howlers, however, were not fully supported. Our estimates for divergence times within Alouatta are generally older compared to estimates in earlier studies. However, they conform to recent studies proposing a Miocene age for the Isthmus of Panama and for the uplift of the northern Andes. Our results also point to an early genetic isolation of A. guariba in the Atlantic Forest, in agreement with the hypothesis of biotic exchange across South American rain forests in the Miocene. Collectively, these findings contribute to a better understanding of the diversification processes among howler monkey species; however, they also suggest that further comprehension of the evolutionary history of the Alouatta radiation will rely on broadened taxonomic, geographic, and genomic sampling. Keywords Alouatta · Molecular phylogeny · Multi-locus · Systematics · Primates
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10329-020-00854-x) contains supplementary material, which is available to authorized users. * Eugene E. Harris [email protected] 1
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Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil
Department of Biology, City College of New York, New York, NY, USA
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Department of Ecology and Evolutionary B
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