Skip to main content
Log in

Weak premating isolation between two parapatric brocket deer species

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

Abstract

Brocket deer Mazama nemorivaga and M. gouazoubira occur at the Amazon basin and southern areas, respectively, in parapatric distribution ranges. Both species can interbreed in captivity, although hybrids have serious fertility problems. Therefore, we expect natural selection to favour behavioural barriers against interspecific mating. We carried out no-choice tests with individuals of both species in captivity, along with white-tailed deer (Odocoileous virginianus) as outgroup. Behaviours were video recorded and analysed by using Generalized Mixed models, with interacting females and males as random subjects. Trials never led to copulation when the white-tailed-deer male was involved. Copulations within brocket deer species were more likely to occur when the individuals belonged to the same species (82.4%) but they also occurred quite frequently in interspecific interactions (35.7%). We identified some courtship behaviours, in males and females, which associated with a higher copulation probability or showed differences in frequency when performed to partners of the same or different species. In conclusion, our results reveal that the occurrence of facilitating behaviours and copulations were more common in intraspecific interactions, evidencing discrimination between species, but also that the precopulatory barrier was not strong between both brocket deer species.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Andersson, M.A., 1994. Sexual Selection. Princeton University Press, Princeton, NJ, USA.

    Book  Google Scholar 

  • Barry, K.L., Kokko, H., 2010. Male mate choice: why sequential choice makes its evolution difficult. Anim. Behav. 80, 163–169.

    Article  Google Scholar 

  • Barton, N.H., Hewitt, G.M., 1985. Análisis of hybrid zones. Annu. Rev. Ecol. Syst. 16, 113–148.

    Article  Google Scholar 

  • Barton, N.H., 2001. The role of hybridization in evolution. Mol. Ecol. 10, 551–568.

    Article  CAS  PubMed  Google Scholar 

  • Biedrzycka, A., Solarz, W., Okarma, H., 2012. Hybridization between native and introduced species of deer in Eastern Europe. J. Mamm. 93, 1331–1341.

    Article  Google Scholar 

  • Birkhead, T.R., Brillard, J.P., 2007. Reproductive isolation in birds: postcopulatory prezygotic barriers. Trends Ecol. Evol. 22, 266–272.

    Article  PubMed  Google Scholar 

  • Black-Decima, P., Vieira Rossi, R., Vogliotti, A., Cartes, J.L., Maffei, L., Duarte, J.M.B., González, S., Juliá, J.P., 2010. Amazonian brown brocket deer Mazama nemorivaga (Cuvier 1817). In: Duarte, J.M.B., Gonzalez, S. (Eds.), Neotropical Cervidology: Biology and Medicine of Latin American Deer. FUNEP-IUCN, pp. 190–201.

    Google Scholar 

  • Black-Decima, P., 2000. Home range, social structure, and scent marking behavious in brown brocket deer (Mazama gouazoubira) in a large enclosure. Mastozoologia Neotrop. 7 (1), 5–14.

    Google Scholar 

  • Bradbury, J.V., Vehrencamp, S.L., 1998. Principles of Animal Communication. Sinauer, Sunderland.

    Google Scholar 

  • Brennan, P.A., 2010. Pheromones and mammalian behavior. In: Menini, A. (Ed.), The Neurobiology of Olfaction. CRC Press/Taylor & Francis, Boca Raton (FL).

    Google Scholar 

  • Burke, J.M., Arnold, M.L., 2001. Genetics and the fitness of hybrids. Annu. Rev. Genet. 35, 31–52.

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock, T.H., Parker, G.A., 1995. Sexual coercion in animal societies. Anim. Behav. 49, 1345–1365.

    Article  Google Scholar 

  • Costa, K.L.C., Matta, S.L.P., Gomes, M.L.M., Paula, T.A.R., Freitas, K.M., Carvalho, F.A.R., Silveira, J.A., Dolder, H., Mendis-Handagama, S.M.L.C., 2011. Histomorphometric evaluation of the neotropical brown brocket deer Mazama gouazoubira testis, with an emphasis on cell population indexes of spermatogenic yield. Anim. Reprod. Sci. 127, 202–212.

    Article  PubMed  Google Scholar 

  • Curlewis, J.D., Loudon, A.S.I., Coleman, A.P.M., 1988. Oestrous cycles and the breeding season of the Père David’s deer hind (Elaphurus davidianus). J. Reprod. Fertil. 82, 119–126.

    Article  CAS  PubMed  Google Scholar 

  • Cursino, M.S., Duarte, J.M.B., 2016. Using sperm morphometry and multivariate analysis to di erentiate species of gray Mazama. R. Soc. Open Sci. 3, 160345, http://dx.doi.org/10.1098/rsos.160345.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawkins, R., 1982. The Extended Phenotype: The Long Reach of the Gene. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Dobzhansky, T., 1937. Genetics and the Origin of Species. Columbia University Press, New York.

    Google Scholar 

  • Dougherty, L.R., Shuker, D.M., 2015. The effect of experimental design on the measurement of mate-choice: a meta-analysis. Behav. Ecol. 26(2), 311–319.

    Article  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 

  • Dunn, J.C., Halenar, L.B., Davies, T.G., Cristobal-Azkarate, J., Reby, D., Sykes, D., Dengg, S., Fitch, W.T., Knapp, L.A., 2015. Evolutionary trade-off between vocal tract and testes dimensions in howler monkeys. Curr. Biol. 25, 1–6.

    Article  CAS  Google Scholar 

  • Eberhard, W.G., 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton Univ. Press, Princeton, NJ.

    Book  Google Scholar 

  • Edwards, D.A., 2015. The description of mate choice. Behav. Ecol. 26 (2), 301–310.

    Article  Google Scholar 

  • Escobedo-Morales, L., Mandujano, S., Eguiarte, L.E., Rodríguez-Rodríguez, M.A., Maldonado, J.E., 2016. First phylogenetic analysis of Mesoamerican brocket deer Mazama pandora and Mazama temama (Cetartiodactyla: Cervidae) based on mitochondrial sequences: implications on Neotropical deer evolution. Mamm. Biol. 81 (3), 303–313, http://dx.doi.org/10.1016/j.mambio.2016.02.003.

    Article  Google Scholar 

  • Ferrandiz-Rovira, M., Lemaître, J.F., Lardy, S., López, B.C., Cohas, A., 2014. Do pre- and post-copulatory sexually selected traits covary in large herbivores? BMC Evol. Biol. 14, 79.

    Article  PubMed  PubMed Central  Google Scholar 

  • Firman, R., Simmons, L.W., 2011. Experimental evolution of sperm competitiveness in a mammal. BMC Evol. Biol. 11, 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Freneau, G.E., Duarte, J.M.B., 2001. Biometria testicular e caracteristicas seminais de veado-catingueiro (Mazama gouazoubira) mantidos em cativeiro em Porto Nacional — TO. Ars Veterinária 17, 1–15.

    Google Scholar 

  • Futuyma, D.J., 2005. Evolution. Sinauer& Associates, Inc., Massachusetts.

    Google Scholar 

  • Gadella, B.M., 2010. Interaction of sperm with the zona pellucida during fertilization. Soc. Reprod. Fertil. Suppl. 67, 267–287.

    CAS  PubMed  Google Scholar 

  • Heckeberg, N.S., Erpenbeck, D., Wörheide, G., Rössner, G.E., 2016. Systematic relationships of five newly sequenced cervid species. Peer J 4, e2307, http://dx.doi.org/10.7717/peerj.2307.

    Article  PubMed  PubMed Central  Google Scholar 

  • Howard, D.J., Palumbi, S.R., Birge, L.M., Manier, M.K., 2009. Sperm and speciation. In: Birkhead, T.R., Hosken, D.J., Pitnick, S. (Eds.), Sperm Biology An Evolutionary Perspective. Elsevier, Oxford, pp. 367–403.

    Chapter  Google Scholar 

  • Hunt, W.G., Selander, R.K., 1973. Biochemical genetics of hybridisation in European house mice. Heredity 31, 11–33.

    Article  CAS  PubMed  Google Scholar 

  • Johnstone, R.A., 1997. The evolution of animal signals. In: Krebs, J.R., Davies, N.B. (Eds.), Behavioural Ecology. Blackwell, Oxford, pp. 155–178.

    Google Scholar 

  • Kodric-Brown, A., West, R.J.D., 2014. Asymmetries in premating isolating mechanisms in a sympatric species flock of pupfish (Cyprinodon). Behav. Ecol. 25, 69–75.

    Article  Google Scholar 

  • Kokko, H., Brooks, R., Jennions, M.D., Morley, J., 2003. The evolution of mate choice and mating biases. Proc. Biol. Sci. 270, 653–666.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lacy, R.C., Sherman, W., 1983. Kin recognition by phenotype matching. Am. Nat. 121, 489–512.

    Article  Google Scholar 

  • Liou, L.W., Price, T.D., 1994. Speciation by reinforcement of premating isolation. Evolution 48, 1451–1459.

    Article  PubMed  Google Scholar 

  • Martins, G.S., 2015. Avaliacao da existencia de isolamento reprodutivo entre duas espécies de veados cinza (Mazama gouazoibira e Mazama nemorivaga) por meio de machos hibridos. MSc. Thesis. Faculdade de Ciencias Agrarias e Veterinarias, Universidade Estadual Paulista, Jaboticabal, 61 pp.

    Google Scholar 

  • Mayr, E., 1963. Animal Species and Evolution. Harvard University Press, Cambridge.

    Book  Google Scholar 

  • McKinnon, J.S., Mori, S., Blackman, B.K., David, L., Kingsley, D.M., Jamieson, L., Chou, J., Schluter, D., 2004. Evidence for ecology’s role in speciation. Nature 429, 294–298.

    Article  CAS  PubMed  Google Scholar 

  • Morales-Pineyrua, J.T., Ungerfeld, R., 2012. Pampas deer (Ozotoceros bezoarticus) courtship and mating behavior. Acta Vet. Scand. 54, 60–66.

    Article  PubMed  PubMed Central  Google Scholar 

  • Muhlhauser, C., Blanckenhorn, W.U., 2002. The costs of avoiding matings in the dung fly Sepsis cynipsea. Behav. Ecol. 13, 359–365.

    Article  Google Scholar 

  • Parker, G.A., Birkhead, T., 2013. Polyandry: the history of a revolution. Philos. Trans. R. Soc. Lond. B368, 20120335.

  • Parker, G.A., Pizzari, T., 2010. Sperm competition and ejaculate economics. Biol. Rev. 85, 897–934.

    Article  PubMed  Google Scholar 

  • Parker, G.A., 1970. Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Philos. Soc. 45, 525–567.

    Article  Google Scholar 

  • Pereira, J.R.G., Polegato, B.F., Souza, S., Negrão, J.A., Duarte, J.M.B., 2006. Monitoring ovarian cycle and pregnancy in brown brocket deer (Mazama gouazoubira) by measurement of fecal progesterone metabolites. Theriogenology 2, 387–399.

    Article  CAS  Google Scholar 

  • Pfennig, K.S., 1998. The evolution of mate choice and the potential for conflict between species and mate-quality recognition. Proc. R. Soc. Lond. B Biol. 265, 1743–1748.

    Article  Google Scholar 

  • Price, E.O., 2008. Principles and Applications of Domestic Animal Behavior. An Introductory Text. CABI, Oxfordshire, UK.

    Google Scholar 

  • Ptacek, M.B., 1998. Interspecific mate choice in sailfin and shortfin mollies. Anim. Behav. 56, 1145–1154.

    Article  CAS  PubMed  Google Scholar 

  • Ptacek, M.B., 2000. The role of mating preferences in shaping interspecific divergence in mating signals invertebrates. Behav. Process. 51, 111–134.

    Article  CAS  Google Scholar 

  • Putman, R.J., Hunt, E.J., 1993. Hybridization between red and sika deer in Britain. Deer 9, 104–110.

    Google Scholar 

  • Rhymer, J.M., Simberloff, D., 1996. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27, 83–109.

    Article  Google Scholar 

  • Ross, C.L., Harrison, R.G., 2002. A fine-scale spatial analysis of the mosaic hybrid zone between Gryllusfirmus and Gryllus pennsylvanicus. Evolution 56, 2296–2312.

    Article  PubMed  Google Scholar 

  • Rossi, R.V., Duarte, J.M.B., 2008. Mazama nemorivaga. In:. The IUCN Red List of Threatened Species.

    Google Scholar 

  • Rossi, R.V., Bodmer, R., Duarte, J.M.B., Trovati, R.G., 2010. Amazonian Brown brocket deer Mazama nemorivaga (Cuvier). In: Duarte, J.M.B., Gonzalez, S. (Eds.), Neotropical Cervidology: Biology and Medicine of Latin American Deer. FUNEP-IUCN, pp. 202–210.

    Google Scholar 

  • Ryan, M.J., Tailor, R.C., 2015. Measures of mate choice: a comment on Dougherty & Shuker. Behav. Ecol. 26 (2), 323–324.

    Article  Google Scholar 

  • Samsudewa, D., Capitan, S.S., 2011. Reproductive behaviour of Timor deer (Rusa timorensis). Indones. Bull. Anim. Vet. Sci. 21, 108–113.

    Google Scholar 

  • Schluter, D., 1998. Ecological speciation in freshwater fishes. In: Grant, P.R. (Ed.), Evolution on Islands. Oxford University Press, New York.

    Google Scholar 

  • Schluter, D., 2001. Ecology and the origin of species. Trens Ecol. Evol. 16 (7), 372–380.

    Article  CAS  Google Scholar 

  • Schwenk, K., Brede, N., Streit, B., 2008. Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Philos. Trans. R. Soc. B Biol. Sci. 363, 2805–2811.

    Article  Google Scholar 

  • Senn, H.V., Pemberton, J.M., 2009. Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C elaphus) in a small geographical area. Mol. Ecol. 18, 862–876.

    Article  CAS  PubMed  Google Scholar 

  • Shah, K.B., Tripathy, S., Suganthi, H., Rudraiah, M., 2014. Profiling of luteal transcriptome during prostaglandin F2-alpha treatment in buffalo cows: analysis of signaling pathways associated with luteolysis. PLoS One 9 (8), e104127, http://dx.doi.org/10.1371/journal.pone.0104127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shurtliff, Q.R., Murphy, P.J., Yeiter, J.D., et al., 2013. Experimental evidence for asymmetric mate preference and aggression: behavioral interactions in a woodrat (Neotoma) hybrid zone. BMC Evol. Biol. 13, 220.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stockley, P., 2004. Sperm competition in mammals. Hum. Fertil. 7 (2), 91–97.

    Article  CAS  Google Scholar 

  • Szymura, J.M., Barton, N.H., 1986. Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Cracow in southern Poland. Evolution 40, 1141–1159.

    PubMed  Google Scholar 

  • Tomkins, T., Bryant, M.J., 1974. Oestrous behaviour of the ewe and the influence of treatment with progestagen. J. Reprod. Fertil. 41, 121–132.

    Article  CAS  PubMed  Google Scholar 

  • Tourmente, M., Gomendio, M., Roldan, E.R.S., 2011. Sperm competition and the evolution of sperm design in mammals. BMC Evol. Biol. 11, 12.

    Article  PubMed  PubMed Central  Google Scholar 

  • Trivers, R.L., 1972. Parental investment and sexual selection. In: Campbell, B. (Ed.), Sexual Selection and the Descent of Man, 1871-1971. Aldine, Chicago, pp. 136–179.

    Google Scholar 

  • Wyman, M.T., Locatelli, Y., Charlton, B.D., Reby, D., 2014. No preference in female sika deer for conspecific over heterospecific male sexual calls in a mate choice context. J. Zool. 293, 92–99.

    Article  Google Scholar 

  • Zanetti, E.S., Duarte, J.M.B., Polegato, B.F., Garcia, J.M., Canola, J.C., 2010. Assisted reproductive technology. In: Duarte, J.M.B., Gonzáles, S. (Eds.), Neotropical Cervidology. FUNEP, Jaboticabal, pp. 255–270.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Carranza.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carranza, J., Roldán, M., Peroni, E.C. et al. Weak premating isolation between two parapatric brocket deer species. Mamm Biol 87, 17–26 (2017). https://doi.org/10.1016/j.mambio.2017.02.009

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2017.02.009

Keywords

Navigation