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Lack of mate selectivity for genetic compatibility within the red brocket deer Mazama americana complex

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Abstract

Red brocket deer Mazama americana includes at least two lineages that differ at the level of karyotypes and phylogenetic relationships based on mtDNA. Also, hybrids between them have been proved to be nonviable or infertile. Since successful breeding is hampered, we expect selection to have produced a precopulatory barrier between these lineages based on courtship behaviour, to prevent investment in unsuccessful breeding. Here we made experiments with specimens in captivity to investigate mating preferences for partners belonging to the same or different karyotypes or lineages, along with a white-tailed deer buck (Odocoileous virginianus) as an outgroup control. Behaviours were video recorded and analysed by using Generalized Linear Mixed Models, with the interacting females and males as random subjects. The results show that although red brocket females never accepted copulations with the control male, trials involving pairs of red brocket deer may or may not end with copulation regardless as to whether the partners belonged to the same or different lineages. Although some male and female behaviours differed when pairs belonged to the same or different lineages, our results do not support the existence of a precopulatory barrier between lineages in the red brocket deer complex. We discuss the implications for sympatric speciation and species conservation.

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References

  • Abril, V.V., Carnelossi, E.A.G., Gonzales, 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 

  • Amato, G., Egan, M.G., Schaller, G.B., 2000. Mitochondrial DNA variation in Muntjac: evidence for discovery, rediscovery, and phylogenetic relationships. In: Schaller, G.B., Vrba, E.S. (Eds.), Antelopes, Deer, and Relatives: Fossil Record, Behavioural Ecology, Systematics, and Conservation. Yale University Press.

    Google Scholar 

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

    Google Scholar 

  • Aquino, C.I., Abril, V.V., Duarte, J.M.D., 2013. Meiotic pairing of B chromosomes, multiple sexual system, and Robertsonian in the red brocket deer Mazama Americana (Mammalia, Cervidae). Genet. Mol. Res. 12, 3566–3574.

    Article  CAS  PubMed  Google Scholar 

  • Baker, R.J., Bickham, J.W., 1986. Speciation by monobrachial centric fusions. Proc. Natl. Acad. Sci. U. S. A. 83, 8245–8248.

    Article  CAS  PubMed  PubMed Central  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 

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

    Article  Google Scholar 

  • Bodmer, R.E., 1997. Ecologia e conservação dos veados mateiro e catingueiro na Amazônia. In: Duarte, J.M.D. (Ed.), Biologia e Conservação de Cervídeos Sul-Americanos: Blastocerus, Ozotozeros e Mazama. Fundação de Estudos e Pesquisas em Agronomia. Medicina Veterinária e Zootecnia Jaboticabal, São Paulo Brazil.

    Google Scholar 

  • Bradbury, J.V., Vehrencamp, S.L., 2011. Principles of Animal Communication. Sinauer Associates, Sunderland MA.

    Google Scholar 

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

    Google Scholar 

  • Britton-Davidian, J., Catalan, J., Ramalhinho, M.G., Ganem, G., Auffray, J.-C., Capela, R., Biscoito, M., Searle, J.B., Mathias, M.L., 2000. Rapid chromosomal evolution in island mice. Nature 403, 158.

    Article  CAS  PubMed  Google Scholar 

  • Cabrera, A., 1960. Catálogo de los mamíferos de América del Sur. Revista Museo Argentino Bernardino Rivadavia 4, 309–732.

    Google Scholar 

  • Carranza, J., Roldán, M., Carvalho-Peroni, E.F., Duarte, J.M.B., 2017. Weak premating isolation between two parapatric brocket deer species. Mamm. Biol. 87, 17–26, http://dx.doi.org/10.1016/j.mambio.2017.02.009.

    Article  Google Scholar 

  • Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer Associates U.S.A, Sunderland, MA.

    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., Salviano, M.B., Abril, V.V., Zanetti, E.S., Duarte, J.M.B., 2014. The role of chromosome variation in the speciation of the red brocket deer complex: the study of reproductive isolation in females. BMC Evol. Biol. 14, 40.

    Article  PubMed  PubMed Central  Google Scholar 

  • Czernay, S., 1987. Spiesshirsche und Pudus. Die Neue Brehm-Bücherei 581, 1–84.

    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 matechoice: a metaanalysis. Behav. Ecol. 26, 311–319.

    Article  Google Scholar 

  • Duarte, J.M.B., Jorge, W., 2003. Morphologic and cytogenetic description of the small red brocket (Mazama bororo Duarte, 1996) in Brazil. Mammalia 67, 403–410.

    Article  Google Scholar 

  • Duarte, J.M.B., Merino, M.L., 1997. Taxonomia e evolução. In: Duarte, J.M.B. (Ed.), Biologia e Conservacao de Cervideos Sulamericanos: Blastocerus, Ozotoceros e Mazama. FUNEP, Jaboticabal, Brazil, pp. 1–21.

    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 

  • Duarte, J.M.B., 1996. Guia de Identificação de Cervídeos Brasileiros. Jaboticabal, Brazil, FUNEP.

    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 tradeoff 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.

    Google Scholar 

  • Eisemberg, J.F., 1989. Mammals of the Neotropics, vol. I. University of Chicago Press, Chicago (pp 449).

    Google Scholar 

  • Emmons, L.H., 1990. Neotropical Rainforest Mammals, a Field Guide. University of Chicago Press, Chicago (pp 281).

    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, 303–313.

    Article  Google Scholar 

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

    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 

  • Geist, V., 1998. Deer of the World: Their Evolution, Behaviour, and Ecology. Stackpole Books, Mechanicsburg.

    Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Howard, D.J., Gregory, P.G., Chu, J.M., Cain, M.L., 1998. Conspecific sperm precedence is an effective barrier to hybridization between closely related species. Evolution 52, 511–516.

    Article  PubMed  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.

    Google Scholar 

  • Huang, L., Wang, J., Nie, W., Su, W., Yang, F., 2006. Tandem chromosome fusions in karyotypic evolution of Muntiacus: evidence from M feae and M. gongshanensis. Chromosome Res. 14, 637–647.

    Article  CAS  PubMed  Google Scholar 

  • Irwin, D.E., Irwin, J.H., Price, T.D., 2001. Ring species as bridges between microevolution and speciation. Genetica 112-113, 223–243.

    Article  CAS  PubMed  Google Scholar 

  • Johnstone, R.A., 1997. The evolution of animal signals. In: Krebs, J.R., Davies, N.B. (Eds.), Behavioural Ecology: An Evolutionary Approach., 4th ed. Blackwell Scientific, Oxford, pp. 155–178.

    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 

  • Ludt, C.J., Schroeder, W., Rottmann, O., Kuehn, R., 2004. Mitochondrial DNA phylogeography of red deer (Cervus elaphus). Mol. Phylogenet. Evol. 31, 1064–1083.

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

  • Morales-Piñeyrua, 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 

  • Parker, G.A., Birkhead, T., 2013. Polyandry: the history of a revolution. Philos. Trans. R. Soc. Lond. B 368, 20120335.

    Article  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 

  • Pfennig, K.S., 1998. The evolution of mate choice and the potential for conflict between species and matequality recognition. Philos. Trans. R. Soc. Lond. Bio. 265, 1743–1748.

    Article  Google Scholar 

  • Piálek, J., Albrecht, T., 2005. Choosing mates: complementary versus compatible genes. Trends Ecol. Evol. 20 (2), 63.

    Article  PubMed  Google Scholar 

  • Price, E.O., 2008. Principles and Applications of Domestic Animal Behavior An Introductory Text. CABI, Cambrige University Press, Cambridge, 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 in vertebrates. 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 

  • Rossi, R.V., 2000. Taxonomia de Mazama Ranfinesque, 1817 do Brasil (Artyodactyla, Cervidae). Universidade de São Paulo, São Paulo, Brazil (Msc, Thesis).

    Google Scholar 

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

    Article  Google Scholar 

  • Salviano, M.B., Cursino, M.S., Zanetti, E.D.S., Abril, V.V., Duarte, J.M.B., 2017. Intraspecific chromosome polymorphisms can lead to reproductive isolation and speciation: an example in red brocket deer (Mazama americana). Biol. Reprod. 96 (6), 1279–1287, http://dx.doi.org/10.1093/biolre/iox041.

    Article  PubMed  Google Scholar 

  • Samsudewa, D., Capitan, S.S., 2011. Reproductive behaviour of Timor deer (Rusa timorensis). Wartazoa 21, 108–113.

    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 

  • Servedio, M.R., Noor, M.A.F., 2003. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Syst. 34, 339–364.

    Article  Google Scholar 

  • Shackleton, M.A., Jennions, M.D., Hunt, J., 2005. Fighting success and attractiveness as predictors of male mating success in the black fleld cricket, Teleogryllus commodus: the effectiveness of nochoice tests. Behav. Ecol. Sociobiol. 58, 1–8.

    Article  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Todesco, M., Pascual, M.A., Owens, G.L., et al., 2016. Hybridization and extinction. Evol. Appl. 9, 892–908.

    Article  CAS  PubMed  PubMed Central  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 

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

    Google Scholar 

  • Varela, D.M., Trovati, R.G., Guzmán, K.R., Rossi, R.V., Duarte, J.M.B., 2010. Red brocket deer-Mazama americana. In: Duarte, J.M.B., González, S. (Eds.), Neotropical Cervidoloy: Biology and Medicine of Latin American Deer. FUNEP/IUCN, Jaboticabal, pp. 151–159.

    Google Scholar 

  • Veen, T., Faulks, J., Rodríguez-Muñoz, R., Tregenza, T., 2011. Premating reproductive barriers between hybridising cricket species differing in their degree of polyandry. PLoS One 6, 1–7.

    Article  CAS  Google Scholar 

  • Wagner, C.E., Harmon, L.J., Seehausen, O., 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487, 366–369.

    Article  CAS  PubMed  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 

  • van Doorn, G., Edelaar, P., Weissing, F.J., 2009. On the origin of species by natural and sexual selection. Science 326, 1704–1707.

    Article  PubMed  CAS  Google Scholar 

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  1. Núcleo de Pesquisa e Conservação de Cervídeos (NUPECCE), Universidade Estadual Paulista (Unesp), Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal, Brazil

    Juan Carranza, Mar Roldán & José Maurício Barbanti Duarte

  2. Ungulate Research Unit, Cátedra de Recursos Cinegéticos y Piscícolas (CRCP), Universidad de Córdoba, 14071, Córdoba, Spain

    Juan Carranza

  3. Medicina Veterinaria y Zootecnia, Universidad Agraria del Ecuador, Guayaquil, Ecuador

    Juan Carranza

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  1. Juan Carranza
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Correspondence to Juan Carranza.

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Carranza, J., Roldán, M. & Duarte, J.M.B. Lack of mate selectivity for genetic compatibility within the red brocket deer Mazama americana complex. Mamm Biol 88, 168–175 (2018). https://doi.org/10.1016/j.mambio.2017.09.006

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