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MHC Variability of a Small Lemur in the Littoral Forest Fragments of Southeastern Madagascar

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Abstract

Habitat fragmentation inhibits gene flow between populations often resulting in a loss of genetic diversity with possible negative effects on fitness parameters. In vertebrates, growing evidence suggests that such genetic diversity is particularly important at the level of the major histocompatibility complex (MHC) because its gene products play an important role in immune functions. Diversity in the MHC is assumed to improve population viability. Here, we investigated the impact of forest fragmentation on the genetic variability of one of the functionally important parts of the MHC, DRB exon 2, of the endemic mouse lemur Microcebus murinus by comparing populations inhabiting two littoral forest fragments of different size in southeastern Madagascar. Twelve different alleles of DRB exon 2 were found in 145 individuals of M. murinus with high levels of sequence divergence between alleles. In both subpopulations, levels of genetic diversity were high, and the genetic analyses revealed only limited effects of fragmentation. Significantly more non-synonymous than synonymous substitutions were found in the functionally important antigen recognition and binding sites indicating selection processes maintaining MHC polymorphism. This is the first study on MHC variation in a free-ranging Malagasy lemur population.

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References

  • Antunes SG, Groot NG, Brok H, Doxiadis G, Menezes AAL, Otting N, Bontrop RE (1998) The common marmoset: A new world primate species with limited MHC class II variability. Proc. Nat. Acad. Sci. USA, 95, 11745–11750.

    PubMed  CAS  Google Scholar 

  • Bergström T, Gyllensten U (1995) Evolution of MHC class II polymorphism: The rise and fall of class II gene function in primates. Immun. Rev., 143, 13–31.

    PubMed  Google Scholar 

  • Bontrop RE, Ottig N, de Groot NG, Doxiadis GGM (1999) Major histocompatibility complex class II polymorphisms in primates. Immun. Rev., 167, 339–350.

    PubMed  CAS  Google Scholar 

  • Brewer BA, Lacy RC, Foster ML, Alaks G (1990) Inbreeding depression in insular and central populations of Peromyscus mice. J. Hered., 81, 257–266.

    PubMed  CAS  Google Scholar 

  • Brown JH, Jardetzky TS, Saper MA, Samraoui B, Bjorkman PJ, Wiley DC (1988) A hypothetical model of foreign antigen binding site of class II histocompatibility molecules. Nature, 332, 845–850.

    Article  CAS  PubMed  Google Scholar 

  • Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature, 364, 33–39.

    Article  CAS  PubMed  Google Scholar 

  • Edwards SV, Potts WK (1996) Polymorphism of genes in the major histocompatibility complex (MHC): Implications for conservation genetics. In: Molecular Genetic Approaches in Conservation (eds. Smith TB, Wayne RK), pp. 214–237. Oxford University Press, New York.

    Google Scholar 

  • FTM (1957 reprinted 1990). Carte de Madagascar. 1: 100.000: Feuille 62. Tolagnaro. Foiben-Taosarintanin’i Madagascar, Antananarivo.

    Google Scholar 

  • Gade DW (1996) Deforestation and its effects in highland Madagascar. Mountain Res. Develop., 16, 101–116.

    Google Scholar 

  • Ganzhorn JU, Lowry II PP, Schatz GE, Sommer S (2001) The biodiversity of Madagaskar: One of the world’s hottest hotspots on its way out. Oryx, 35, 1–3.

    Google Scholar 

  • Ganzhorn JU, Schmid J (1998) Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. Int. J. Primatol., 19, 785–796.

    Google Scholar 

  • Garbutt N (1999) Mammals of Madagascar. Pica Press, East Sussex.

    Google Scholar 

  • Go Y, Satta Y, Kawamoto Y, Rakotoarisoa G, Randrianjafy A, Koyama N, Hirai H (2002) MHC-DRB genes evolution in lemurs. Immunogenetics, 54, 403–417.

    PubMed  CAS  Google Scholar 

  • Green GM, Sussman RW (1990) Deforestation history of the eastern rainforest of Madagascar from satellite images. Science, 248, 212–215.

    PubMed  Google Scholar 

  • Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics, 48, 361–372.

    CAS  PubMed  Google Scholar 

  • Gyllensten U, Bergström T, Josefsson A, Sundvall M, Savage A, Blumer ES, Giraldo LH, Soto LH, Watkins DI (1994) The cotton-top tamarin revisited: MHC class I polymorphism of wild tamarins, and polymorphism and allelic diversity of the class II DQA1, DQB1, and DRB loci. Immunogenetics, 40, 167–176.

    PubMed  CAS  Google Scholar 

  • Hartl DL, Clark AG (1989) Principles of population genetics. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts.

    Google Scholar 

  • Hedrick PW (1994) Evolutionary genetics at the major histocompatibility complex. Am. Nat., 143, 945–964.

    Google Scholar 

  • Hedrick PW, Lee RN, Parker KM (2000) Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids. Heredity, 85, 617–624.

    PubMed  CAS  Google Scholar 

  • Hedrick PW, Kim TJ, Parker KM (2001a) Parasite resistance and genetic variation in the endangered Gila topminnow. Anim. Conserv., 4, 103–109.

    Google Scholar 

  • Hedrick PW, Parker KM, Lee RN (2001b) Using microsatellite and MHC variation to identify species, ESUs, and MUs in the endangered Sonoran topminnow. Mol. Ecol., 10, 1399–1412.

    PubMed  CAS  Google Scholar 

  • Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocombatibility complex class I loci reveals over-dominant selection. Nature, 335, 167–170.

    Article  CAS  PubMed  Google Scholar 

  • Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: Evidence for over-dominant selection. Proc. Nat. Acad. Sci. USA, 86, 948–962.

    Google Scholar 

  • Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Ann. Rev. Genet., 32, 415–434.

    PubMed  CAS  Google Scholar 

  • Jordan WC, Bruford MW (1998) New perspectives on mate choice and the MHC. Heredity, 81, 127–133.

    PubMed  CAS  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Mammalian Protein Metabolism (ed. Munro HN), pp. 21–132. Academic Press, New York.

    Google Scholar 

  • Kumar S, Tamura K, Jakobson IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software, Arizona State University, Tempe Arizona, USA.

    Google Scholar 

  • Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J. Mamm., 78, 320–335.

    Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science, 241, 1455–1460.

    PubMed  CAS  Google Scholar 

  • Lahann, P (2001) Verhaltensflexibilität von Microcebus murinus in Trocken-und Regenwäldern Madagaskars. Diploma thesis, Universität Hamburg, Germany.

    Google Scholar 

  • Langefors A, Lohm J, Grahn M, Andersen O, von Schantz T (2001) Association between major histocombatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc. Roy. Soc. Lond. B, 268, 479–485.

    CAS  Google Scholar 

  • Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.

    Google Scholar 

  • Mc Carthy C (1998) CHROMAS. Version 1.45. Griffith University, Southport, Queensland, Australia.

    Google Scholar 

  • MIR Télédétection Inc (1998) Etude sur la déforestation dans la région de Fort-Dauphin, Madagascar. Rapport final soumis à QIT Madagascar Minerals, Montreal.

  • Miththapala S, Seidensticker J, O’Brien SJ (1996) Phylogeographic subspecies recognition in leopards (Panthera pardus): Molecular genetic variation. Conserv. Biol., 10, 1115–1132.

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Ken J (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.

    Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the number of synonymous and nonsynonymous nucleotid substitutions. Mol. Biol. Evol., 3, 418–426.

    PubMed  CAS  Google Scholar 

  • Nelson R, Horning N (1993) AVHRR-LAC estimates of forest area in Madagascar, 1990. Intern. J. Rem. Sens., 14, 1463–1475.

    Google Scholar 

  • Nicholas KB, Nicholas HB (2000) GeneDoc: A Tool for Editing and Annotating multiple Sequence Alignment. Version 2.6. Pittsburgh.

  • Nino-Vasquez JJ, Vogel D, Rodriguez R, Moreno A, Patarroyo ME, Pluschke G, Daubenberger CA (2000) Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for human malaria parasites. Immunogenetics, 51, 219–230.

    Article  PubMed  CAS  Google Scholar 

  • Packer C, Pusey AE, Rowley H, Gilbert DA, Martenson J, O’Brien SJ (1991) Case study of a population bottleneck: Lions of the Ngorongoro Crater. Conserv. Biol., 5, 219–230.

    Google Scholar 

  • Paterson S, Wilson K, Pemberton JM (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Evolution, 95, 3714–3719.

    CAS  Google Scholar 

  • Potts WK, Wakeland EK (1993) Evolution of MHC genetic diversity: A tale of incest, pestilence and sexual preference. Trends Genet., 9, 408–412.

    PubMed  CAS  Google Scholar 

  • Potts WK, Manning CJ, Wakeland EK (1994) The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: An experimental test. Phil. Trans. Roy. Soc. Lond. B, 346, 369–378.

    CAS  Google Scholar 

  • Radespiel U, Sarikaya Z, Zimmermann E, Bruford MW (2001) Sociogenetic structure in a free-living nocturnal primate population: Sex-specific differences in the grey mouse lemur (Microcebus murinus). Behav. Ecol. Sociobiol., 50, 493–502.

    Google Scholar 

  • Ramanamanjato J-B, Ganzhorn JU (2001) Effects of forest fragmentation, introduced Rattus rattus and the role of exotic tree plantations and secondary vegetation for the conservation of an endemic rodent and a small lemur in littoral forests of southeastern Madagascar. Anim. Conserv., 4, 175–183.

    Google Scholar 

  • Ratsirarson J, Goodman SM (1998) Inventaire biologique de la foret littorale de Tampolo (Fenoarivo Atsinanana). Série Sciences Biologiques, Vol. 14. Centre d’Information et de Documentation Scientifique et Technique. Antananarivo, Madagascar.

    Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution, 49, 1280–1283.

    Google Scholar 

  • Rosal-Sánchez M, Paz-Artal E, Moreno-Pelayo MA, Martinez-Quiles N, Martinez-Laso J, Martin-Villa JM, Arnaiz-Villena A (1998) Polymorphism of MHC-DRB allels in Cercophithecus aethiops (green monkey): Generation and functionality. Tissue Antigens, 51, 541–548.

    Article  PubMed  Google Scholar 

  • Schatz GE (2000) Endemism in the Malagasy tree flora. In: Biogeography of Madagascar (eds. Lourenço W, Goodman SM), pp. 1–9. Mémoires de la Société de Biogéographie, Paris.

    Google Scholar 

  • Schatz GE, Birkinshaw C, Lowry II PP, Randriantfika F, Ratovoson F (2000) The endemic plant families of Madagascar project: Integrating taxonomy and conservation. In: Biogeography of Madagaskar (eds. Lourenço WR, Goodman SM), pp. 11–24. Mémoires de la Société de Biogéographie, Paris.

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN. A software for Population Genetics Data Analysis. Version 2000, Geneva, Switzerland.

  • Seddon JM, Baverstock PR (1998) Eight rat RT1.Ba sequences. Immunogenetics, 48, 161–162.

    PubMed  CAS  Google Scholar 

  • Seddon JM, Baverstock PR (1999) Variation on islands: Major histocombatibility complex (MHC) polymorphism in population of the Australian bush rat. Mol. Ecol., 8, 2071–2079.

    PubMed  CAS  Google Scholar 

  • Sommer S, Schwab D, Ganzhorn JU (2002) MHC diversity of endemic Malagasy rodents in relation to range contraction and social system. Behav. Ecol. Sociobiol., 51, 214–221.

    Google Scholar 

  • Sommer S (2003) Effects of habitat fragmentation and changes of dispersal behaviour after a recent population decline on the genetic variability of non-coding and coding DNA of an monogamous Malagasy rodent. Mol. Ecol. (in press).

  • Van den Bussche RA, Ross TG, Hoofer SR (2002) Genetic variation at a major histocompatibility locus within and among populations of white-tailed deer (Odocoileus virginianus). J. Mamm., 83, 31–39.

    Google Scholar 

  • Wimmer B, Tautz D, Kappeler PM (2002) The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav. Ecol. Sociobiol., 52, 166–175.

    Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution, 19, 395–420.

    Google Scholar 

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Schad, J., Sommer, S. & Ganzhorn, J. MHC Variability of a Small Lemur in the Littoral Forest Fragments of Southeastern Madagascar. Conserv Genet 5, 299–309 (2004). https://doi.org/10.1023/B:COGE.0000031137.50239.d3

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