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Genetic Diversity and Insights into the Distribution of Brown Howler Monkeys (Alouatta guariba Group) (Atelidae, Alouattinae)

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Abstract

The assessment of genetic diversity and karyotypes can help to identify new species and taxonomic units and contribute to species conservation. Ecological niche modeling can be used to predict species distribution and to estimate the impact of climate changes on its survival. The Alouatta guariba group is one of the most threatened primates in the Americas, with two endemic Atlantic Forest subspecies: A. g. guariba and A. g. clamitans, referred to as Northern and Southern populations, respectively. Although extensively studied, the distribution and the genetic diversity of these subspecies remains unclear. We assessed species relationships and genetic diversity in the A. guariba group and evaluated the potential future distribution of populations. We sequenced the mitochondrial cytochrome b gene of 14 captive and 108 free-living individuals to generate a maximum likelihood phylogenetic tree and median-joining haplotype network and to estimate the nucleotide diversity between the taxa. We conducted neutrality tests to test for population expansion. We also linked ten new karyotypes, obtained from cell cultures from blood samples of captive individuals, with the positions of the clades in the gene tree. Finally, we used ecological niche modeling to predict the potential distribution of the Northern and Southern populations. We found three lineages within the A. guariba group: North A and North B associated with A. g. guariba, and South C associated with A. g. clamitans. The results showed that A. guariba group is a species complex, with reduced haplotype and nucleotide diversity within each lineage, compared with other Alouatta species. The neutrality tests and median-joining analysis suggest a recent diversification and expansion of each lineage, and the geographical data, based on the localities of the individuals that we analyzed genetically, increase the geographic distribution of A. g. guariba, expanding the distribution farther south in southeastern Brazil than previously described. Our findings show the distribution of the A. guariba group and genetic diversity of recently expanding populations, contributing to the assessment of this Critically Endangered species. We also suggest that environmental losses and climate change are major factors in the drastic population decline of the A. guariba group.

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Data Availability

The datasets generated and analyzed during the present study were uploaded to NCBI (Accession OP985658—OP985779).

Change history

  • 01 July 2023

    A minor correction has been made in the article title.

References

  • Abreu, F. V. S., Dos Santos, E., Gomes, M. Q., Vargas, W. P., de Oliveira Passos, P. H., Nunes e Silva, C., Araújo, P. C., Pires, J. R., Romano, A. P. M., Teixeira, D. S., & Lourenço-de-Oliveira, R. (2019). Capture of Alouatta guariba clamitans for the surveillance of sylvatic yellow fever and zoonotic malaria: Which is the best strategy in the tropical Atlantic Forest? American Journal of Primatology, 81(6), e23000. https://doi.org/10.1002/ajp.23000

  • Agostini, I., Holzmann, I., & Di Bitetti, M. (2017). The brown howler monkey (Alouatta guariba clamitans) in Argentina: Current status, threats and conservation challenges. In M. Kowalewski & L. I. Oklander (Eds.), Primatology in Argentina (pp. 475–480). Sociedad Argentina para Estudio de los Mamíferos SAREM.

    Google Scholar 

  • Almeida, M. A. B., Santos, E., Cardoso, J. C., Fonseca, D. F., Noll, C. A., Silveira, V. R., Maeda, A. Y., de Souza, R. P., Kanamura, C., & Brasil, R. A. (2012). Yellow fever outbreak affecting Alouatta populations in Southern Brazil (Rio Grande do Sul State), 2008–2009. American Journal of Primatology, 74(1), 68–76. https://doi.org/10.1002/ajp.21010

    Article  PubMed  Google Scholar 

  • Ascunce, M. S., Hasson, E., Mulligan, C. J., & Mudry, M. D. (2007). Mitochondrial sequence diversity of the southernmost extant New World monkey, Alouatta Caraya. Molecular Phylogenetics and Evolution, 43(1), 202–215. https://doi.org/10.1016/j.ympev.2006.10.004

    Article  CAS  PubMed  Google Scholar 

  • Bandelt, H. J., Forster, P., & Röhl, A. (1999). A Median-joining network for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

    Article  CAS  PubMed  Google Scholar 

  • Berthet, M., Mesbahi, G., Duvot, G., Zuberbühler, K., Cäsar, C., & Bicca-Marques, J. C. (2021). Dramatic decline in a titi monkey population after the 2016–2018 sylvatic yellow fever outbreak in Brazil. American Journal of Primatology, 83(12), e23335. https://doi.org/10.1002/ajp.23335

    Article  PubMed  Google Scholar 

  • Bicca-Marques, J. C., Calegaro-Marques, C., Rylands, A. B., Strier, K. B., Mittermeier, R. A., De Almeida, M. A. B., De Castro, P. H. G., Chaves, Ó. M., Ferraz, L. P., Fortes, V. B., Hirano, Z. M. B., Jerusalinsky, L., Kowalewski, M., Martins, W. P., De Melo, F. R., Mendes, S. L., Neves, L. G., Passos, F. C., Port-Carvalho, M., … Texeira, D. S. (2017). Yellow fever threatens Atlantic forest primates. Science Advances, 3, e1600946.

    Google Scholar 

  • Bonvicino, C. R., Viana, M. C., Bueno, C., Santos, H. S., & Geise, L. (2015). Genetic diversity of Alouatta (Primates) from Brazilian Atlantic Forest. Journal of Primatology, 4(131), 2. https://doi.org/10.4172/2167-6801.1000131

    Article  Google Scholar 

  • Boubli, J. P., Byrne, H., Silva, M. N. F., José Silva-Júnior, J. S., Araújo, R. C., Bertuol, F., Gonçalves, J., Melo, F. R., Rylands, A. B., Mittermeier, R. A., Silva, F. E., Nash, S. D., Canale, G., Alencar, R. M., Rossi, R. V., Carneiro, J., Sampaio, I., Farias, I. P., Scheneider, H., & Hrbek, T. (2016). On a new species of titi monkey (Primates: Plecturocebus), from Alta Floresta, southern Amazon, Brazil. Molecular Phylogenetics and Evolution, 132, 117–137. https://doi.org/10.1016/j.ympev.2018.11.012

    Article  Google Scholar 

  • Buss, G., Bicca-Marques, J. C., Alves, S. L., Ingberman, B., Fries, B. G., Alonso, A. C., da Cunha, R. G. T., Miranda, J. M. D., de Melo, F. R., Jerusalinsky, L., Mittermeier, R. A., Cortés-Ortiz, L., & Talebi, M. (2021). Alouatta guariba ssp. clamitans (amended version of 2020 assessment). The IUCN Red List of Threatened Species, 2021, e.T39918A190419216. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T39918A190419216.en

  • Cabrera, A. (1958). Catálogo de los mamíferos de América del Sur. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”. 4(1), 1–307.

  • Cardoso Coimbra, A. P. (2015). Cytogenetic studies in Alouatta clamitans (Primates, Platyrrhini): analysis of chromosomal variability of howler monkeys from South and Southeast regions of Brazil [Master’s dissertation], University of São Paulo.

  • Chapman, C. A., Lawes, M. J., & Eeley, H. A. C. (2006). What hope for African primate diversity? African Journal of Ecology, 44, 116–133. https://doi.org/10.1111/j.1365-2028.2006.00636.x

    Article  Google Scholar 

  • Coates, D. J., Byrne, M., & Moritz, C. (2018). Genetic diversity and conservation units: Dealing with the species-population continuum in the age of genomics. Frontiers in Ecology and Evolution, 6, 165. https://doi.org/10.3389/fevo.2018.00165

    Article  Google Scholar 

  • Collins, M., Knutti, R., Arblaster, J., Dufresne, J.-L., Fichefet, T., Friedlingstein, P., Gao, X., Gutowski, W. J., Johns, T., Krinner, G., Shongwe, M., Tebaldi, C., Weaver, A. J., Wehner, M. F., Allen, M. R., Andrews, T., Beyerle, U., Bitz, C. M., Bony, S., & Booth, B. B. B. (2013). Long-term climate change: Projections, commitments and irreversibility. In T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, & P. M. Midgley (Eds.), Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press.

  • Cortés-Ortiz, L., Bermingham, E., Rico, C., Rodríguez-Luna, E., Sampaio, I., & Ruiz-Garcia, M. (2003). Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution, 26(1), 64–81. https://doi.org/10.1016/S1055-7903(02)00308-1

    Article  PubMed  Google Scholar 

  • Cortés-Ortiz, L., Rylands, A. B., & Mittermeier, R. A. (2015a). The taxonomy of howler monkeys: integrating old and new knowledge from morphological and genetic studies. In M. Kowalewski, P. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys (pp. 55–84). Developments in primatology: progress and prospects. Springer. https://doi.org/10.1007/978-1-4939-1957-4_3

  • Cortés-Ortiz, L., Agostini, I., Aguiar, L. M., Kelaita, M., Silva, F. E., & Bicca-Marques, J. C. (2015b). Hybridization in howler monkeys: Current understanding and future directions. In M. Kowalewski, P. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys (pp. 107–131). Developments in primatology: progress and prospects. Springer. https://doi.org/10.1007/978-1-4939-1957-4_5

  • Costa-Araújo, R., Silva, J. S., Boubli, J. P., Rossi, R. V., Canale, G. R., Melo, F. R., Bertuol, F., Silva, F. E., Silva, D. A., Nash, S. D., Sampaio, I., Farias, I. P., & Hrbek, T. (2021). An integrative analysis uncovers a new, pseudo-cryptic species of Amazonian marmoset (Primates: Callitrichidae: Mico) from the arc of deforestation. Scientific Reports, 11, 15665. https://doi.org/10.1038/s41598-021-93943-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Culot, L., Pereira, L. A., Agostini, I., de Almeida, M. A. B., Alves, R. S. C., Aximoff, I., Bager, A., Baldovino, M. C., Bella, T. R., Bicca-Marques, J. C., Braga, C., Brocardo, C. R., Campelo, A. K. N., Canale, G. R., Cardoso, J. C., Carrano, E., Casanova, D. C., Cassano, C. R., Castro, E., & Galetti, M. (2019). Atlantic-primates: a dataset of communities and occurrences of primates in the Atlantic Forests of South America. Ecology, 100(1), e02525. https://doi.org/10.1002/ecy.2525

    Article  PubMed  Google Scholar 

  • Dalponte, J. C., Silva, F. E., & Silva, J. S., Jr. (2014). New species of titi monkey, genus Callicebus Thomas, 1903 (Primates, Pitheciidae), from Southern Amazonia, Brazil. Papeis Avulsos De Zoologia, 54(32), 457–472. https://doi.org/10.1590/0031-1049.2014.54.32

    Article  Google Scholar 

  • de Almeida, M. A., Dos Santos, E., Cardoso, J. D. C., da Silva, L. G., Rabelo, R. M., & Bicca-Marques, J. C. (2019). Predicting yellow fever through species distribution modeling of virus, vector, and monkeys. EcoHealth, 16(1), 95–108. https://doi.org/10.1007/s10393-018-1388-4

    Article  PubMed  Google Scholar 

  • de Mello Martins, F., Gifalli-Iughetti, C., Koiffman, C. P., & Harris, E. E. (2011). Coalescent analysis of mtDNA indicates Pleistocene divergence among three species of howler monkey (Alouatta spp.) and population subdivision within the Atlantic Coastal Forest species, A. guariba. Primates, 52(1), 77–87. https://doi.org/10.1007/s10329-010-0226-2

    Article  PubMed  Google Scholar 

  • de Oliveira, E. H. C., de Lima, M. C., Sbalqueiro, I. J., & Pissinati, A. (1998). The karyotype of Alouatta fusca clamitans from Rio de Janeiro, Brazil: Evidence for a y-autosome translocation. Genetics and Molecular Biology, 21(3). https://doi.org/10.1590/S1415-47571998000300012

  • de Oliveira, E. H. C., Suemitsu, E., da Silva, A. F., & Sbalqueiro, I. J. (2000). Geographical variation of chromosomal number in Alouatta fusca clamitans (Primates, Atelidae). Caryologia, 53(2), 163–168. https://doi.org/10.1080/00087114.2000.10589192

    Article  Google Scholar 

  • Dunn, J. C., Shedden-González, A., Cristóbal-Azkarate, J., Cortés-Ortiz, L., Rodríguez-Luna, E., & Knapp, L. A. (2014). Limited genetic diversity in the critically endangered Mexican howler monkey (Alouatta palliata mexicana) in the Selva Zoque. Mexico. Primates, 55(2), 155–160. https://doi.org/10.1007/s10329-013-0399-6

    Article  PubMed  Google Scholar 

  • Elith, J., Graham, C. H., Anderson, R. P., Dudík, M., Ferrier, S., Guisan, A., Hijmans, R. J., Huettmann, F., Leathwick, J. R., Lehmann, A., Li, J., Lohmann, L. G., Loiselle, B. A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., Overton, J. M. C., Peterson, A. T., … Zimmermann, N. E. (2006). Novel methods improve prediction of species’ distributions from occurrence data. Ecography, 29, 129–151. https://doi.org/10.1111/j.2006.0906-7590.04596.x

    Article  Google Scholar 

  • Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Di Fiore, A., Nekaris, K. A., Nijman, V., Heymann, E. W., Lambert, J. E., Rovero, F., Barelli, C., Setchell, J. M., Gillespie, T. R., Mittermeier, R. A., Arregoitia, L. V., Guinea, M., Gouveia, S., Dobrovolski, R., … Li, B. (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3(1), e1600946. https://doi.org/10.1126/sciadv.1600946

    Article  PubMed  PubMed Central  Google Scholar 

  • Estrada, A., Garber, P. A., Mittermeier, R. A., Wich, S., Gouveia, S., Dobrovolski, R., Nekaris, K. A. I., Nijman, V., Rylands, A. B., Maisels, F., Williamson, E. A., Bicca-Marques, J., Fuentes, Jerusalinsky, L., Johnson, S., Melo, F. R., Oliveira, L., Schitzer, C., Ross, C., … Setiawan, A. (2018). Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation. PeerJ, 6, e4869. https://doi.org/10.7717/peerj.4869

    Article  PubMed  PubMed Central  Google Scholar 

  • Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315. https://doi.org/10.1002/joc.5086

    Article  Google Scholar 

  • Frankham, R., Ballou, S. E. J. D., Briscoe, D. A., & Ballou, J. D. (2002). Introduction to conservation genetics. Cambridge University Press.

    Book  Google Scholar 

  • Freire Filho, R., & Palmeirim, J. M. (2020). Potential distribution of and priority conservation areas for the endangered Caatinga howler monkey Alouatta ululata in north-eastern Brazil. Oryx, 54(6), 794–802. https://doi.org/10.1017/S0030605318001084

    Article  Google Scholar 

  • GBIF.org (2021). GBIF Home Page. Available from: https://www.gbif.org. Accessed 17 March 2021.

  • Gifalli-Iughetti, C. (2008). Evolução cromossômica: Estudo da variabilidade cariotípica em Platyrrhini e das homeologias e sintenias com cromossomos humanos [unpublished doctoral dissertation]. Universidade de São Paulo.

  • Gregorin, R. (2006). Taxonomia e variação geográfica das espécies do gênero Alouatta Lacépède (Primates, Atelidae) no Brasil. Revista Brasileira De Zoologia, 23(1), 64–144. https://doi.org/10.1590/S0101-81752006000100005

    Article  Google Scholar 

  • Gualda-Barros, J., Nascimento, F. O., & Amaral, M. K. (2012). A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papeis Avulsos De Zoologia, 52(23), 261–279. https://doi.org/10.1590/S0031-10492012002300001

    Article  Google Scholar 

  • Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3), 307–321. https://doi.org/10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  • Hansen, M. C., Potapov, P. V., Moore, R., Hancher, M., Turubanova, S. A., Tyukavina, A., Thau, D., Stehman, S. V., Goetz, S. J., Loveland, T. R., Kommareddy, A., Egorov, A., Chini, L., Justice, C. O., & Townshend, J. R. G. (2013). High-resolution global maps of 21st-Century forest cover change. Science, 342(6160), 850–853. https://doi.org/10.1126/science.1244693

    Article  CAS  PubMed  Google Scholar 

  • Harding, K. C., Härkönen, T., & Caswell, H. (2002). The 2002 European seal plague: Epidemiology and population consequences. Ecology Letters, 5(6), 696–704. https://doi.org/10.1046/j.1461-0248.2002.00390.x

    Article  Google Scholar 

  • Harris, E., Gifalli-Iughetti, C., Hirano, Z., & Koiffmann, C. (2005). Cytochrome b sequences show subdivision between populations of the brown howler monkey (Alouatta guariba) from Rio de Janeiro and Santa Catarina. Brazil. Neotropical Primates, 13(2), 16–21. https://doi.org/10.1896/1413-4705.13.2.16

    Article  Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology: A Journal of the Royal Meteorological Society, 25(15), 1965–1978. https://doi.org/10.1002/joc.1276

    Article  Google Scholar 

  • Hijmans, R. J., Phillips, S., Leathwick, J., Elith, J., & Hijmans, M. R. J. (2017). Package ‘dismo.’ Circles, 9(1), 1–68.

    Google Scholar 

  • Hijmans, R. J., Van Etten, J., Cheng, J., Mattiuzzi, M., Sumner, M., Greenberg, J. A., Lamigueiro, O. P., Bevan, A., Racine, E. B., Shortridge, A., & Hijmans, M. R. J. (2015). Package ‘raster’. R package, 734.

  • Hoang, D. T., Chernomor, O., Von Haeseler, A., Minh, B. Q., & Vinh, L. S. (2018). UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35(2), 518–522. https://doi.org/10.1093/molbev/msx281

    Article  CAS  PubMed  Google Scholar 

  • Hoban, S., Campbell, C. D., da Silva, J. M., Ekblom, R., Funk, W. C., Garner, B. A., Godoy, J. A., Kershaw, F., MacDonald, A. J., Mergeay, J., Minter, M., O’Brien, D., Vinas, I. P., Pearson, S. K., Pérez-Espona, S., Potter, K. M., Russo, I.-R.M., Segelbacher, G., Vernesi, C., & Hunter, M. E. (2021). Genetic diversity is considered important but interpreted narrowly in country reports to the convention on biological diversity: Current actions and indicators are insufficient. Biological Conservation, 261, 109233. https://doi.org/10.1016/j.biocon.2021.109233

    Article  Google Scholar 

  • Holzmann, I., Agostini, I., DeMatteo, K., Areta, J. I., Merino, M. L., & Di Bitetti, M. S. (2015). Using species distribution modeling to assess factors that determine the distribution of two parapatric howlers (Alouatta spp.) in South America. International Journal of Primatology, 36(1), 18–32. https://doi.org/10.1007/s10764-014-9805-1

    Article  Google Scholar 

  • INPE. (2020). Instituto Nacional de Pesquisas Espaciais. Available from: http://www.inpe.br/noticias/noticia.php?Cod_Noticia=5450. Accessed 18 Jan 2022.

  • Irwin, D. M., Kocher, T. D., & Wilson, A. C. (1991). Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution, 32(2), 128–144. https://doi.org/10.1007/BF02515385

    Article  CAS  PubMed  Google Scholar 

  • James, R. A., Leberg, P. L., Quattro, J. M., & Vrijenhoek, R. C. (1997). Genetic diversity in black howler monkeys (Alouatta pigra) from Belize. American Journal of Physical Anthropology, 102(3), 329–336. https://doi.org/10.1002/(SICI)1096-8644(199703)102:3%3c329::AID-AJPA3%3e3.0.CO;2-Q

    Article  CAS  PubMed  Google Scholar 

  • Joly, S., Stevens, M. I., & van Vuuren, B. J. (2007). Haplotype networks can be misleading in the presence of missing data. Systematic Biology, 56(5), 857–862. https://doi.org/10.1080/10635150701633153

    Article  PubMed  Google Scholar 

  • Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., Von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587–589. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelaita, M. A., & Cortés-Ortiz, L. (2013). Morphological variation of genetically confirmed Alouatta pigra× A. palliata hybrids from a natural hybrid zone in Tabasco. Mexico. American Journal of Physical Anthropology, 150(2), 223–234. https://doi.org/10.1002/ajpa.22196

    Article  PubMed  Google Scholar 

  • Kinzey, W. G. (1982). Distribution of primates and forest refuges. In G. T. Prance (Ed.), Biological diversification in the tropics (pp. 455–482). Columbia Univ. Press.

    Google Scholar 

  • Koiffmann, C. P., & Saldanha, P. H. (1974). Cytogenetics of Brazilian monkeys. Journal of Human Evolution, 3(4), 275–282. https://doi.org/10.1016/0047-2484(74)90021-9

    Article  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). Mega X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machado, S. (2011). Filogeografia do Bugio Ruivo, Alouatta guariba (Primates, Atelidae). [unpublished Master’s dissertation], Pontifícia Universidade Católica do Rio Grande do Sul.

  • Marsh, L. K. (2014). A taxonomic revision of the saki monkeys, Pithecia Desmarest, 1804. Neotropical Primates, 21(1), 1–163. https://doi.org/10.1896/044.021.0101

    Article  Google Scholar 

  • Melo-Carrillo, A., Dunn, J. C., & Cortés-Ortiz, L. (2020). Low genetic diversity and limited genetic structure across the range of the critically endangered Mexican howler monkey (Alouatta palliata mexicana). American Journal of Primatology, 82(8), e23160. https://doi.org/10.1002/ajp.23160

    Article  PubMed  Google Scholar 

  • Miller, S. A., Dykes, D. D., & Polesky, H. F. (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research, 16(3), 1215. https://doi.org/10.1093/nar/16.3.1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittermeier, R. A., Reuter, K. E., Rylands, A. B., Jerusalinsky, L., Schwitzer, C., Strier, K. B., Ratsimbazafy, J., & Humle, T. (Eds.). (2022). Primates in peril: The world’s 25 most endangered primates 2022–2023. IUCN SSC Primate Specialist Group.

    Google Scholar 

  • Nabholz, B., Mauffrey, J. F., Bazin, E., Galtier, N., & Glemin, S. (2008). Determination of mitochondrial genetic diversity in mammals. Genetics, 178(1), 351–361. https://doi.org/10.1534/genetics.107.073346

    Article  PubMed  PubMed Central  Google Scholar 

  • Nascimento, F. D., Bonvicino, C. R., Da Silva, F. C. D., Schneider, M. P. C., & Seuánez, H. N. (2005). Cytochrome b polymorphisms and population structure of two species of Alouatta (Primates). Cytogenetic and Genome Research, 108(1–3), 106–111. https://doi.org/10.1159/000080808

    Article  CAS  PubMed  Google Scholar 

  • Nascimento, F. F., Bonvicino, C. R., & Seuánez, H. N. (2007). Population genetic studies of Alouatta caraya (Alouattinae, Primates): Inferences on geographic distribution and ecology. American Journal of Primatology, 69(10), 1093–1104. https://doi.org/10.1002/ajp.20423

    Article  PubMed  Google Scholar 

  • Nascimento, F. F., Bonvicino, C. R., de Oliveira, M. M., Schneider, M. P. C., & Seuánez, H. N. (2008). Population genetic studies of Alouatta belzebul from the Amazonian and Atlantic Forests. American Journal of Primatology, 70(5), 423–431. https://doi.org/10.1002/ajp.20507

    Article  CAS  PubMed  Google Scholar 

  • Neves, L. G., Jerusalinsky, L., Talebi, M., Mittermeier, R. A., Cortés-Ortiz, L., & de Melo, F. R. (2021). Alouatta guariba ssp. guariba (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2021: e.T39917A190420483. Downloaded on 05 April 2021.

  • Nguyen, L. T., Schmidt, H. A., Von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1), 268–274. https://doi.org/10.1093/molbev/msu300

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell, M. S., & Ignizio, D. A. (2012). Bioclimatic predictors for supporting ecological applications in the conterminous United States. US Geological Survey Data Series, 691(10), 4–9.

    Google Scholar 

  • Osada, N. (2015). Genetic diversity in humans and non-human primates and its evolutionary consequences. Genes & Genetic Systems, 90(3), 133–145. https://doi.org/10.1266/ggs.90.133

    Article  CAS  Google Scholar 

  • Pearson, R. G., Raxworthy, C. J., Nakamura, M., & Townsend Peterson, A. (2007). Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar. Journal of Biogeography, 34(1), 102–117. https://doi.org/10.1111/j.1365-2699.2006.01594.x

    Article  Google Scholar 

  • Peterson, A. T., Soberon, J., Pearson, R. G., Anderson, R. P., Martinez-Meyer, E., Nakamura, M., & Araujo, M. B. (2011). Ecological niches and geographic distributions. Princeton University Press.

    Book  Google Scholar 

  • Petit-Marty, N., Vázquez-Luis, M., & Hendriks, I. E. (2021). Use of the nucleotide diversity in COI mitochondrial gene as an early diagnostic of conservation status of animal species. Conservation Letters, 14(1), e12756. https://doi.org/10.1111/conl.12756

    Article  Google Scholar 

  • Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026

    Article  Google Scholar 

  • Pissinatti, A., Muniz, J. A. P. C., da Silva, K. S. M., & Andrade, M. C. R. (2016). Primatas não humanos mantidos em instalações de instituições de ensino e pesquisa científica. Resolução Normativa nº28 in CONCEA (Ed.), Guia brasileiro de produção, manutenção ou utilização de animais em atividades de ensino ou pesquisa científica (pp. 40–93). Ministério da Ciência, Tecnologia e Inovação.

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

  • Reed, D. H., & Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation Biology, 17, 230–237. https://doi.org/10.1046/j.1523-1739.2003.01236.x

    Article  Google Scholar 

  • Rezende, C. L., Scarano, F. R., Assad, E. D., Joly, C. A., Metzger, J. P., Strassburg, B. B. N., Tabarelli, M., Fonseca, G. A., & Mittermeier, R. A. (2018). From hotspot to hopespot: An opportunity for the Brazilian Atlantic Forest. Perspectives in Ecology and Conservation, 16, 208–214. https://doi.org/10.1016/j.pecon.2018.10.002

    Article  Google Scholar 

  • Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., & Hirota, M. M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142, 1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021

    Article  Google Scholar 

  • Ricklefs, R. E. (2004). A comprehensive framework for global patterns in biodiversity. Ecology Letters, 7, 1–15. https://doi.org/10.1046/j.1461-0248.2003.00554.x

    Article  Google Scholar 

  • Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., & Sánchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution, 34(12), 3299–3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  • Rylands, A. B. (2000). An assessment of the diversity of New World primates. Neotropical Primates, 8, 61–93.

    Google Scholar 

  • Rylands, A. B., & Mittermeier, R. A. (2009). The diversity of the New World primates (Platyrrhini): an annotated taxonomy. In P. A. Garber, A. Estrada, J, C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American Primates (pp. 23–54). Springer. https://doi.org/10.1007/978-0-387-78705-3_2

  • Sacchetto, L., Silva, N. I. O., Rezende, I. M. D., Arruda, M. S., Costa, T. A., de Mello, É. M., Oliveira, G. F. G., Alves, P. A., de Mendonça, V. E., Stumpp, R. G. A. V., Prado, A. I. A., Paglia, A. P., Perini, F. A., Nogueira, M. L., Kroon, E. G., de Thoisy, B., Trindade, G. S., & Drumond, B. P. (2020). Neighbor danger: Yellow fever virus epizootics in urban and urban-rural transition areas of Minas Gerais state, during 2017–2018 yellow fever outbreaks in Brazil. PLoS Neglected Tropical Diseases, 14(10), e0008658. https://doi.org/10.1371/journal.pntd.0008658

    Article  PubMed  PubMed Central  Google Scholar 

  • Salazar, L. F., Nobre, C. A., & Oyama, M. D. (2007). Climate change consequences on the biome distribution in tropical South America. Geophysical Research Letters, 34(9), L09708. https://doi.org/10.1029/2007GL029695

  • Sambrook, J., & Russell, D. W. (2001). Molecular cloning: a laboratory manual (3rd ed.). Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Steinberg, E. R., Nieves, M., & Mudry, M. D. (2014). Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta). Comparative Cytogenetics, 8(1), 43. https://doi.org/10.3897/CompCytogen.v8i1.6716

    Article  PubMed  PubMed Central  Google Scholar 

  • Steinberg, E. R., Fortes, V. B., Rossi, L. F., Murer, L., Lovato, M., Merani, M. S., & Mudry, M. D. (2017). Cytogenetic characterization of brown howler monkeys, Alouatta guariba clamitans (Atelidae, Platyrrhini): Meiotic confirmation of an X1X1X2X2X3X3/X1X2X3Y1Y2 sex chromosome system. Cytogenetic and Genome Research, 151(3), 131–140. https://doi.org/10.1159/000464375

    Article  CAS  PubMed  Google Scholar 

  • Sumner, A. T. (1972). A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research, 75, 304–306.

    Article  CAS  PubMed  Google Scholar 

  • Swets, J. A. (1988). Measuring the accuracy of diagnostic systems. Science, 240(4857), 1285–1293. https://doi.org/10.1126/science.3287615

    Article  CAS  PubMed  Google Scholar 

  • Teixeira, D. S., Bernal-Valle, S., Ramos, A. V. V., Santos, L. K. N. S. S., dos Abreu, F. V. S., Santos, E., Bandeira, J. C., & de Almeida, R. M. (2022). Capture and collection of biological samples from free-living Neotropical Primates. Primate Conservation, 36, 01–12.

    Google Scholar 

  • Urbanek, S. (2021). Package ‘rJava’. R package, 48.

  • Vincent, L. A., Peterson, T. C., Barros, V. R., Marino, M. B., Rusticucci, M., Carrasco, Ramirez, E., Alves, L. M., Ambrizzi, T., Berlato, M. A., Grimm, A. M., Marengo, J. A., Molion, L., Moncunill, D. F., Rebello, E., Anunciação, Y. M. T., Quintana, J., Santoso, J. L., Baez, J., … Karoly, D. (2005). Observed trends in indices of daily temperature extremes in South America 1960–2000. Journal of Climate, 18(23), 5011–5023. https://doi.org/10.1175/JCLI3589.1

    Article  Google Scholar 

  • Wan, Q. H., Wu, H., Fujihara, T., & Fang, S. G. (2004). Which genetic marker for which conservation genetics issue? Electrophoresis, 25(14), 2165–2176. https://doi.org/10.1002/elps.200305922

    Article  CAS  PubMed  Google Scholar 

  • Wiederholt, R., & Post, E. (2010). Tropical warming and the dynamics of endangered primates. Biology Letters, 6(2), 257–260. https://doi.org/10.1098/rsbl.2009.0710

    Article  PubMed  Google Scholar 

  • Winters, M., Devictor, V., & Schweiger, O. (2012). Phylogenetic diversity and nature conservation: Where are we? Trends in Ecology and Evolution, 28, 199–204.

    Article  Google Scholar 

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Acknowledgements

The authors are grateful to Dr. Julio Cesar Bicca-Marques and anonymous reviewers for the comments and suggestions in a previous version of this manuscript. Thanks to the veterinarian Silvia Bahadian Moreira for samples collection of Alouatta in captivity from Centro de Primatologia do Rio de Janeiro; to Department of Applied Research of Fundação Parque Zoológico de São Paulo for samples from Parque Estadual das Fontes do Ipiranga (PEFI) and the veterinarian staff; and to Danilo Simonini Teixeira and Marcelo Quintela Gomes for their support during the fieldwork in Rio de Janeiro. This study was developed thanks to scholarship awarded in part by the Coordenação de Aperfeiçoamento de Nível Superior (CAPES-88882.331370/2019-01) and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ-E-26/200.742/2019) to Cintia Povill, and from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq- 304498/2014-9 and 312446/2018-7) and FAPERJ (E26/201.200/2014 and E-26/210.047/2014) to Cibele R. Bonvicino and R. Lourenço-de-Oliveira, respectively, and Marcione B. Oliveira thanks to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, 162273/2018-5) for the PhD scholarship.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Genética, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Cintia Povill

  2. Programa de Pós-Graduação em Zoologia, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão, Rio de Janeiro, RJ, Brazil

    Marcione B. de Oliveira

  3. Laboratório de Mosquitos Transmissores de Hematozoários, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil

    Filipe Vieira Santos de Abreu & Ricardo Lourenço de Oliveira

  4. Laboratório de Evolução de Mamíferos, Departamento de Zoologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil

    Fernando Araújo Perini

  5. Universidade Federal de São Carlos, São Carlos, SP, Brazil

    Cauê Monticelli

  6. Centro de Estudos de Vertebrados Silvestres, Universidade Veiga de Almeida, Maracanã, Rio de Janeiro, RJ, Brazil

    Cecilia Bueno

  7. Centro Estadual de Vigilância em Saúde, Secretaria de Saúde do Rio Grande do Sul, Porto Alegre, RS, Brazil

    Edmilson dos Santos

  8. Centro de Primatologia do Rio de Janeiro, Guapimirim, RJ, Brazil

    Alcides Pissinatti

  9. Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, RJ, Brazil

    Cibele Rodrigues Bonvicino

  10. Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Pavilhão Lauro Travassos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brazil, 4365, Manguinhos, 21040-360, Ou 900, Rio de Janeiro, RJ, Brazil

    Cibele Rodrigues Bonvicino

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  1. Cintia Povill
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Contributions

CP conceived (lead), designed (lead), performed the experiments (lead), analyzed the data (lead), writing, review and editing (lead). CRB conceived (equal), funding acquisition (lead), writing review & editing (equal). MBO analyzed and wrote spatial distribution (lead), writing review and editing (equal). FVSA performed the experiments (equal). FVSA, RLO, ES, FAP, CB, CM, AP, CRB got the samples, writing review and editing (supporting), contributed to the final version (supporting).

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Correspondence to Cibele Rodrigues Bonvicino.

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Handling Editor: Julio Cesar Bicca-Marques

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Povill, C., de Oliveira, M.B., de Abreu, F.V.S. et al. Genetic Diversity and Insights into the Distribution of Brown Howler Monkeys (Alouatta guariba Group) (Atelidae, Alouattinae). Int J Primatol 44, 517–539 (2023). https://doi.org/10.1007/s10764-023-00352-z

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