Skip to main content

Hybridization in Howler Monkeys: Current Understanding and Future Directions

  • Chapter
  • First Online:
Howler Monkeys

Abstract

Hybridization, or the process by which individuals from genetically distinct populations (e.g., species, subspecies) mate and produce at least some offspring, is of great relevance to understanding the basis of reproductive isolation and, in some cases, the origins of biodiversity. Natural hybridization among primates has been well documented for a few taxa, but just recently the genetic confirmation of hybridization for a number of taxa has produced new awareness of the prevalence of this phenomenon within the order and its importance in primate evolution. The study of hybridization of Alouatta pigra and A. palliata in Mexico was among the first to genetically confirm the current occurrence of hybridization in primates. Following this study, other reports of hybridization have shown that this phenomenon is more widespread among primates than previously anticipated. Within the genus Alouatta, there have been reports on the presence of hybridization between A. caraya and A. guariba in a number of contact zones in Brazil and Argentina, and various studies are currently ongoing in some of these sites to understand the extent and patterns of hybridization between these species. In this chapter, we evaluate the extent of hybridization in the genus Alouatta, revise the current knowledge of the genetic and morphological aspects of these hybrid systems, and identify future directions in the study of hybridization within this genus, to understand the possible implications of the hybridization process in the evolutionary history of howler monkeys.

Resumen

Hibridación, o el proceso mediante el cual individuos de poblaciones genéticamente distintas (especies o subespecies) se aparean y producen descendencia, tiene gran relevancia en la comprensión de las bases para el aislamiento reproductivo entre distintos taxa y, en algunos casos, para entender el origen de la biodiversidad. La hibridación natural entre primates ha sido bien conocida para unas cuantas especies, pero sólo recientemente la confirmación genética de hibridación entre numerosos taxa de primates ha sido posible y ha conducido a una nueva percepción de la prevalencia de este fenómeno entre los primates y su importancia en la evolución de este grupo. El estudio de la hibridación entre Alouatta pigra and A. palliata en México fue uno de los primeros que confirmó con evidencia genética la ocurrencia de hibridación en primates. Después de este estudio, otros reportes de hibridación en distintos taxa de primates han puesto de manifiesto que este fenómeno es más común en el orden Primates de lo que inicialmente se pensaba. Dentro del género Alouatta, también han habido reportes de hibridación entre A. caraya y A. guariba en distintas zonas de contacto en Brasil y Argentina, y varios estudios actualmente están en curso en algunas de estas áreas para entender la magnitud de este fenómeno y los patrones de hibridación entre estas especies. En este capítulo evaluamos la presencia de hibridación en el género Alouatta, revisamos lo que se conoce sobre los aspectos genéticos y morfológicos en estos sistemas híbridos y planteamos direcciones futuras en el estudio de la hibridación en este género, para entender las implicaciones del proceso de hibridación en la historia evolutiva de los monos aulladores.

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

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Ackermann RR (2010) Phenotypic traits of primate hybrids: recognizing admixture in the fossil record. Evol Anthropol 19:258–270

    Article  Google Scholar 

  • Ackermann RR, Bishop JM (2010) Morphological and molecular evidence reveals recent hybridization between gorilla taxa. Evolution 64:271–290

    Article  PubMed  Google Scholar 

  • Ackermann RR, Rogers J, Cheverud JM (2006) Identifying the morphological signatures of hybridization in primate and human evolution. J Hum Evol 51:632–645

    Article  PubMed  Google Scholar 

  • Agostini I, Holzmann I, Di Bitetti MS (2008) Infant hybrids in a newly formed mixed-species group of howler monkeys (Alouatta guariba clamitans and Alouatta caraya) in northeastern Argentina. Primates 49:304–307

    Article  PubMed  Google Scholar 

  • Agostini I, Holzmann I, Di Bitetti MS (2010) Are howler monkeys ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya. Am J Primatol 72:173–186

    Article  PubMed  Google Scholar 

  • Aguiar LM (2010) Sistema social de grupos mistos de espécies de bugios (Alouatta caraya e A. clamitans) e potenciais híbridos no Alto Rio Paraná, sul do Brasil. Ph.D. thesis. Universidade Federal do Paraná, Curitiba

    Google Scholar 

  • Aguiar LM, Mellek DM, Abreu KC, Boscarato TG, Bernardi IP, Miranda JMD, Passos FC (2007) Sympatry of Alouatta caraya and Alouatta clamitans and the rediscovery of free-ranging potential hybrids in Southern Brazil. Primates 48:245–248

    Article  PubMed  Google Scholar 

  • Aguiar LM, Pie MR, Passos FC (2008) Wild mixed groups of howler species (Alouatta caraya and Alouatta clamitans) and new evidence for their hybridization. Primates 49:149–152

    Article  PubMed  Google Scholar 

  • Aguiar LM, Tonetto J, Bicca-Marques JC (2014) Novas zonas de contato entre Alouatta caraya e A. guariba clamitans no sul do Brasil. In: Miranda JMD, Passos FC (eds) A primatologia no Brasil, vol. 13. Sociedade Brasileira de Primatologia, Curitiba

    Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Arnold ML (2009) Reticulate evolution and humans origins and ecology. Oxford University Press, Oxford

    Google Scholar 

  • Arnold M, Meyer A (2006) Natural hybridization in primates: one evolutionary mechanism. Zoology 109:261–276

    Article  PubMed  Google Scholar 

  • Barton NH (2001) The role of hybridisation in evolution. Mol Ecol 10:551–568

    Article  CAS  PubMed  Google Scholar 

  • Barton NH, Hewitt GM (1989) Adaptation, speciation and hybrid zones. Nature 341:497–503

    Article  CAS  PubMed  Google Scholar 

  • Bergman TJ, Beehner JC (2004) The social system of a hybrid baboon group (Papio hamadryas anubis × P. h. hamadryas). Int J Primatol 25:1313–1330

    Article  Google Scholar 

  • Bergman TJ, Phillips-Conroy JE, Jolly CJ (2008) Behavioral variation and reproductive success of male baboons (Papio anubis × Papio hamadryas) in a hybrid social group. Am J Primatol 70:136–147

    Article  PubMed  Google Scholar 

  • Bernstein IS (1966) Naturally occurring primates hybrid. Science 154:1559–1560

    Article  CAS  PubMed  Google Scholar 

  • Bicca-Marques JC, Calegaro-Marques C (1995) Locomotion of black howlers in a habitat with discontinuous canopy. Folia Primatol 64:55–61

    Article  CAS  PubMed  Google Scholar 

  • Bicca-Marques JC, Prates HM, Aguiar FRC, Jones CB (2008) Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization. Primates 49:246–252

    Article  PubMed  Google Scholar 

  • Bradley BJ, Lawler RR (2011) Linking genotypes, phenotypes and fitness in wild primate populations. Evol Anthropol 20:104–119

    Article  PubMed  Google Scholar 

  • Brockett RC, Horwich RH, Jones CB (2000) Female dispersal in the Belizean black howling monkey Alouatta pigra. Neotrop Primates 8:32–34

    Google Scholar 

  • Büntge ABS, Pyritz LW (2007) Sympatric occurrence of Alouatta caraya and Alouatta sara at the Río Yacuma in the Beni Department, Northern Bolivia. Neotrop Primates 14:82–83

    Article  Google Scholar 

  • Bynum EL (2002) Morphological variation within a macaque hybrid zone. Am J Phys Anthropol 118:45–49

    Article  PubMed  Google Scholar 

  • Cheverud J, Jacobs S, Moore A (1993) Genetic differences among subspecies of the saddle-back tamarin (Saguinus fuscicollis): evidence from hybrids. Am J Primatol 31:23–39

    Article  Google Scholar 

  • Chiarelli B (1973) Check-list of catarrhina primate hybrids. J Hum Evol 2:301–305

    Article  Google Scholar 

  • Coimbra-Filho AF, Silva RR, Pissinatti A (1984) Heterose em fêmea híbrida de Callithrix (Callitrichidae—Primates). In: Mello MT (ed) A primatologia no Brasil 1. Sociedade Brasileira de Primatologia, Belo Horizonte

    Google Scholar 

  • Cortés-Ortiz L (2003) Evolution of howler monkeys, Genus Alouatta. Ph.D. dissertation. University of East Anglia, Norwich, Norfolk

    Google Scholar 

  • Cortés-Ortiz L, Bermingham E, Rico C, Rodríguez-Luna E, Sampaio I, Ruiz-García M (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Phylogenet Evol 26:64–81

    Article  PubMed  Google Scholar 

  • Cortés-Ortiz L, Duda TJ Jr, Canales- Espinosa D, García-Orduna F, Rodríguez-Luna E, Bermingham E (2007) Hybridization in large-bodied New World primates. Genetics 176:2421–2425

    Article  PubMed Central  PubMed  Google Scholar 

  • Cortés-Ortiz L, Rylands AB, Mittermeier R (2014) The taxonomy of howler monkeys: integrating old and new knowledge from morphological and genetic studies. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: adaptive radiation, systematics, and morphology. Springer, New York

    Google Scholar 

  • Cruz Lima E (1945) Mammals of Amazônia. I. General Introduction and Primates. Contrib. Mus. Paraense Emílio Goeldi Hist. Nat., Ethnogr., Belém do Pará, Rio de Janeiro

    Google Scholar 

  • Cruzan MB, Arnold ML (1993) Ecological and genetic associations in an Iris hybrid zone. Evolution 47:1432–1445

    Article  Google Scholar 

  • da Cunha RGT, Oliveira DAG, Holzmann I, Kitchen DM (2015) Production of loud and quiet calls in howler monkeys. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: adaptive radiation, systematics, and morphology. Springer, New York

    Google Scholar 

  • da Silva BTF, Sampaio MIC, Schneider H, Schneider MPC, Montoya E, Encarnacion F, Salzano FM (1992) Natural hybridization between Saimiri taxa in the Peruvian Amazonia. Primates 33:107–113

    Article  Google Scholar 

  • Jesus AS, Schunemann HE, Müller J, da Silva MA, Bicca-Marques JC (2010) Hybridization between Alouatta caraya and Alouatta guariba clamitans in captivity. Primates 51:227–230

    Article  Google Scholar 

  • de Oliveira EHC, Neusser M, Figueiredo WB, Nagamachi CY, Pieczarka JC, Sbalqueiro IJ, Wienberg J, Müller S (2002) The phylogeny of the howler monkeys, (Alouatta, Platyrrhini): reconstruction by multicolor or cross species chromosome painting. Chromosome Res 10:669–683

    Article  PubMed  Google Scholar 

  • Defler TR (1994) La conservación de primates en Colombia. Trianea (Act Cien INDERENA) 5:255–287

    Google Scholar 

  • Detwiler KM (2002) Hybridization between red-tailed monkeys (Cercopithecus ascanius) and blue monkeys (C. mitis) in East African forests. In: Glenn ME, Cords M (eds) The guenons: diversity and adaptation in African monkeys. Plenum, New York

    Google Scholar 

  • Detwiler KM, Burrell AS, Jolly CJ (2005) Conservation implications of hybridization in African cercopithecine monkeys. Int J Primatol 26:661–684

    Article  Google Scholar 

  • Di Bitetti MS (2005) Perspectivas para a conservacao de primatas em Misiones. In: Galindo-Leal C, Camara IG (eds) Mata Atlantica: biodiversidade, ameacas e perspectivas. Fundacao SOS Mata Atlantica, Sao Paulo, Conservacao Internacional, Belo Horizonte

    Google Scholar 

  • Di Fiore A, Link A, Campbell CJ (2010) The Atelines: behavior and socioecological diversity in a New World monkey radiation. In: Campbell CJ, Fuentes AF, MacKinnon KC, Stumpf R, Bearder S (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Dias PAD, Alvarado-Serrano D, Rangel-Negrín A, Canales-Espinosa D, Cortés-Ortiz L (2013) Landscape attributes affecting the natural hybridization of Mexican howler monkeys. In: Marsh L, Chapman C (eds) Primates in Fragments II. Springer, New York.

    Google Scholar 

  • Dowling TE, Secor CL (1997) The role of hybridization in the evolutionary diversification of animals. Annu Rev Ecol Syst 28:593–619

    Article  Google Scholar 

  • Dunbar RIM, Dunbar P (1974) On hybridization between Theropithecus gelada and Papio anubis in the wild. J Hum Evol 3:187–192

    Article  Google Scholar 

  • Ellsworth JA (2000) Molecular evolution, social structure and phylogeography of the mantled howler monkey (Alouatta palliata). Ph.D. dissertation, University of Nevada. Reno, Nevada

    Google Scholar 

  • Field DL, Ayre DJ, Whelan RJ, Young AG (2011) The importance of pre-mating barriers and the local demographic context for contemporary mating patterns in hybrid zones of Eucalyptus aggregata and Eucalyptus rubida. Mol Ecol 20:2367–2379

    Article  PubMed  Google Scholar 

  • Ford SM (2006) The biogeographic history of Mesoamerican primates. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior and conservation. Developments in primatology: progress and prospects. Tuttle RA (series ed). Kluwer/Springer, New York

    Google Scholar 

  • Gaubert P, Taylor PJ, Fernandes CA, Bruford MW, Veron G (2005) Patterns of cryptic hybridization revealed using an integrative approach: a case study on genets (Carnivora, Viverridae, Genetta spp.) from the southern African subregion. Biol J Linn Soc 86:11–33

    Article  Google Scholar 

  • Glander KE (1992) Dispersal patterns in Costa Rican mantled howling monkeys. Int J Primatol 13:415–436

    Article  Google Scholar 

  • Gompert Z, Parchman TL, Buerkle CA (2012) Genomics of isolation in hybrids. Phil Trans R Soc B 367:439–450

    Article  PubMed Central  PubMed  Google Scholar 

  • Grant PR, Grant BR (2010) Conspecific versus heterospecific gene exchange between populations of Darwin’s finches. Philos Trans R Soc B Biol Sci 365:1065–1076

    Article  Google Scholar 

  • Grant PR, Grant BR, Markert JA, Keller LF, Petren K (2004) Convergent evolution of Darwin’s finches caused by introgressive hybridization and selection. Evolution 58:1588–1599

    Article  PubMed  Google Scholar 

  • Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MHY, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prufer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Hober B, Hoffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Z, Gusic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, De La Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Pääbo S (2010) A draft sequence of the Neandertal genome. Science 328:710–722

    Article  CAS  PubMed  Google Scholar 

  • Gregorin R (2006) Taxonomia e variacao geografica das especies do genero Alouatta Lacepede (Primates, Atelidae) no Brasil. Rev Bras Zool 23:64–144

    Article  Google Scholar 

  • Groves CP (2001) The taxonomy of primates. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101–109

    Article  Google Scholar 

  • Hernández-Camacho J, Cooper R (1976) The nonhuman primates of Colombia. In: Thorington R Jr, Heltne P (eds) Neotropical primates. National Academy of Sciences, Washington, DC

    Google Scholar 

  • Hewitt G (1988) Hybrid zones—natural laboratories for evolution studies. Trends Ecol Evol 3:158–166

    Article  CAS  PubMed  Google Scholar 

  • Hill WCO (1962) Primates comparative anatomy and taxonomy IV—Cebidae, Part B. Edinburgh University Pubs Science & Maths, Edinburgh

    Google Scholar 

  • Ho L, Cortés-Ortiz L, Dias PA, Canales-Espinosa D, Kitchen DM, Bergman TJ (2014) Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigra and A. palliata) and their hybrids. Am J Primatol 76:855–867

    Google Scholar 

  • Holzmann I (2012) Distribución geográfica potencial y comportamiento vocal de dos especies de mono aullador (Alouatta guariba clamitans y Alouatta caraya). Ph.D. dissertation. Universidad Nacional de La Plata, Argentina

    Google Scholar 

  • Holzmann I, Agostini I, Di Bitetti M (2012) Roaring behavior of two syntopic howler species (Alouatta caraya and A. guariba clamitans): evidence supports the mate defense hypothesis. Int J Primatol 33:338–355

    Article  Google Scholar 

  • Horwich RH, Johnson EW (1986) Geographic distribution of the black howler monkey (Alouatta pigra) in Central America. Primates 27:53–62

    Article  Google Scholar 

  • Isabelle A (1983) Viagem ao Rio Grande do Sul, 1833-1834. Tradução e notas de Dante de Laytano. Martins Livreiro, Porto Alegre

    Google Scholar 

  • Iwanaga S, Ferrari SF (2002) Geographic distribution of red howlers (Alouatta seniculus) in Southwestern Brazilian Amazonia, with notes on Alouatta caraya. Int J Primatol 23:1245–1256

    Article  Google Scholar 

  • Jasinska AK, Wachowiak W, Muchewicz E, Boratyn´ Ska K, Montserrat JM, Boratyn´ Ski A (2010) Cryptic hybrids between Pinus uncinata and P. sylvestris. Bot J Linn Soc 163:473–485

    Article  Google Scholar 

  • Jolly CJ (2001) A proper study for mankind: analogies from the Papionin monkeys and their implications for human evolution. Yearb Phys Anthropol 44:177–204

    Article  Google Scholar 

  • Jolly CJ, Woolley-Barker T, Beyene S, Disotell TR, Phillips-Conroy JE (1997) Intergeneric hybrid baboons. Int J Primatol 18:597–627

    Article  Google Scholar 

  • Jones CB, Cortés-Ortiz L (1998) Facultative polyandry in the howling monkey (Alouatta palliata): Carpenter was correct. Bol Primatol Lat 7:1–7

    Google Scholar 

  • Kelaita M, Cortés-Ortiz L (2013) Morphology of genetically-confirmed Alouatta pigra × A. palliata hybrids from a natural hybrid zone in Tabasco, Mexico. Am J Phys Anthropol 150:223–234

    Article  PubMed  Google Scholar 

  • Kelaita MA, Dias PAD, Aguilar-Cucurachi MS, Canales-Espinosa D, Cortés-Ortiz L (2011) Impact of intrasexual selection on sexual dimorphism and testes size in the Mexican howler monkeys Alouatta palliata and A. pigra. Am J Phys Anthropol 146:179–187

    Article  PubMed  Google Scholar 

  • Kinzey WG (1982) Distribution of primates and forest refuges. In: Prance GT (ed) Biological diversification in the tropics. Columbia University Press, New York

    Google Scholar 

  • Kitchen DM, da Cunha RGT, Holzmann I, Oliveira DAG (2015) Function of loud calls in howler monkeys. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: adaptive radiation, systematics, and morphology. Springer, New York

    Google Scholar 

  • Kohn L, Langton L, Cheverud J (2001) Subspecific genetic differences in the saddle-back tamarin (Saguinus fuscicollis): postcranial skeleton. Am J Primatol 54:41–56

    Article  CAS  PubMed  Google Scholar 

  • Lorini ML, Persson VG (1990) A contribuicao de Andre Mayer a historia natural no Parana (Brasil) II. Mamıferos do terceiro planalto paranaense. Arq Bras Biol Tecnol 33:117–132

    Google Scholar 

  • Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237

    Article  PubMed  Google Scholar 

  • Mandujano S, Estrada A (2005) Detección de umbrales de área y distancia de aislamiento para la ocupación de fragmentos de selva por monos aulladores, Alouatta palliata, en Los Tuxtlas, Mexico. Universidad y Ciencia Número Especial II 11–21

    Google Scholar 

  • Merker S, Driller C, Perwitasari-Farajallah D, Pamungkas J, Zischler H (2009) Elucidating geological and biological processes underlying the diversification of Sulawesi tarsiers. Proc Natl Acad Sci U S A 106:8459–8464

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Milton K, Lozier JD, Lacey EA (2009) Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama. Conserv Genet 10:347–358

    Article  Google Scholar 

  • Mudry MD, Nieves M, Steinberg ER (2015) Cytogenetics of howler monkeys. In: Kowalewski M, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: adaptive radiation, systematics, and morphology. Springer, New York

    Google Scholar 

  • Nagel U (1973) A comparison of anubis baboons, hamadryas baboons and their hybrids at a species border in Ethiopia. Folia Primatol 19:104–165

    Article  CAS  PubMed  Google Scholar 

  • Napier PH (1976) Catalogue of primates in the British Museum (Natural History), part 1: families Callitrichidae and Cebidae. British Museum (Natural History), London

    Google Scholar 

  • Neaves LE, Zenger KR, Cooper DW, Eldridge MDB (2010) Molecular detection of hybridization between sympatric kangaroo species in south-eastern Australia. Heredity 104:502–512

    Article  CAS  PubMed  Google Scholar 

  • Peres CA, Patton JL, Da Silva MNF (1996) Riverine barriers and gene flow in Amazonian saddle-back tamarin monkeys. Folia Primatol 67:113–124

    CAS  PubMed  Google Scholar 

  • Pinto LP, Setz EZF (2000) Sympatry and new locality for Alouatta belzebul discolor and Alouatta seniculus in the Southern Amazon. Neotrop Primates 8:150–151

    Google Scholar 

  • Pozo-Montuy G, Serio-Silva JC (2007) Movement and resource use by a group of Alouatta pigra in a forest fragment in Balancán, México. Primates 48:102–107

    Article  PubMed  Google Scholar 

  • Rheindt FE, Edwards SV (2011) Genetic introgression: an integral but neglected component of speciation in birds. Auk 128:620–632

    Article  Google Scholar 

  • Rohwer S, Bermingham E, Wood C (2001) Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution 55:405–422

    Article  CAS  PubMed  Google Scholar 

  • Samuels A, Altmann J (1986) Immigration of a Papio anubis male into a group of cynocephalus baboons and evidence for anubis-cynocephalus hybrid zone in Amboseli, Kenya. Int J Primatol 7:131–138

    Article  Google Scholar 

  • Schillaci MA, Froehlich JW, Supriatna J, Jones-Engel L (2005) The effects of hybridization on growth allometry and craniofacial form in Sulawesi macaques. J Hum Evol 49:335–369

    Article  PubMed  Google Scholar 

  • Silva FE (2010) Extensão da zona de contato e potencial hibridação entre Alouatta caraya e Alouatta guariba clamitans na região de São Francisco de Assis, RS. M.Sc. dissertation. Porto Alegre, Brazil

    Google Scholar 

  • Smith JD (1970) The systematic status of the black howler monkey, Alouatta pigra Lawrence. J Mammal 51:358–369

    Article  Google Scholar 

  • Steinberg ER, Cortés-Ortiz L, Nieves M, Bolzán AD, García- Orduña F, Hermida-Lagunes J, Canales-Espinosa D, Mudry MD (2008) The karyotype of Alouatta pigra (primates: platyrrhini): mitotic and meiotic analyses. Cytogenet Genome Res 122:103–109

    Article  CAS  PubMed  Google Scholar 

  • Strier KB (2010) Long-term field studies: positive impacts and unintended consequences. Am J Primatol 72:772–778

    Article  PubMed  Google Scholar 

  • Struhsaker TT (1970) Phylogenetic implications of some vocalizations of Cercopithecus monkeys. In: Napier JR, Napier PH (eds) Old World monkeys: evolution, systematics, and behavior. Academic, London

    Google Scholar 

  • Sun GZ, Huang B, Guan ZH, Geissmann T, Jiang XL (2011) Individuality in male songs of wild black crested gibbons (Nomascus concolor). Am J Primatol 73:431–438

    Article  PubMed  Google Scholar 

  • Tenaza R (1984) Songs of hybrid gibbons (Hylobates lar × H. muelleri). Am J Primatol 8:249–253

    Article  Google Scholar 

  • Tung J, Charpentier M, Garfield D, Altmann J, Alberts S (2008) Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population. Mol Ecol 17:1998–2011

    Article  CAS  PubMed  Google Scholar 

  • Van Belle S, Bicca-Marques JC (2015) Insights into reproductive strategies and sexual selection in howler monkeys. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation. Springer, New York

    Google Scholar 

  • Van Belle S, Estrada A, Strier KB (2008) Social relationships among male Alouatta pigra. Int J Primatol 29:1481–1498

    Article  Google Scholar 

  • Van Belle S, Estrada A, Strier KB (2011) Insights into social relationships among female black howler monkeys Alouatta pigra at Palenque National Park, Mexico. Current Zool 57:1–7

    Google Scholar 

  • Wallace RB, Painter RLE, Rumiz DI, Taber AB (2000) Primate diversity, distribution and relative abundances in the Rios Blanco y Negro Wildlife Reserve, Santa Cruz Department, Bolivia. Neotrop Primates 8:24–28

    Google Scholar 

  • Whitehead JM (1995) Vox Alouattinae—a preliminary survey of the acoustic characteristics of long distance calls of howling monkeys. Int J Primatol 16:121–144

    Article  Google Scholar 

  • Wirtz P (1999) Mother species—father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12

    Article  PubMed  Google Scholar 

  • Wyner YM, Johnson SE, Stumpf RM, DeSalle R (2002) Genetic assessment of a white-collared x red-fronted lemur hybrid zone at Andringitra. Madagascar. Am J Primatol 67:51–66

    Article  Google Scholar 

  • Zinner D, Groeneveld L, Keller C, Roos C (2009) Mitochondrial phylogeography of baboons (Papio spp.): indication for introgressive hybridization? BMC Evol Biol 9:83

    Article  PubMed Central  PubMed  Google Scholar 

  • Zinner D, Arnold ML, Roos C (2011) The strange blood: natural hybridization in primates. Evol Anthropol 20:96–103

    Article  PubMed  Google Scholar 

  • Zunino G, Kowaleski M, Oklander L, Gonzalez V (2007) Habitat fragmentation and population trends of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in northern Argentina. Am J Primatol 69:966–975

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work has been supported by NSF grant # BCS-0962807 to LCO. Genetic, behavioral, and morphologic work presented in this study for the Mexican hybrid zone was supported by the University of Michigan (OVPR #U014374), Universidad Veracruzana, PROMEP UVER 98-11-019 and 103.5/03/1154EXB-9, and NSF grants DEB-0640519 and BCS-0962807 to LCO. Research in Argentina was supported by a Conservation Grant of the International Primatological Society to IA and from Idea Wild. Behavioral and morphological studies in Paraná Brazil by LMA were supported by CNPq and Universidade Federal do Paraná (UFPR). Research in the State of Rio Grande do Sul, Brazil, was supported by a CAPES fellowship to FES and by CNPq research grants (#306090/2006-6 and 303154/2009-8) to JCBM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Liliana Cortés-Ortiz .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Cortés-Ortiz, L., Agostini, I., Aguiar, L.M., Kelaita, M., Silva, F.E., Bicca-Marques, J.C. (2015). Hybridization in Howler Monkeys: Current Understanding and Future Directions. In: Kowalewski, M., Garber, P., Cortés-Ortiz, L., Urbani, B., Youlatos, D. (eds) Howler Monkeys. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1957-4_5

Download citation

Publish with us

Policies and ethics