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Multiple paternity and kinship in the gray fox (Urocyon cinereoargenteus)

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Abstract

Despite mounting evidence that extra-pair copulations (EPCs) are common in the Canidae, no studies have examined the most basal member of this family, the gray fox (Urocyon cinereoargenteus). In this study we explored the possibility that gray foxes may be socially, but not genetically, monogamous. Multiple paternity was confirmed in one litter and suspected in three others (n =7), thus 14.3–57.1% of all litters had more than one father. In this high-density population, multiple paternity may be one strategy to reduce inbreeding, although only one pair was significantly related to each other (r =0.36). Mother-daughter pairs were more common than father-son pairs. These results coupled with a previous study showing a female-biased sex ratio suggest male-biased dispersal and the potential for helper females.

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References

  • Baker, P.J., Funk, S.M., Bruford, M.W., Harris, S. 2004. Polygynandry in a red fox population: implications for the evolution of group living in canids? Behav. Ecol. 15, 766–778.

    Article  Google Scholar 

  • Bisbal, F.G. 1982. Nuevos registros de distribution para el zorro gris Urocyon cinereoargenteus venezuelae. Acta Cient. Venez. 33, 255–257.

    Google Scholar 

  • Boutin-Ganache, I., Raposo, M., Raymond, M., Deschepper, C.F. 2001. M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechniques 31, 24–28.

    Article  CAS  Google Scholar 

  • Chamberlain, M.J., Leopold, B.D. 2000. Spatial use patterns, seasonal habitat selection, and interactions among adult gray foxes in Mississippi. J. Wildl. Manage. 64, 742–751.

    Article  Google Scholar 

  • Cothran, E.G., Smith, M.H., Wolff, J.O., Gentry J.B. 1991. Mammals of the Savannah River Site. SRO-NERP-21, Aiken, SC.

    Google Scholar 

  • Cumbie, P.M., Jenkins, J.H. 1975. Mercury accumulation in native mammals of the southeast. In: Proceedings of the Twenty-Eighth Annual Conference of the Southeastern Association of Game and Fish Commissioners, White Sulphur Springs, West Virginia, pp. 639–648.

    Google Scholar 

  • DeWoody, J.A., Schupp, J., Kenefic, L., Busch, J., Murfitt, L., Keim, P. 2004. Universal method for producing ROX-labeled size standards suitable for automated genotyping. BioTechniques 37, 348–352.

    Article  CAS  Google Scholar 

  • Follmann, E.H. 1973. Comparative ecology and behavior of red and gray foxes. Ph.D. Dissertation, Southern Illinois University, Carbondale.

    Google Scholar 

  • Fritzell, E.K., Haroldson, K.J. 1982. Urocyon cinereoargenteus. Mamm. Species 189, 1–8.

    Article  Google Scholar 

  • Fuller, T.K. 1978. Variable home-range sizes of female gray foxes. J. Mammal. 59, 446–449.

    Article  Google Scholar 

  • Gaines, K.F., Lord, C.G., Boring, C.S., Brisbin Jr., I.L., Gochfeld, M., Burger, J. 2000. Raccoons as potential vectors of radionuclide contamination to human food chains from a nuclear industrial site. J. Wildl. Manage. 64, 199–208.

    Article  Google Scholar 

  • Geffen, E., Gompper, M.E., Gittleman, J.L., Luh, H.K., Macdonald, D.W., Wayne, R.K. 1996. Size, life-history traits, and social organization in the canidae: reevaluation. Am. Nat. 147, 140–160.

    Article  Google Scholar 

  • Gittleman, J.L. 1989. Carnivore group living; comparative trends. In: Gittleman, J.L. (Ed.), Carnivore Behavior, Ecology, and Evolution, vol. 1. Cornell University Press, Ithaca, NY, pp. 183–207.

    Chapter  Google Scholar 

  • Goodnight, K.F., Queller, D.C. 1999. Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol. 8, 1231–1234.

    Article  Google Scholar 

  • Jenkins, J.H., Fendley, T.T. 1968. The extent of contamination, detection, and health significance of high accumulations of radio-activity in southeastern game populations. Proc. Southeast. Assoc. Game Fish Comm. 22, 89–95.

    Google Scholar 

  • Jenkins, J.H., Provost, E.E., Fendley, T.T., Monroe, J.R., Brisbin Jr., I.L., Lenarz, M.S. 1979. Techniques and problems associated with a consecutive twenty-five year furbearer trapline census. In: Bobcat Research Conference, Front Royal, Virginia.

  • Jeselnik, D.L. 1981. Comparative analysis of movement, behavior, and habitat utilization of free-ranging gray foxes. M.S. Thesis, University of Georgia, Athens.

    Google Scholar 

  • Kalinowski, S.T., Taper, M.L., Marshall, T.C. 2006. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106.

    Article  Google Scholar 

  • Kamler, J.F., Ballard, W.B., Gese, E.M., Harrison, R.L., Karki, S., Mote, K. 2004. Adult male emigration and a female-based social organization in swift foxes, Vulpes velox. Anim. Behav. 67, 699–702.

    Article  Google Scholar 

  • Kitchen, A.M., Gese, E.M., Waits, L.P., Karki, S.M., Schauster, E.R. 2006. Multiple breeding strategies in the swift fox, Vulpes velox. Anim. Behav. 71, 1029–1038.

    Article  Google Scholar 

  • Kleiman, D.G. 1977. Monogamy in mammals. Quat. Rev. Biol. 52, 39–69.

    Article  CAS  Google Scholar 

  • Layne, J.N. 1958. Reproductive characteristics of the gray fox in southern Illinois. J. Wildl. Manage. 22, 157–163.

    Article  Google Scholar 

  • Lindblad-Toh, K., Wade, C.M., Mikkelsen, T.S., Karlsson, E.K., Jaffe, D.B., et al. 2005. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438, 803–819.

    Article  CAS  Google Scholar 

  • Macdonald, D.W. 1979. “Helpers” in fox society. Nature 282, 69–71.

    Article  Google Scholar 

  • Moehlman, P.D. 1989. Intraspecific variation in canid social systems. In: Gittleman, J.L. (Ed.), Carnivore Behavior, Ecology, and Evolution. Cornell University Press, Ithaca, NY, pp. 143–163.

    Chapter  Google Scholar 

  • Peakall, R., Smouse, P.E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295.

    Article  Google Scholar 

  • Ralls, K., Pilgrim, K.L., White, P.J., Paxinos, E.E., Schwartz, M.K., Fleischer, R.C. 2001. Kinship, social relationships, and den sharing in kit foxes. J. Mammal. 82, 858–866.

    Article  Google Scholar 

  • Raymond, M., Rousset, F. 1995. GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.

    Article  Google Scholar 

  • Roemer, G.W., Smith, D.A., Garcelon, D.K., Wayne, R.K. 2001. The behavioural ecology of the island fox (Urocyon littoralis). J. Zool. 255, 1–14.

    Article  Google Scholar 

  • Sawyer, D.T. 1988. Gray fox home range dynamics and validation of the scent station transect technique. M.S. Thesis, Clemson University.

  • Selvin, S. 1980. Probability of non-paternity determined by multiple allele codominant systems. Am. J. Hum. Genet. 32, 276–278.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sillero-Zubiri, C., Gottelli, D., Macdonald, D.W. 1996. Male philopatry, extra pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav. Ecol. Sociobiol. 38, 331–340.

    Article  Google Scholar 

  • Small, R.L. 1971. Interspecific competition among three species of carnivora on the Spider Ranch, Yavapai County, Arizona. M.S. Thesis, University of Arizona, Tucson.

    Google Scholar 

  • Smouse, P.E., Long, J.C., Sokal, R.R. 1986. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst. Zool. 35, 627–632.

    Article  Google Scholar 

  • Trapp, G.R. 1973. Comparative behavioral ecology of two southwest Utah carnivores: Bassariscus astutus and Urocyon cinereoargenteus. Ph.D. Dissertation, University of Wisconsin, Madison.

    Google Scholar 

  • Waits, L.P., Luikart, G., Taberlet, P. 2001. Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol. Ecol. 10, 249–256.

    Article  CAS  Google Scholar 

  • Weston, J.L. 2001. Demographics of a protected population of gray foxes (Urocyon cinereoargenteus) in South Carolina. Ph.D. Dissertation, University of Georgia, Athens.

    Google Scholar 

  • Weston, J.L., Brisbin Jr., I.L. 2003. Demographics of a protected population of gray foxes (Urocyon cinereoargenteus) in South Carolina. J. Mammal. 84, 996–1005.

    Article  Google Scholar 

  • Weston, J.L., Schable, N.A., Glenn, T.C. 2004. Characterization of 6 microsatellite primers for the grey fox (Urocyon cinereoargenteus). Mol. Ecol. Notes 4, 503–505.

    Article  CAS  Google Scholar 

  • Wood, J.E. 1958. Age structure and productivity of a gray fox population. J. Mammal. 39, 74–86.

    Article  Google Scholar 

  • Wooding, J.B. 1984. Coyote food habits and the spatial relationship of coyotes and foxes in Mississippi and Alabama. M.S. Thesis, Mississippi State University, Starkville.

    Google Scholar 

  • Zabel, C.J., Taggart, S.J. 1989. Shift in red fox, Vulpes vulpes, mating system associated with El Nino in the Bering Seas. Anim. Behav. 38, 830–838.

    Article  Google Scholar 

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Correspondence to Julie L. Weston Glenn.

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Weston Glenn, J.L., Civitello, D.J. & Lance, S.L. Multiple paternity and kinship in the gray fox (Urocyon cinereoargenteus). Mamm Biol 74, 394–402 (2009). https://doi.org/10.1016/j.mambio.2008.10.003

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