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Abstract:

In light of the multiple sex chromosome systems observed in howler monkeys (Alouatta Lacépède, 1799) a combined cladistic analysis using chromosomal and molecular characters was applied to discuss the possible origin of these systems. Mesoamerican and South American howlers were karyologically compared. FISH analysis using the chromosome painting probes for the #3 and #15 human chromosomes was applied to corroborate the homeology of the sexual systems. We found that the HSA3/15 syntenic association, present in the sex chromosome systems of South American Howlers, is not present in those of Mesoamerican ones. The autosomes involved in the translocation that formed the sexual systems in the Mesoamerican and South American species are different, thus suggesting an independent origin. Parsimony analysis resolved the phylogenetic relationships among howler species, demonstrating utility of the combined approach. A hypothesis for the origin of the multiple sex chromosome systems for the genus is proposed. © Eliana Ruth Steinberg et al.

Registro:

Documento: Artículo
Título:Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta)
Autor:Steinberg, E.R.; Nieves, M.; Mudry, M.D.
Filiación:Grupo de Investigación en Biología Evolutiva (GIBE) - Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires - IEGEBA (CONICET-UBA), Ciudad Universitaria - Pab. II -4 piso - Labs 43-46, Buenos Aires, C1428EGA, Argentina
Palabras clave:Combined phylogenetic analysis; Cytochrome b; FISH; Multiple sex chromosome systems; Neotropical Primates
Año:2014
Volumen:8
Número:1
Página de inicio:43
Página de fin:69
DOI: http://dx.doi.org/10.3897/compcytogen.v8i1.6716
Título revista:Comparative Cytogenetics
Título revista abreviado:Comp. Cytogenet.
ISSN:19930771
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19930771_v8_n1_p43_Steinberg

Referencias:

  • Amaral, P., Finotelo, L., de Oliveira, E., Pissinatti, A., Nagamachi, C., Pieczarka, J., Phylogenetic studies of the genus Cebus (Cebidae-Primates) using chromosome painting and G-banding (2008) BMC Evolutionary Biology, 8, p. 169
  • Armada, J.L.A., Barroso, C.M.L., Lima, M.M.C., Muniz, J.A.P.C., Seuánez, H.N., Chromosome studies in Alouatta belzebul (1987) American Journal of Primatology, 13, pp. 283-296
  • Bick, Y.A.E., Jackson, W.D., Karyotype of the Monotremes Ornithorhynchus anatinus (Platypus) and Tachyglossus aculeatus (Echidna) (1967) Nature, 214, pp. 600-601
  • Bonvicino, C.R., Lemos, B., Seuánez, H., Molecular Phylogenetics of howler monkeys (Alouatta, Platyrrhini) a comparison with karyotypic data (2001) Chromosoma, 110 (3), pp. 241-246
  • Cabrera, A., Los nombres científicos de algunos monos american (1940) Ciencia, 9, pp. 402-405
  • Casado, F., Bonvicino, C.R., Nagle, C., Comas, B., Manzur, T.D., Lahoz, M.M., Seuánez, H.N., Mitochondrial divergence between 2 populations of the hooded capuchin, Cebus (Sapajus) cay (Platyrrhini, Primates) (2010) Journal of Heredity, 101 (3), pp. 261-269
  • Cioffi, M.B., Liehr, T., Trifonov, V., Molina, W.F., Bertollo, L.A.C., Independent Sex Chromosome Evolution in Lower Vertebrates: A Molecular Cytogenetic Overview in the Erythrinidae Fish Family (2013) Cytogenetic and Genome Research, 141 (2-3), pp. 186-194
  • Clemente, I.C., Ponsà, M., García, M., Egozcue, J., Evolution of the simiiformes and the phylogeny of human chromosomes (1990) Human Genetics, 84 (6), pp. 493-506
  • Coates, A.G., Collins, L.S., Aubry, M-P., Berggren, W.A., The Geology of the Darien, Panama, and the late Miocene-Pliocene collision of the Panama arc with northwestern South America (2004) Bulletin of Geological Society of America, 116 (11-12), pp. 1327-1344
  • Consigliere, S., Stanyon, R., Koehler, U., Agoramoorthy, G., Wienberg, J., Chromosome painting defines genomic rearrangements between red howler monkey subspecies (1996) Chromosome Research, 4 (4), pp. 264-270
  • Consigliere, S., Stanyon, R., Koehler, U., Arnold, N., Wienberg, J., In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini, Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes (1998) American Journal of Primatology, 46 (2), pp. 119-133
  • Cooke, S.B., Rosenberger, A.L., Turvey, S., An extinct monkey from Haiti and the origins of the Greater Antillean primates (2011) Proceedings of the National Academy of Sciences, 108 (7), pp. 2699-2704
  • Cortés-Ortiz, L., Bermingham, E., Rico, C., Rodríguez-Luna, E., Sampaio, I., Ruiz-García, M., Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta (2003) Molecular Phylogenetics and Evolution, 26 (1), pp. 64-81
  • Crockett, C., Eisenberg, J., Howlers: variations in group size and demography (1987) Primate societies., pp. 54-68. , Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (Eds) Chicago IL, USA
  • de Grouchy, J., Turleau, C., Roubin, M., Klein, M., Karyotypic evolution in man and chimpanzees A comparative study of band topographies after controlled denaturation. (1972) Annales de Génètique, 15 (2), pp. 79-84
  • de Oliveira, E.H.C., Lima, M.M.C., Sbalqueiro, I.J., Chromosomal variation in Alouatta fusca (1995) Neotropical Primates, 3, pp. 181-183
  • de Oliveira, E.H.C., de Lima, M.M.C., Sbalqueiro, I.J., Pissinati, A., The karyotype of Alouatta fusca clamitans from Rio de Janeiro, Brazil: Evidence for a y-autosome translocation (1998) Genetics and Molecular Biology, 21 (3), pp. 361-364
  • de Oliveira, E.H.C., Neusser, M., Figueiredo, W.B., Nagamachi, C., Pieczarka, J.C., Sbalqueiro, I.J., Wienberg, J., Müller, S., The phylogeny of howler monkeys (Alouatta, Platyrrhini): Reconstruction by multicolor cross-species chromosome painting (2002) Chromosome Research, 10 (8), pp. 669-683
  • de Oliveira, E.H.C., Neusser, M., Müller, S., Chromosome Evolution in New World Monkeys (Platyrrhini) (2012) Cytogenetics and Genome Research, 137 (2-4), pp. 259-272
  • de Oliveira, E.H.C., Neusser, M., Pieczarka, J.C., Nagamachi, C., Sbalqueiro, I.J., Müller, S., Phylogenetic inferences of Atelinae (Platyrrhini) based on multi-directional chromosome painting in Brachyteles arachnoides, Ateles paniscus paniscus and Ateles b (2005) marginatus. Cytogenetics and Genome Research, 108 (1-3), pp. 183-190
  • Deuve, J., Bennett, N., O'Brien, P., Ferguson-Smith, M., Faulkes, C., Britton-Davidian, J., Robinson, T., Complex evolution of X and Y autosomal translocations in the giant mole-rat, Cryptomys mechowi (Bathyergidae) (2006) Chromosome Research, 14 (6), pp. 681-691
  • Dobigny, G., Ducroz, J.F., Robinson, T.J., Volobouev, V., Cytogenetics and Cladistics (2004) Systematic Biology, 53 (3), pp. 470-484
  • Dutrillaux, B., Couturier, J., The ancestral karyotype of platyrrhine monkeys (1981) Cytogenetics and Cell Genetics, 30 (4), pp. 232-242
  • Egozcue, J., De Egozcue, V., The Chromosome Complement of the Howler Monkey (Alouatta caraya, HUMBOLDT 1812) (1966) Cytogenetics and Genome Research, 5 (1), pp. 20-27
  • Elliot, D.G., Description of a new species of monkeys of the Genera Galago, Alouatta and Cercopithecus (1910) Annals and Magazine of Natural History, 18 (5), pp. 77-83
  • Ellsworth, J.A., Hoelzer, G.A., Genetic Evidence on the Historical Biogeography of Central American Howler Monkeys (2006) Primate Biogeography, pp. 81-103. , Lehman SM, Fleagle JG (Eds). New York, USA
  • Felsenstein, J., Confidence limits on phylogenies: an approach using the bootstrap (1985) Evolution, 39 (4), pp. 783-791. , http://www.jstor.org/stable/10.2307/2408678
  • Fleagle, J.G., (1999) Primate adaptation and evolution, p. 486. , Academic Press, San Diego, California, USA
  • Flores, S.V., Evans, A.L., McAllister, B.F., Independent Origins of New Sex-Linked Chromosomes in the melanica and robusta Species Groups of Drosophila (2008) BMC Evolutionary Biology, 8 (1), p. 33
  • García, F., Nogués, C., Ponsà, M., Ruiz-Herrera, A., Egozcue, J., García Caldés, M., Chromosomal homologies between humans and Cebus apella (Primates) revealed by ZOO-FISH (2000) Mammalian Genome, 11 (5), pp. 399-401
  • García, F., Ruiz-Herrera, A., Egozcue, J., Ponsà, M., García, M., Chromosomal homologies between Cebus and Ateles (Primates) based on ZOO-FISH and G-banding comparisons (2002) American Journal of Primatology, 57 (4), pp. 177-188
  • Geoffroy Saint-Hilaire, E., Tableau des quadrumanes ou des animaux composant le premier ordre de la classe des mammifères (1812) Annales du Muséum national d'histoire naturelle, Paris, 7, pp. 260-273
  • Geoffroy Saint-Hilaire, E., (1829) Cours de l'histoire naturelle des Mammifères, p. 36. , Pichon et Didier, Paris, Leçon IX
  • Geoffroy Saint-Hilaire, I., de, Blainville., Raport sur les résultats scientifiques du voyage de Alcide d'Orbigny dans 1'Amérique du Sud, pendant des années 1826, 1827, 1828, 1829, 1830, 1831, 1832 et 1833. Partie Zoologique. (1834) Nouvelles annales du Muséum d'Histoire Naturelle, 3, pp. 84-115
  • Gray, J.E., Description of two species of Mammalia from Caracas (1849) Proceedings of the Zoological Society of London, 848, p. 138
  • Gregorin, R., Taxonomia e variação geográfica das espécies do gênero Alouatta Lacépède (Primates, Atelidae) no Brasil (2006) Revista Brasileira de Zoologia, 23 (1), pp. 64-144
  • Groves, C.P., Order Primates (2005) Mammal species of the world: a taxonomic and geographic reference, pp. 111-185. , Wilson DE, Reeder DM (Eds) Johns Hopkins University Press, Baltimore, Maryland, USA
  • Groves, C.P., (2001) Primate Taxonomy, p. 350. , Smithsonian Institution Press, Washington DC, USA
  • Gutiérrez Calvache, D.A., Jaimez Salgado, E.J., Introducción a los primates fósiles de las Antillas. 120 años de Paleoprimatología en el caribe insultar (2007), p. 208. , Editora Universitaria-UASD, Santo Domingo, Cuba; Harris, E.E., Gifalli-Iughetti, C., Braga, Z.H., Koiffmann, C.P., Cytochrome b Sequences Show Subdivision between Populations of the Brown Howler Monkey (Alouatta guariba) from Rio de Janeiro and Santa Catarina, Brazil (2005) Neotropical Primates, 13 (2), pp. 16-21
  • de Humboldt, A., Recueil d'observations de zoologie et d'anatomie comparée, faites dans l'océan Atlantique, dans l'intérieur du noveau continent et dans la mer du sur pendant les années 1799, 1800, 1801, 1802 et 1803 (1812), 1, p. 368. , Paris, France, VIII; Illiger, J.C.W., Prodomus systematis mammalium et avium additis terminis zoographicis utriusque classis, eorumque versione germanica. (1811), p. 301. , Berlim, Berolini, Sumptibus, C. Salfeld, XVIII; Kluge, A.G., A Concern for Evidence and a Phylogenetic Hypothesis of Relationships Among Epicrates (Boidae, Serpentes) (1989) Systematic Zoology, 38 (1), pp. 7-25
  • Knowlton, N., Weigt, L.A., New dates and new rates for divergence across the Isthmus of Panama (1998) Proceedings of the Royal Society B, 265 (1412), pp. 2257-2263
  • Koiffmann, C.P., Saldanha, P.H., Cytogenetics of Brazilian monkeys (1974) Journal of Human Evolution, 3 (4), pp. 275-282
  • Kuhl, H., (1820) Beiträge zur Zoologie und Vergleichenden Anatomie, p. 152. , Hermannschen Buchhandlung, Frankfurt
  • Lacépède, B.G.E.V., Tableau des divisions, sous-divisions, ordres et genres des Mammifères (1799), p. 18. , Plassan, Paris; Lawrence, B., Howler monkeys of the palliata group (1933) Bulletin of the Museum of Comparative Zoology, 75 (8), pp. 313-354
  • Lesson, R.P., Species de Mammifères: Bimanes et quadrimanes; suivi d`un mémoire sur les Oryctéropes (1840), p. 291. , JB Baillère, Paris, VIII; Linnaeus, C., Systema Naturae per Regna tria naturae, classes, ordines, genera, species cum bracteribus, differentiis, synonymis, locis (1758), p. 823. , Regnum Animale. Estocolmo, Holmiae; Linnaeus, C., Systema Naturae per Regna tria naturae, classes, ordines, genera, species cum bracteribus, differentiis, synonymis, locis (1766) Regnum Animale. Estocolmo, Holmiae, vol, 1, p. 823 pp
  • Lima, M.M.C., Sampaio, M.I.C., Schneider, M.P.C., Scheffrahn, W., Schneider, H., Salzano, F.M., Chromosome and protein variation in red howler monkeys (1990) Revista Brasilera de Genetica, 13 (4), pp. 789-802
  • Lima, M.M.C., Seuánez, H., Chromosome studies in the red Howler Monkey, Alouatta seniculus stramineus (Platyrrhini, Primates): description of an X1X2Y1Y2/X1X1X2X2 sex chromosome system and karyological comparisons with other subspecies (1991) Cytogenetics and Cell Genetics, 57 (2-3), pp. 151-156
  • Lönnberg, E., Notes on members of the genera Alouatta and Aotus (1941) Arkiv für Zoologi, 33A (10), pp. 1-44
  • Lorenz, J.G., Jackson, W.E., Beck, J.C., Hanner, R., The Problems and Promise of DNA Barcodes for Species Diagnosis of Primate Biomaterials (2005) Philosophical Transactions of the Royal Society B, 360 (1462), pp. 1869-1877
  • Ma, N.S.F., Elliott, M.W., Morgan, L., Miller, A., Jones, T.C., Translocation of Y chromosome to an autosome in the Bolivian owl monkey, Aotus (1976) American Journal of Physical Anthropology, 45 (2), pp. 191-201
  • Meireles, C.M., Czelusniak, J., Ferrari, S.F., Schneider, M.P.C., Goodman, M., Phylogenetic relationships among Brazilian howler monkeys, genus Alouatta (Platyrrhini, Atelidae), based on gama1-globin pseudogene sequences (1999) Genetics and Molecular Biology, 22 (3), pp. 337-344
  • Minezawa, M., Harada, M., Jordan, O.C., Borda, C.J.V., Cytogenetics of Bolivian endemic red howler monkeys (Alouatta seniculus sara): accessory chromosomes and Y-autosome translocation- related numerical variations (1985) Research Report on New World Monkeys, 5, pp. 7-16
  • de Miranda Ribeiro, A., Zwei neue Affen unserer Fauna (1912) Brasilianische Rundschau, 2 (1), pp. 21-23
  • Morescalchi, M., Schempp, W., Consigliere, S., Bigoni, F., Wienberg, J., Stanyon, R., Mapping chromosomal homology between humans and the black-handed spider monkey by fluorescence in situ hybridization (1997) Chromosome Research, 5 (8), pp. 527-536
  • Moura-Pensin, C., Pieczarka, J., Nagamachi, C., Pereira Carneiro Muniz, J.A., Do Carmo de Oliveira Brigido, M., Pissinatti, A., Marinho, A., de Souza Barros, R.M., Cytogenetic relations among the genera of the subfamily Pitheciinae (Cebidae, Primates) (2001) Caryologia, 54 (4), pp. 385-391
  • Mudry, M.D., Cytogenetic variability within and across populations of Cebus apella in Argentina (1990) Folia Primatologica, 54 (3-4), pp. 206-216
  • Mudry, M.D., Labal de Vinuesa, M.L., Colillas, O.J., Brieux de Salum, S., Banding patterns of Alouatta caraya (1984) Revista Brasilera de Genetica, 7, pp. 373-379
  • Mudry, M.D., Ponsà, M., Borrell, A., Egozcue, J., García, M., Prometaphase chromosomes of the howler monkey (Alouatta caraya): G, C, NOR, and restriction enzyme (RES) banding (1994) American Journal of Primatology, 33 (2), pp. 121-132
  • Mudry, M.D., Rahn, M.I., Gorostiaga, M., Hick, A., Merani, M.S., Solari, A.J., Revised Karyotype of Alouatta caraya (Primates: Platyrrhini) Based on Synaptonemal Complex and Banding Analyses (1998) Hereditas, 128 (1), pp. 9-16
  • Mudry, M.D., Rahn, M.I., Solari, A.J., Meiosis and chromosome painting of sex chromosome systems in Ceboidea (2001) American Journal of Primatology, 54 (2), pp. 65-78
  • Müller, S., Primate Chromosome Evolution (2006) Genomic Disorders, pp. 133-152. , Lupski JR, Stankiewicz P (Eds) Humana Press Inc, New Jersey, USA
  • Müller, S., Stanyon, R., Finelli, P., Archidiacono, N., Wienberg, J., Molecular cytogenetic dissection of human chromosomes 3 and 21 evolution (2000) Proceedings of the National Academy of Sciences, 97 (1), pp. 206-211
  • Nascimento, F.F., Bonvicino, C.R., Da Silva, F.C.D., Schneider, M.P.C., Seuánez, H., Cytochrome b polymorphisms and population structure of two species of Alouatta (Primates) (2005) Cytogenetics and Genome Research, 108 (1-3), pp. 106-111
  • Neusser, M., Stanyon, R., Bigoni, F., Wienberg, J., Müller, S., Molecular cytotaxonomy of New World monkeys (Platyrrhini)-comparative analysis of five species by multicolor chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae (2001) Cytogenetics and Cell Genetics, 94 (3-4), pp. 206-215
  • Rahn, M.I., Mudry, M.D., Merani, M.S., Solari, A.J., Meiotic behavior of the X1X2Y1Y2 quadrivalent of the Primate Alouatta caraya (1996) Chromosome Research, 4 (5), pp. 350-356
  • Rens, W., O'Brien, P.C., Grützner, F., Clarke, O., Graphodatskaya, D., Tsend-Ayush, E., Trifonov, V.A., Ferguson-Smith, M.A., The multiple sex chromosomes of platypus and echidna are not completely identical and several share homology with the avian Z (2007) Genome Biology, 8 (11), p. R243
  • Rosenberger, A.L., Tejedor, M.F., Cooke, S.B., Pekar, S., Platyrrhine Ecophylogenetics in Space and Time (2009) South American Primates, pp. 69-113. , Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB, Barrett L (Eds), Springer, New York, USA
  • Rylands, A.B., An assessment of the diversity of New World Primates (2000) Neotropical Primates, 8 (2), pp. 61-93
  • Rylands, A.B., Mittermeier, R.A., The Diversity of the NewWorld Primates (Platyrrhini): An Annotated Taxonomy (2009) South American Primates: Comparatives Perspectives in the study of behavior ecology, and conservation, pp. 23-54. , Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (Eds), Springer, New York, USA
  • Sankoff, D., Rearrangements and chromosomal evolution (2003) Current Opinion in Genetics and Development, 13 (6), pp. 583-587
  • Seuánez, H.N., (1979) The phylogeny of human chromosomes, p. 208. , Springer-Verlag, New York, USA
  • Seuánez, H.N., Forman, L., Matayoshi, T., Fanning, T.G., The Callimico goeldii (Primates, Platyrrhini) genome: Karyology and middle repetitive (LINE-1) DNA sequences (1989) Chromosoma, 98 (6), pp. 389-395
  • Smith, J.D., The systematic status of the black howler monkey, Alouatta pigra Lawrence (1970) Journal of Mammalogy, 51 (2), pp. 358-369. , http://www.jstor.org/stable/1378486
  • Solari, A.J., Rahn, M.I., Fine structure and meiotic behaviour of the male multiple sex chromosomes in the genus Alouatta (2005) Cytogenetics and Genome Research, 108 (1-3), pp. 262-267
  • von Spix, J.B., Simiarum et vespertilionum Brasiliensium species novae ou Histoire Naturelle des Esèces Nouvelles de Singes et de Chauves-souris observées et recueillies pendant le voyage dans l`intérieur du Brésil (1823), p. 72. , Munique, Typis Francisci Seraphici Hubschmanni, VIII; Stanyon, R., Consigliere, S., Bigoni, F., Ferguson-Smith, M., O'Brien, P.C.M., Wienberg, J., Reciprocal chromosome painting between a New World primate, the woolly monkey, and humans (2001) Chromosome Research, 9 (2), pp. 97-106
  • Stanyon, R., Garofalo, F., Steinberg, E.R., Capozzi, O., Di Marco, S., Nieves, M., Archidiacono, N., Mudry, M.D., Chromosome Painting in Two Genera of South American Monkeys: Species Identification, Conservation, and Management (2011) Cytogenetics and Genome Research, 134 (1), pp. 40-50
  • Stanyon, R., Rocchi, M., Capozzi, O., Roberto, R., Misceo, D., Ventura, M., Cardone, M.F., Archidiacono, N., Primate chromosome evolution: ancestral karyotypes, marker order and neocentromeres (2008) Chromosome Research, 16 (1), pp. 17-39
  • Stanyon, R., Tofanelli, S., Morescalchi, M.A., Agoramoorthy, G., Ryder, O.A., Wienberg, J., Cytogenetic analysis shows extensive genomic rearrangements between red howler (Alouatta seniculus, Linnaeus) subspecies (1995) American Journal of Primatology, 35 (3), pp. 171-183
  • Steinberg, E.R., Cortés-Ortiz, L., Nieves, M., Bolzán, A.D., García-Orduña, F., Hermida-Lagunes, J., Canales-Espinosa, D., Mudry, M.D., The karyotype of Alouatta pigra (Primates: Platyrrhini): mitotic and meiotic analyses (2008) Cytogenetics and Genome Research, 122 (2), pp. 103-109
  • Steinberg, E.R., Nieves, M., Mudry, M.D., Meiotic characterization and sex determination system of neotropical primates: Bolivian squirrel monkey Saimiri boliviensis (Primates: Cebidae) (2007) American Journal of Primatology, 69 (11), pp. 1236-1241
  • Swofford, D., PAUP*. Phylogenetic analysis using parsimony (* and other methods) (2002), http://paup.csit.fsu.edu/, Sinauer Associates, Sunderland, Massachusetts; Szapkievich, V., Mudry, M.D., Polimorfismos Genéticos en el mono aullador negro de la Argentina (Alouatta caraya) (2003) Historia Natural, 2 (7), pp. 37-51
  • Thomas, O., On small mammals from the lower Amazon (1912) Annals and Magazine of Natural History, 9 (8), pp. 84-90
  • Thompson, J.D., Higgins, D.G., Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice (1994) Nucleid Acids Research, 22 (22), pp. 4673-4680
  • Torres, O.M., Leibovici, M., Caracterización del cariotipo del mono aullador colorado Alouatta seniculus que habita en Colombia. (2001) Caldasia, 23 (2), pp. 537-548. , http://www.revistas.unal.edu.co/index.php/cal/article/view/17722
  • Torres, O.M., Ramírez, C., Estudios Citogenético de Alouatta palliata (Cebidae). (2003) Caldasia, 25 (1), pp. 193-198. , http://www.unal.edu.co/icn/publicaciones/caldasia/25(1)/zoologia3.pdf
  • Villalobos, F., Valerio, A.A., Retana, A.P., A phylogeny of howler monkeys (Cebidae: Alouatta) based on mitochondrial, chromosomal and morphological data. (2004) Revista de Biología Tropical, 52 (3), pp. 665-677. , http://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0034-77442004000300028&lng=es&nrm=iso
  • Whittaker, D.J., Morales, J.C., Melnick, D.J., Resolution of the Hylobates phylogeny: Congruence of mitochondrial D-loop sequences with molecular, behavioral, and morphological data sets (2007) Molecular Phylogenetics and Evolution, 45 (2), pp. 620-628
  • Yunis, E.J., De Caballero, O.M.T., Ramírez, C., Efraín Ramírez, E., Chromosomal Variations in the Primate Alouatta seniculus seniculus (1976) Folia Primatologica, 25 (2-3), pp. 215-224
  • Zunino, G.E., González, V., Kowalewski, M.M., Bravo, S.P., Alouatta caraya, Relations among habitat, density and social organizations. (2001) Primate Report, 61, pp. 37-46

Citas:

---------- APA ----------
Steinberg, E.R., Nieves, M. & Mudry, M.D. (2014) . Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta). Comparative Cytogenetics, 8(1), 43-69.
http://dx.doi.org/10.3897/compcytogen.v8i1.6716
---------- CHICAGO ----------
Steinberg, E.R., Nieves, M., Mudry, M.D. "Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta)" . Comparative Cytogenetics 8, no. 1 (2014) : 43-69.
http://dx.doi.org/10.3897/compcytogen.v8i1.6716
---------- MLA ----------
Steinberg, E.R., Nieves, M., Mudry, M.D. "Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta)" . Comparative Cytogenetics, vol. 8, no. 1, 2014, pp. 43-69.
http://dx.doi.org/10.3897/compcytogen.v8i1.6716
---------- VANCOUVER ----------
Steinberg, E.R., Nieves, M., Mudry, M.D. Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta). Comp. Cytogenet. 2014;8(1):43-69.
http://dx.doi.org/10.3897/compcytogen.v8i1.6716