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Genetic polymorphism and structure of wild and zoo populations of the fosa (Eupleridae, Carnivora), the largest living carnivoran of Madagascar

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Abstract

Cryptoprocta ferox, or fosa, is the largest living endemic carnivoran of Madagascar, with presumably high dispersal capacity, and for which no broad scale phylogeographic study has been conducted to date. This species is considered “Vulnerable” by the IUCN and the subject of a captive breeding program; approximately 113 individuals are held in 57 zoos. The aim of this study was to examine the genetic structure and polymorphism within both captive and wild populations, to determine possible lineage variation, and to make recommendations for the captive breeding program. For this purpose, we analyzed three mitochondrial (Cytochrome b, ND2, Control Region) and one nuclear (Beta-fibrinogen intron 7) markers. The results showed an overall low level of genetic polymorphism, likely related to its dispersal capacity, and some genetic structure possibly associated with geographical barriers, such as large rivers. The genetic diversity of the captive population was greater than that of wild individuals included herein, suggesting that the captive population encompasses a considerable proportion of the genetic diversity of the species. This genetic variability is presumably the consequence of frequent imports of wild animals into zoos from different areas of Madagascar, and subsequent exchanges between zoos. Based on the low overall genetic polymorphism of the species and the absence of deeply divergent lineages, we recommend the continued mixing of captive animals. Our results may help the management of the fosa in the wild and in captivity, which is crucial for a species that faces many threats in the wild, in particular habitat degradation and hunting pressure. In any case, enhanced protection of the species and its forested habitat is urgently needed.

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References 68-77

  • Albignac, R., 1975. Breeding the fossa at Montpellier Zoo. Int. Zoo Yearb. 15, 147–150.

    Google Scholar 

  • Albignac, R., 1976. L’écologie de Mungotictis decemlineata dans les forêts décidues de l’ouest de Madagascar. Terre et Vie 30, 347–376.

    Google Scholar 

  • Alroy, J., 2015. Limits to captive breeding of mammals in zoos. Conserv. Biol 29, 926–931.

    PubMed  Google Scholar 

  • Bandelt, H.J., Forster, P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48.

    CAS  PubMed  Google Scholar 

  • Bennett, C.E., Pastorini, J., Dollar, L., Hahn, W.J., 2009. Phylogeography of the Malagasy ring-tailed mongoose, Galidia elegans, from mtDNA sequence analysis. Mitochondrial DNA 20, 7–14.

    CAS  PubMed  Google Scholar 

  • Crowley, B.E., 2010. A refined chronology of prehistoric Madagascar and the demise of the megafauna. Quat. Sci. Rev. 29, 2591–2603.

    Google Scholar 

  • Cushman, S.A., Lewis, J., 2010. Movement behavior explains genetic differentiation in American black bears. Landsc. Ecol. 25, 1613–1625.

    Google Scholar 

  • Decary, R., Payot, Paris 1950. La faune Malgache: son rôle dans les croyances et les usages indigènes.

    Google Scholar 

  • Dollar, L., 1999. Preliminary report on the status, activity cycle, and ranging of Cryptoprocta ferox in the Malagasy rainforest, with implications for conservation. Small Carnivore Conser. 20, 7–10.

    Google Scholar 

  • Dollar, L., Ganzhorn, J.U., Goodman, S.M., 2007. Primates and other prey in the seasonally variable diet of Cryptoprocta ferox in the dry deciduous forest of western Madagascar. In: Gursky, S., Nekaris, K.A. (Eds.), Predation on Primates. Springer, New York, pp. 63–76.

    Google Scholar 

  • Ebenhard, T., 1995. Conservation breeding as a tool for saving animal species from extinction. Trends Ecol. Evol. 10, 438–443.

    CAS  PubMed  Google Scholar 

  • Farris, Z.J., Gerber, B.D., Valenta, K., Rafaliarison, R., Razafimahaimodison, J.-C., Larney, E., Rajaonarivelo, T., Randriana, Z., Wright, P.C., Chapman, C.A., 2017. Threats to a rainforest carnivore community: A multi-year assessment of occupancy and co-occurrence in Madagascar. Biol. Conserv. 210, 116–124.

    Google Scholar 

  • Farris, Z.J., Golden, C.D., Karpanty, S., Murphy, A., Stauffer, D., Ratelolahy, F., Andrianjakarivelo, V., Holmes, C.M., Kelly, M.J., 2015. Hunting, exotic carnivores, and habitat loss: Anthropogenic effects on a native carnivore community, Madagascar. PLoS One 10, https://doi.org/10.1371/journal.pone.0136456.

    Google Scholar 

  • Farris, Z.J., Kelly, M.J., Karpanty, S., Ratelolahy, F., 2016. Patterns of spatial co-occurrence among native and exotic carnivores in north-eastern Madagascar. Anim. Conserv 19, 189–198.

    Google Scholar 

  • Flynn, J.J., Finarelli, J.A., Zehr, S., Hsu, J., Nedbal, M.A., 2005. Molecular phylogeny of the Carnivora (Mammalia): Assessing the impact of increased sampling on resolving enigmatic relationships. Syst. Biol 54, 317–337.

    PubMed  Google Scholar 

  • Garbe, J.R., Da, Y., 2008. Pedigraph: a software tool for the graphing and analysis of large complex pedigree. In: User manual Version 2.4. University of Minnesota: Department of Animal Science.

    Google Scholar 

  • Gerber, B., Karpanty, S.M., Crawford, C., Kotschwar, M., Randianantenaina, J., 2010. An assessment of carnivore relative abundance and density in the eastern rainforests of Madagascar using remotely-triggered camera traps. Oryx 44, 219–222.

    Google Scholar 

  • Gippoliti, S., 2011. Zoos and conservation in the XXI Century: overlooked meeting points between ecology and social sciences? MuseologiaScientifica 5, 168–176.

    Google Scholar 

  • Goodman, S.M., 2009. Family Eupleridae. Madagascar carnivores. In: Wilson, D., Mittermeier, R.A. (Eds.), Handbook of the Mammals of the World, vol. 1. Lynx edicions, Barcelona, pp. 330–351, Carnivores.

    Google Scholar 

  • Goodman, S.M., 2013. Carnivorans or the order Carnivora. In: Goodman, S.M., Raherilalao, M.J. (Eds.), Atlas of Selected Land Vertebrates of Madagascar. Association Vahatra, Antananarivo, pp. 271–285.

    Google Scholar 

  • Goodman, S.M., Ganzhorn, J.U., 2004. Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers. J. Biogeogr. 1, 47–55.

    Google Scholar 

  • Goodman, S.M., Rasoloarison, R.M., Ganzhorn, J.U., 2004. On the specific identification of subfossil Cryptoprocta (Mammalia, Carnivora) from Madagascar. Zoosystema 26, 129–143.

    Google Scholar 

  • Hall, T.E., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids S 41, 95–98.

    CAS  Google Scholar 

  • Harper, G.J., Steininger, M.K., Tucker, C.J., Juhn, D., Hawkins, F., 2007. Fifty years of deforestation and forest fragmentation in Madagascar. Environ. Conserv 34, 325–333.

    Google Scholar 

  • Hassanin, A., Veron, G., 2016. The complete mitochondrial genome of the boky-boky, Mungotictis decemlineata, the first representative of the Malagasy carnivores (Mammalia, Carnivora, Eupleridae). Mitochondrial DNA 27, 908–909.

    CAS  PubMed  Google Scholar 

  • Hawkins, C.E., 2003. Cryptoprocta ferox, Fossa, Fosa. In: Goodman, S.M., Benstead, J.P. (Eds.), The Natural History of Madagascar. The University of Chicago Press, Chicago, pp. 1360–1363.

    Google Scholar 

  • Hawkins, C.E., Racey, P.A., 2005. Low population density of a tropical forest carnivore, Cryptoprocta ferox: Implications for protected area management. Oryx 39, 35–43.

    Google Scholar 

  • IUCN, e.T5760A97189 2016. The IUCN Red List of Threatened Species 2016., https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T5760A97189.en (accessed 3 May 2017).

    Google Scholar 

  • Irwin, M.T., Wright, P.C., Birkinshaw, C., Fisher, B.L., Gardner, C.J., Glos, J., Goodman, S.M., Loiselle, P., Robeson, P., Raharison,J.L., Raherilalao, M.J., Rakotondravony, D., Raselimanana, A., Ratsimbazafy, J., Sparks, J.S., Wilmé, L., Ganzhorn, J.U., 2010. Patterns of species change in anthropogenically disturbed forests of Madagascar. Biol. Conserv. 143, 2351–2362.

    Google Scholar 

  • Jansen Van Vuuren, B., Woolaver, L., Goodman, S.M., 2012. Genetic population structure in the boky-boky (Carnivora: Eupleridae), a conservation flagship species in the dry deciduous forests of central western Madagascar. Anim. Conserv. 15, 164–173.

    Google Scholar 

  • Koepfli, K.P., Jenks, S.M., Eizirik, E., Zahirpour, T., Van Valkenburgh, B., Wayne, R.K., 2006. Molecular systematics of the Hyaenidae: relationships of a relictual lineage resolved by a molecular supermatrix. Mol. Phylogenet. Evol. 38, 603–620.

    CAS  PubMed  Google Scholar 

  • Kremen, C., Cameron, A., Moilanen, A., Phillips, S.J., Thomas, C.D., Beentje, H., Dransfield, J., Fisher, B.L., Glaw, F., Good, T.C., Harper, G.J., Hijmans, R.J., Lees, D.C., Louis Jr., E., Nussbaum, R.A., Raxworthy, C.J., Razafimpahanana, A., Schatz, G.E., Vences, M., Vieites, D.R., Wright, P.C., Zjhra, M.L., 2008. Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science 320 (5873), 222–226, https://doi.org/10.1126/science.1155193.

    CAS  PubMed  Google Scholar 

  • Librado, P., Rosas, J., 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.

    CAS  PubMed  Google Scholar 

  • Logan, M.K., Gerber, B.D., Karpanty, S.M., Justin, S., Rabenahy, F.N., 2015. Assessing carnivore distribution from local knowledge across a human-dominated landscape in central-southeastern Madagascar. Anim. Conserv. 18, 82–91.

    Google Scholar 

  • Lührs, M.L., 2012. Social organisation and mating system of the fosa (Cryptoprocta ferox). PhD Thesis. Georg-August-Universität Göttingen.

    Google Scholar 

  • Lührs, M.L., Dammhahn, M., 2010. An unusual case of cooperative hunting in a solitary carnivore. J. Ethol. 28, 379–383.

    Google Scholar 

  • Lührs, M.L., Kappeler, P.M., 2013. Simultaneous GPS tracking reveals male associations in a solitary carnivore. Behav. Ecol. Sociobiol. 67, 1731–1743.

    Google Scholar 

  • Lührs, M.L., Dammhahn, M., Kappeler, P.M., 2013. Strength in numbers: Males in a carnivore grow bigger when they associate and hunt cooperatively. Behav. Ecol. 24, 21–28.

    Google Scholar 

  • Manel, S., Schwartz, M.K., Luikart, G., Taberlet, P., 2003. Landscape genetics: combining landscape ecology and population genetics. Trends Ecol. Evol. 18, 189–197.

    Google Scholar 

  • McPhee, M.E., 2003. Generations in captivity increases behavioral variance: considerations for captive breeding and reintroduction programs. Biol. Conserv 115, 71–77.

    Google Scholar 

  • Meador, L.R., Godfrey, LR., Rakotondramavo, J.C., Ranivoharimanana, L., Zamora, A., Sutherland, M.R., Irwin, M.T., 2017. Cryptoprocta spelea (Carnivora: Eupleridae): What did it eat and how do we know? J. Mamm. Evol., https://doi.org/10.1007/s10914-017-9391-z.

    Google Scholar 

  • Palomares, F., Godoy, J., Piriz, A., O’Brien, S., Johnson, W., 2002. Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility forthe Iberian lynx. Mol. Ecol. 11, 2171–2182.

    CAS  PubMed  Google Scholar 

  • Patou, M.L., McLenachan, P.A., Morley, C.G., Couloux, A., Jennings, A.P., Veron, G., 2009. Molecular phylogeny of the Herpestidae (Mammalia, Carnivora) with a special emphasis on the Asian Herpestes. Mol. Phylogenet. Evol. 53, 69–80.

    CAS  PubMed  Google Scholar 

  • Patou, M.L., Wilting, A., Gaubert, P., Esselstyn, J.A., Cruaud, C., Jennings, A.P., Fickel, J., Veron, G., 2010. Evolutionary history of the Paradoxurus palm civets - a new model for Asian biogeography. J. Biogeogr. 37, 2077–2097.

    Google Scholar 

  • Pomerantz, J., Rasambainarivo, F.T., Dollar, L., Rahajanirina, L.P., Andrianaivoarivelo, R., Parker, P., Dubovi, E., 2016. Prevalence of antibodies to selected viruses and parasites in introduced and endemic carnivores in western Madagascar. J. Wildl. Dis. 52, 544–552.

    PubMed  Google Scholar 

  • Poux, C., Madsen, O., Marquard, E., Vieites, D.R., de Jong, W.W., Vences, M., 2005. Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Syst. Biol. 54, 719–730.

    PubMed  Google Scholar 

  • Rambaut, A., 2012. Figtree Version 1.4.0 (accessed 30 September 2013) https://doi.org/tree.bio.ed.ac.uk/software/figtree/.

    Google Scholar 

  • Ramiadantsoa, T., Ovaskainen, O., Rybicki, J., Hanski, I., 2015. Large-scale habitat corridors for biodiversity conservation: a forest corridor in Madagascar. PLoS One 10 (7), e0132126, https://doi.org/10.1371/journal.pone.0132126.

    PubMed  PubMed Central  Google Scholar 

  • Rasambainarivo, F.T., Goodman, S.M., 2018. Diseases risks from introduced species to malagasy wildlife. In: Miller, R.E., Calle, P., Lamberski, N. (Eds.), Fowler’S Zoo and Wildlife Medicine., 9th edition. W. B. Saunders, St. Louis.

    Google Scholar 

  • Rasoloarison, R.M., Rasolonandrasana, B.P.N., Ganzhorn, J.U., Goodman, S.M., 1995. Predation on vertebrates in the Kirindy Forest, western Madagascar. Ecotropica 1, 59–65.

    Google Scholar 

  • Razafimanantsoa, L., 2003. Goodman, S.M., Benstead, J.P. (Eds.), The Natural History of Madagascar. The University of Chicago Press, Chicago, pp. 1357–1360.

    Google Scholar 

  • Reiter, J., 2015. Fossa Cryptoprocta ferox International Studbook 2014. EAZA, Zoo Duisburg, Duisburg.

    Google Scholar 

  • Rivera-Ortiz, F.A., Aguilar, R., Arizmendi, M.D.C., Quesada, M., Oyama, K., 2015. Habitat fragmentation and genetic variability of tetrapod populations. Anim. Conserv. 18, 249–258.

    Google Scholar 

  • Schneider, T.C., Kappeler, P.M., Pozzi, L., 2016. Genetic population structure and relatedness in the narrow-striped mongoose (Mungotictis decemlineata), a social Malagasy carnivore with sexual segregation. Ecol. Evol. 11, 3734–3749.

    Google Scholar 

  • Schwitzer, C., Mittermeier, R., Davies, N., Johnson, S., Ratsimbazafy, J., Razafindramanana, J., Louis Jr., E.E., Rajaobelina, S., 2013. Lemurs of Madagascar: A Strategy for Their Conservation 2013–2016. IUCN SSC Primate Specialist Group. Bristol Conservation and Science Foundation, and Conservation International, Bristol.

    Google Scholar 

  • Snyder, N.F.R., Derrickson, S.R., Beissinger, S.R., Wiley, J.W., Smith, T.B., Toone, W.D., Miller, B., 1996. Limitations of captive breeding in endangered species recovery. Conserv. Biol. 10, 338–348.

    Google Scholar 

  • Sorenson, M.D., Ast, J.C., Dimcheff, D.E., Yuri, T., Mindell, D.P., 1999. Primers for PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol. Phylogenet. Evol. 12, 105–114.

    CAS  PubMed  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor, M.E., 1989. Locomotor adaptations by carnivores. In: Gittleman, J.L. (Ed.), Carnivore Behaviour, Ecology and Evolution. Chapman and Hall, London, pp. 382–409.

    Google Scholar 

  • Veron, G., 1999. Pads morphology in the Viverridae (Carnivora). Acta Theriol 44, 363–376.

    Google Scholar 

  • Veron, G., Dupré, D., Jennings, A.P., Gardner, L.C.J., Hassanin, A., Goodman, S.M., 2017. New insights into the systematics of Malagasy mongoose-like carnivorans (Carnivora, Eupleridae, Galidiinae) based on mitochondrial and nuclear DNA sequences. J. Zool. Syst. Evol. Res. 55, 250–264.

    Google Scholar 

  • Veron, G., Goodman, S.M., 2018. One or two species of the rare Malagasy carnivoran Eupleres (Eupleridae)? New insights from molecular data. Mammalia 2, 107–112, https://doi.org/10.1515/mammalia-2016-0182.

    Google Scholar 

  • Veron, G., Heard, S., 2000. Molecular systematics of the Asiatic Viverridae (Carnivora) inferred from mitochondrial cytochrome b sequence analysis. J. Zool. Syst. Evol. Res. 38, 209–217.

    Google Scholar 

  • Veron, G., Heard Rosenthal, S., Long, B., Roberton, S., 2004. The molecular systematics and conservation of an endangered carnivore, the Owston’s palm civet Chrotogale owstoni (Thomas, 1912) (Carnivora, Viverridae, Hemigalinae). Anim. Conserv 7, 107–112.

    Google Scholar 

  • Veron, G., Patou, M.L., Debruyne, R., Couloux, A., Fernandez, DAP., Wong, S.T., Fuchs, J., Jennings, A.P., 2015a. Systematics of the Southeast Asian mongooses (Herpestidae, Carnivora) - Solving the mystery of the elusive collared mongoose and Palawan mongoose. Zool. J. Linn. Soc. 173, 236–248.

    Google Scholar 

  • Veron, G., Patou, M.L., Jennings, A.P., 2015b. Molecular systematics of the small-toothed palm civet (Arctogalidia trivirgata) reveals a strong divergence of Bornean populationsMamm. Biol 80, 347–354.

    Google Scholar 

  • Veron, G., Willsch, M., Dacosta, V., Patou, M.L., Seymour, A., Bonillo, C., Couloux, A., Wong, S.T., Jennings, A.P., Fickel, J., Wilting, A., 2014. The distribution of the Malay civet Viverra tangalunga (Carnivora: Viverridae) across Southeast Asia: natural or human-mediated dispersal? Zool. J. Linn. Soc. 170, 917–932.

    Google Scholar 

  • Vogler, B.R., Bailey, C.A., Shore, G.D., McGuire, S.M., Engberg, S.E., Fickel, J., Louis Jr., E.E., Brenneman, R.A., 2009. Characterization of 26 microsatellite marker loci in the fossa (Cryptoprocta ferox). Conserv. Genet. 10, 1449–1453.

    CAS  Google Scholar 

  • Whitmee, S., Orme, C.D.L., 2013. Predicting dispersal distance in mammals: a trait-based approach. J. Anim. Ecol. 82, 211–221.

    PubMed  Google Scholar 

  • Wilmé, L., Goodman, S.M., Ganzhorn, J.U., 2006. Biogeographic evolution of Madagascar’s microendemic biota. Science 312, 1063–1065.

    PubMed  Google Scholar 

  • Winnepenninckx, B., Backeljau, T., De Wachter, R., 1993. Extraction of high molecular weight DNA from molluscs. Trends Genet 9, 407.

    CAS  PubMed  Google Scholar 

  • Yoder, A.D., Burns, M.M., Zehr, S., Delefosse, T., Veron, G., Goodman, S.M., Flynn, J.J., 2003. Single origin of Malagasy Carnivora from an African ancestor. Nature 421, 734–737.

    CAS  PubMed  Google Scholar 

  • Yu, L., Zhang, Y.P., 2005. Phylogenetic studies of pantherine cats (Felidae) based on multiple genes, with novel application of nuclear beta-fibrinogen intron 7 to carnivores. Mol. Phylogenet. Evol. 35, 483–495.

    CAS  PubMed  Google Scholar 

  • Zinner, D., Wygoda, C., Razafimanantsoa, L., Rasoloarison, R., Andrianandrasana, H.T., Ganzhorn,J.U., Torkler, F., 2014. Analysis of deforestation patterns in the central Menabe, Madagascar, between 1973 and 2010. Reg. Environ. Change 14, 157–166.

    Google Scholar 

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Veron, G., Dupré, D., Lührs, ML. et al. Genetic polymorphism and structure of wild and zoo populations of the fosa (Eupleridae, Carnivora), the largest living carnivoran of Madagascar. Mamm Biol 92, 68–77 (2018). https://doi.org/10.1016/j.mambio.2018.04.007

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