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Phylogenetic relationships, population demography, and species delimitation of the Alouatta belzebul species complex (Atelidae: Alouattinae)

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Abstract

Howler monkeys (genus Alouatta) exhibit the most extensive distribution among platyrrhines, comprising Mesoamerican and South American species groups, with the South American group including the Brazilian endemic A. belzebul species complex encompassing A. belzebul, A. discolor, and A. ululata. We herein analyzed their phylogenetic relationship, nucleotide and haplotype diversity, and population demography based on the mitochondrial gene cytochrome b. The phylogenetic and median-joining network analyses distinguished A. discolor, distributed in the west bank of the Xingu River, from A. belzebul on the east bank. This river is a zoogeographic barrier for these species. We did not find evidence of phylogenetic structure between the A. belzebul populations of opposite banks of the Tocantins River, likely related to the changes in the position of this river to the northeast in the late Pleistocene. The A. belzebul along this river showed great morphologic and haplotype diversity, and A. belzebul from the Amazon have kept a larger population size than A. discolor. We herein describe the karyotype of A. discolor, which was similar to those described for A. ululata and A. belzebul. Our results showed two well-defined and supported clades for A. discolor and A. belzebul. However, a new assessment of A. ululata across a large distribution of sampling is required due to the lack of a clear phylogenetic structure.

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Acknowledgements

We are grateful to unknown reviewers for valuable comments that improve the quality of this manuscript. The samples herein analyzed were already available prior to this study. We are grateful to all participants of the Belo Monte faunal rescue operation and to collaborators and institutions that kindly provided Alouatta discolor samples from Vitória do Xingu and Altamira, mainly Victor Yunes, Biota Projetos e Consultoria Ambiental Ltda, Arcadis Logo, and Naturae. We are also grateful to Alcides Pissinatti and Silvia Bahadian Moreira from Centro de Pimatologia do Rio de Janeiro (CPRJ) for the A. discolor sample from Paranaíta, and to M. Marcelino, L. Jerusalinsky and G. Ferreira from Instituto Chico Mendes de Conservação da Biodiversidade-ICMBio, for A. ululata taxa identification, and A. belzebul Atlantic Forest samples. Michel B. Faria for his help with the samples from Belo Monte and Larissa Marques Borges for DNA isolation of tissue samples and sequencing of some of the samples from Vitória do Xingu. Laboratory work was supported by grants to C. R. Bonvicino (Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq 304498/2014-9 and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro—FAPERJ E26/201.200/2014), and fellowship to Cintia Povill (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES 88882.331370/2019-01and FAPERJ nota 10 E_01/2019).

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Contributions

CP conceived (lead) and designed (equal) the study; performed the experiments (lead); analyzed the data (lead); writing original draft (lead); writing review and editing (lead). MAPO analyzed Bayesian skyline plot (lead); contributed to the final version (equal). FRM obtained samples; contributed to the final version (equal). CRB conceived (equal) and designed (equal) the study; acquired funding (lead); writing review and editing (equal); contributed to the final version (equal).

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Correspondence to Cibele Rodrigues Bonvicino.

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The authors declare that they have no conflicts of interest.

Ethical approval

The samples donated for analysis in the present study were collected following the legal requirements of the ICMBio and IBAMA, the Brazilian government environmental agencies. Samples from the animals collected on the Xingu River during the faunal rescue operation at the Belo Monte hydroelectric dam were kindly donated for this research (license number 474 73/2014—2nd correction–DILIC/IBAMA).

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Povill, C., de Assis Passos Oliveira, M., de Melo, F.R. et al. Phylogenetic relationships, population demography, and species delimitation of the Alouatta belzebul species complex (Atelidae: Alouattinae). Primates 63, 65–78 (2022). https://doi.org/10.1007/s10329-021-00959-x

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  • DOI: https://doi.org/10.1007/s10329-021-00959-x

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