Skip to main content
SpringerLink
Log in

First phylogenetic analysis of Mesoamerican brocket deer Mazama pandora and Mazama temama (Cetartiodactyla: Cervidae) based on mitochondrial sequences: Implications for Neotropical deer evolution

  • Original investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Several recent studies have tried to unravel the complex evolutionary history of Neotropical cervids. However, the two Mesoamerican brocket deer Mazama pandora and M. temama have not been included in these studies and their relationship to other Neotropical cervids remains unclear. Here, we present analyses that included concatenated sequences from the mitochondrial genes ND2, Cytb, and tRNA-Pro-Control region. Our results suggest that both Mesoamerican brocket deer fall within the “red” clade, more closely related to genus Odocoileus and red brocket deer species, such as South American Mazama americana, M. bororo, M. nana, and M. rufina. We estimated that M. temama diverged from other red brocket deer ca. two MYA. Two hypothesis emerge regarding the relationship of the Yucatan brocket deer M. pandora with respect to the other Neotropical deer. The first one, based on analyses of concatenated sequences from all three genes, implies an early split from a larger clade that includes Odocoileus and other red Mazama species, with an estimated divergence time dating back to 2.7 MYA. This would suggest isolation on the Yucatan peninsula, limiting the crossing of this species into South America. The second one, based only on Cytb, places M. pandora more closely related to Odocoileus and with an estimated divergence time of ca. 1.9 MYA. This would suggest that the humid tropical forests of Mexico and Central America could have been the most likely place of origin of members of the red brocket deer clade. Deer colonization into South America occurred after the complete formation of the Panamanian land bridge in the late Pliocene, more than one ancestor of the gray brocket deer clade crossed into South America, as well as a red brocket deer ancestor and Odocoileus dispersed southward. A posterior event probably occurred when divergent ancestors of M. temama and M. pandora respectively moved northward after the split with South American red brocket deer. Our results add to the growing body of evidence calling for an extensive taxonomic revision of this group, and we concur with previous recommendations that the generic taxonomic designation of Mazama should be applied not only to the red brocket deer but also to all of the species currently recognized under the genus Odocoileus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abril, V.V., Carnelossi, E.A.G., González, S., Duarte, J.M.B., 2010. Elucidating the evolution of the red brocket deer Mazama americana complex (Artiodactyla; cervidae), Cytogenet. Genome Res. 128, 177–187.

    Article  CAS  PubMed  Google Scholar 

  • Allen, J.A., 1915. Notes on American deer of the genus Mazama, Bull. Am. Mus. Nat. Hist. 34, 521–553.

    Google Scholar 

  • Agnarsson, I., May-Collado, L.J., 2008. The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies, Mol. Phylogenet. Evol. 48, 964–985.

    Article  CAS  PubMed  Google Scholar 

  • Barrantes, G., 2009. The role of historical and local factors in determining species composition of the highland avifauna of Costa Rica and Western Panama, Int. J. Trop. Biol. 57, 333–349.

    Google Scholar 

  • Beheregaray, LB., Cooke, G.M., Chao, N.L., Landguth, E.L., 2015. Ecological speciation in the tropics: insights from comparative genetic studies in Amazonia. Front. Genet. 5, e477.

    Google Scholar 

  • Bello-Gutiérrez,J., Reyna-Hurtado, R., Wilham, J., 2010. Central American red brocket deer Mazama temama (Kerr, 1992). In: Duarte, J.M.B., González, S. (Eds.), Neotropical Cervidology. Biology and Medicine of Latin American Deer. Funep, Jaboticabal, Brasil/IUCN, pp. 166–171.

    Google Scholar 

  • Bickham, J.W., Patton, J.C., Schlitter, DA, Rautenbach, I.L, Honeycutt, R.L, 2004. Molecular phylogenetics, karyotypic diversity and partition of the genus Myotis (Chiroptera: Vespertilionidae), Mol. Phylogenet. Evol. 33, 333–338.

    Article  CAS  PubMed  Google Scholar 

  • Bickham, J.W., Wood, C.C., Patton, J.C., 1995. Biogeographic implications of cytochrome-b sequences and allozymes in sockeye (Oncorhynchus nerka).J, Hered. 86, 140–144.

    Article  CAS  Google Scholar 

  • Cody, S., Richardson, J.E., Rull, V., Ellis, C, Pennington, R.T., 2010. The Great American Biotic Interchange revisited, Ecography 33, 326–332.

    Google Scholar 

  • Czernay, S., 1987. Spiesshirsche und Pudus, Die Neue Brehm Bucherei 581, 1–84. Darriba, D., Taboada, G.L, Doallo, R., Posada, D., 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772.

    Google Scholar 

  • Douzery, E., Randi, E., 1997. The mitochondrial control region of Cervidae: evolutionary patterns and phylogenetic content, Mol. Biol. Evol. 14, 1154–1166.

    Article  CAS  PubMed  Google Scholar 

  • Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7, Mol. Biol. Evol. 29, 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duarte, J.M.B., González, S., Maldonado, J.E., 2008. The surprising evolutionary history of South American deer, Mol. Phylogenet. Evol. 49, 17–22.

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg, J.F., 1998. Mammals of the Neotropics volume 1, The Northern Neotropics: Panama, Colombia, Venezuela, Guyana, Suriname, French Guiana. The University of Chicago Press Chicago.

  • Eisenberg, J.F., 2000. The contemporany cervidae of Central and South America. In: Vbra, S., Schaller, G.B. (Eds.), Antelopes, Deer, and Relatives. Fossil Record, Behavioral Ecology, Systematic, and Conservation. Yale University Press, New Haven and London, pp. 189–202.

    Google Scholar 

  • Eisenberg, J.F., Redford, K.H., 1999. Mammals of the Neotropics volume 3. In: The Central Neotropics: Ecuador, Peru, Bolivia, Brazil. The University of Chicago Press, Chicago.

    Google Scholar 

  • Emmons, L.H., Feer, F., 1997. Neotropical Rain Forest Mammals, a Field Guide, second ed. The University of Chicago Press, Chicago.

    Google Scholar 

  • Fisher-Reid, M.C., Wiens, J.J., 2011. What are the consequences of combining nuclear and mitochondrial data for phylogenetic analysis? Lessons from Pletodon salamanders and 13 other vertebrate clades. BMC Evol. Biol. 11, 300.

    Google Scholar 

  • Geist, V., 1998. Deer of the World: their Evolution, Behavior, and Ecology. Stackpole Books, Washington, D.C.

    Google Scholar 

  • Gilbert, C, Ropiquet, A., Hassanin, A., 2006. Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia) systematics, morphology, and biogeography, Mol. Phylogenet. Evol. 40, 101–117.

    Article  CAS  PubMed  Google Scholar 

  • Goldman, E.A., Moore, R.T., 1945. The biotic provinces of Mexico, J. Mammal. 26, 347–360.

    Article  CAS  PubMed  Google Scholar 

  • González, E., Labarca, R., Chavez-Hoffmeister, M., Pino, M., 2014. First fossil record of the smallest deer cf, Pudu Molina 1782 (Artiodactyla, Cervidae), in the late pleistocene of South America. J. Vertebr. Paleontol. 34, 483–488.

    Article  Google Scholar 

  • González, S., Maldonado, J.E., Leonard, J.A., Vila, C, Duarte, J.M., Merino, M., Brum-Zorrilla, N., Wayne, R.K., 1998. Conservation genetics of the endangered Pampas deer (Ozotoceros bezoarticus), Mol. Ecol. 7, 47–56.

    Article  PubMed  Google Scholar 

  • Gouy, M., Guindon, S., Gascuel, O., 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building, Mol. Biol. Evol. 27, 221–224.

    Article  CAS  PubMed  Google Scholar 

  • Groves, C.P., Grubb, P., 1987. Relationships of living deer. In: Wemmer, CM. (Ed.), Biology and Management of the Cervidae. Smithsonian Institution Press, Washington, D.C, pp. 21–59.

    Google Scholar 

  • Groves, C.P., Grubb, P., 2011. Ungulate Taxonomy. Johns Hopkins University Press, Baltimore.

    Google Scholar 

  • Grubb, P., 2005. Artiodactyla. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World. A Taxonomic and Geographic Reference., third ed. Johns Hopkins University Press, Baltimore, pp. 637–722.

    Google Scholar 

  • Gutíerrez, E.E., Maldonado, J.E., Radosavljevic, A., Molinari, J., Patterson, B.D., Martínez-C, J.M., Rutter, A.R., Hawking, M.T.R., García, F.J., Helgen, K.M., 2015. The taxonomic status of Mazama bricenii and the significance of the Tíchira depression for mammalian endemism in the Cordillera de Márida Venezuela. PLoS One 10, e0129113.

    Google Scholar 

  • Hassanin, A., Douzery, E.J.P., 2003. Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae, Syst. Biol. 52, 206–228.

    Article  PubMed  Google Scholar 

  • Hassanin, A., Delsuc, F., Ropiquet, A., Hammer, C, van Vuuren, B.J., Maththee, C, Ruiz-Garcia, M., Catzeflis, F., Areskoug, V., Nguyen, T.T., Couloux, A., 2012. Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C. R. Biol. 335, 32–50.

  • Havird, J.C., Santos, S.R., 2014. Performance of single and concatenated sets of mitochondrial genes at inferring metazoan relationships relative to full mitogenome data. PLoS One 9, e84080.

    Book  Google Scholar 

  • Hershkovitz, P., 1951. British Honduras, Mexico, Jamaica and Haiti, FieldianaZool. 31, 547–569.

    Google Scholar 

  • Hershkovitz, P., 1966. Mice, land bridges and Latin American faunal interchange. In: Wenzel, R.L., Tipton, V.J. (Eds.), Ectoparasites of Panama. Field Museum of Natural History, Chicago, pp. 725–751.

    Google Scholar 

  • Hershkovitz, P., 1969. The recent mammals of the Neotropical region: a zoogeographic and ecological review, Quarterly Rev. Biol. 44, 1–70.

    Article  Google Scholar 

  • Jorge, W., Benirschke, K., 1977. Centromeric heterochromatin and G-banding of the red brocket deer, Mazama americana temama (Cervoidea, Artiodactyla) with a probable non-Robertsonian translocation, Cytologia 42, 711–721.

    Article  CAS  PubMed  Google Scholar 

  • Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol. 30, 772–780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerr, R., 1792. The Animal Kingdom, or Zoological System, of the celebrated Sir Charles Linnæus, Class I Mammalia: containing a complete systematic description, arrangement, and nomenclature, of all the known species and varieties of the mammalia, or animals which give suck to their young. Strahan A., Cadell T., London, Creech, W., Edinburgh.

    Google Scholar 

  • Maddison, W.P., Maddison, D.R., 2015. Mesquite: a modular system for evolutionary analysis. Version 3.02 https://doi.org/mesquiteproject.org

  • Márquez, A., Maldonado,J.E., González, S., Beccaceci, M.D., Garcia, J.E., Duarte, J.M.B., 2006. Phylogeography and Pleistocene demographic history of the endangered marsh deer (Blastocerus dichotomus) from the Río de la Plata Basin, Conserv. Genet. 7, 563–575.

    Article  CAS  Google Scholar 

  • Marshall, L.G., 1988. Land mammals and the Great American interchange, Am. Sci. 76, 380–388.

    Google Scholar 

  • Medellín, R.A., Gardner, A.L., Aranda, J.M., 1998. The taxonomic status of the Yucatan brown brocket, Mazama pandora (Mammalia, Cervidae), Proc. Biol. Soc. Washington 111, 1–14.

    Google Scholar 

  • Merriam, C.H., 1901. A new brocket of Yucatan, Proc. Biol. Soc. Washington 16, 105–106.

    Google Scholar 

  • Mueller, R.L., 2006. Evolutionary rates divergence dates, and the performance of mitochondrial genes in bayesian phylogenetic analysis, Syst. Biol. 55, 289–300.

    Article  PubMed  Google Scholar 

  • Rambaut A., 2012. FigTree v1.4.2 https://doi.org/tree.bio.ed.ac.uk/software/figtree/

  • Rambaut, A., Drummond, A.J., 2013. LogCombiner v1.8.2. https://doi.org/beast.bio.ed.ac.uk/

  • Rambaut, A., Drummond, A.J., 2013. TreeAnnotator v1.8.2. https://doi.org/beast.bio.ed.ac.uk/

  • Rambaut, A., Suchard, M.A., Xie, W., Drummond, A.J., 2013. Tracer v1.6.0 https://doi.org/tree.bio.ed.ac.uk/software/tracer/

  • Randi, E., Mucci, N., Pierpaoli, M., Douzery, E., 1998. New phylogenetic perspectives on the Cervidae (Artiodactyla) are provided by the mitochondrial cytochrome b gene, Proc. R. Soc. London. B 265, 793–801.

    Article  CAS  Google Scholar 

  • Randi, E., Mucci, N., Claro-Hergueta, F., Bonnet, A., Douzery, E.J.P., 2001. A mitochondrial DNA control region phylogeny of the Cervinae: speciation in Cervus and implications for conservation, Anim. Conserv. 4, 1–11.

    Article  Google Scholar 

  • Räsänen, K., Hendry, A.P., 2008. Disentangling interactions between adaptative divergence and gene flow when ecology drives diversification, Ecol. Lett. 11, 624–636.

    Article  PubMed  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Lu, L, Suchard, M.A., Huelsenbeck, J.P., 2012. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space, Syst. Biol. 61, 39–542.

    Google Scholar 

  • Ruiz-García, M., Randi, E., Martínez-Agüero, M., Alvarez, D., 2007. Relaciones filogenéticas entre géneros de ciervos neotropicales (Artiodactyla, Cervidae) mediante secuenciación de AND mitochondrial y marcadores microsatelitales, Rev. Biol. Trop. (Int. J. Trop. Biol.) 55, 723–741.

    Google Scholar 

  • Rubinoff, D., Holland, B.S., 2005. Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetics and taxonomic inference, Syst. Biol. 54, 952–961.

    Article  PubMed  Google Scholar 

  • Sbisà, E., Tanzariello, F., Reyes, A., Pesole, G., Saccone, C, 1997. Mammalian mitochondrial D-loop region structural analysis: identification of new conserved sequences and their functional and evolutionary implications, Gene 205, 125–140.

    Article  PubMed  Google Scholar 

  • Schluter, D., 2000. The Ecology of Adaptative Radiation. Oxford University Press, Oxford.

    Google Scholar 

  • Simpson, G.G., 1950. History of the fauna of Latin America, Am. Sci. 38, 361–389. Smith, M.H., Branan, W.V., Marchinton, R.L., Johns, P.E., Wooten, M.C., 1986. Genetic and morphologic comparisons of red brocket, brown brocket, and white-tailed deer. J. Mammal. 67, 103–111.

  • Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models, Bioinformatics 22, 2688–2690.

    Article  CAS  PubMed  Google Scholar 

  • Sun, K., Feng, J., Jin, L., Liu, Y., Shi, L, Jiang, T., 2009. Structure: DNA sequence variation and phylogenetic implications of the mitochondrial control region in horseshoe bats, Mamm. Biol. 74, 130–144.

    Article  Google Scholar 

  • Vázquez-Domínguez, E., Arita, H.T., 2010. The Yucatan peninsula: biogeographical history 65 million years in the making. Ecography33, 212–219.

    Google Scholar 

  • Vislobokova, I., 1980. The systematic position of a deer from Pavlodar and the origin of neocervinae, Paleontol. J. 3, 97–111.

    Google Scholar 

  • Webb, S.D., 1991. Ecogeography and the Great American Interchange, Paleobiology 17, 266–280.

    Article  Google Scholar 

  • Webb, S.D., 2006. The Great American Biotic Interchange: patterns and processes, Ann. Mo. Bot. Gard. 93, 245–257.

    Article  Google Scholar 

  • Wisely, S.M., Maldonado,J.E., Fleisher, R.C., 2004. A technique for sampling ancient DNA that minimizes damage to museum specimens, Conserv. Genet. 5, 105–107.

    Article  CAS  Google Scholar 

  • Woodburne, M., 2010. The Great American Biotic Interchange: Dispersals, tectonics, climate, sea level and holding pens, J. Mamm. Evol. 17, 245–264.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zandorya, R., Meyer, A., 1996. Phylogenetic performance of mitochondrial protein-coding genes in resolving relationships among vertebrates, Mol. Biol. Evol. 13, 933–942.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. División de Posgrado, Instituto de Ecología, A. C., Carretera Antigua a Coatepec 351, El Haya, Xalapa, 91070, Veracruz, México

    Luis A. Escobedo-Morales

  2. Red de Biología y Conservación de Vertebrados, Instituto de Ecología, A. C., Carretera Antigua a Coatepec 351, 91070, El Haya, Xalapa, Veracruz, México

    Salvador Mandujano

  3. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, 04510, Distrito Federal, México

    Luis E. Eguiarte

  4. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, 04510, Distrito Federal, México

    Marco A. Rodríguez-Rodríguez

  5. Center for Conservation and Evolutionary Genetics, Smithsonian Conservation Biology Institute, National Zoological Park, and Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 20008, Washington, D.C., US

    Jesús E. Maldonado

Authors
  1. Luis A. Escobedo-Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Salvador Mandujano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis E. Eguiarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marco A. Rodríguez-Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jesús E. Maldonado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luis A. Escobedo-Morales.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Escobedo-Morales, L.A., Mandujano, S., Eguiarte, L.E. et al. First phylogenetic analysis of Mesoamerican brocket deer Mazama pandora and Mazama temama (Cetartiodactyla: Cervidae) based on mitochondrial sequences: Implications for Neotropical deer evolution. Mamm Biol 81, 303–313 (2016). https://doi.org/10.1016/j.mambio.2016.02.003

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2016.02.003

Keywords

Search

Navigation