Molecular Markers for Genetic Diversity Studies of European Hare (Lepus europaeus Pallas, 1778) Populations

Noémi Soós, Szilvia Kusza

Abstract


The purpose of this article is to give an overview of different molecular techniques which have been used in studies concerning population genetic issues of Lepus species and specifically of L. europaeus. The importance of these researches is ever-growing as the European populations of the brown hare have suffered several falloffs as a consequent upon both natural and anthropogenic effects. With developing tools and techniques molecular genetics have become the centrepiece of population genetics and conservation biology. Nucleic acid methods based on both bi- and uniparentally inherited DNA (allozymes, microsatellites, Y chromosome, mtDNA) are often used to study genetic structure, diversity and phylogeography of different species’ populations due to their effectiveness in identifying genetic variability

Keywords


brown hare, diversity studies, genetic methods, molecular markers

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References


Harris H., Enzyme polymorphisms in man, Proceedings of the Royal Society B, 1966, 164, 298–310

Hubby, J.L., Lewontin, R.C., A molecular approach to the study of genic heterozygosity in natural populations I. The number of alleles at different loci in Drosophila pseudoobscura, Genetics, 1966, 54, 577–594

Johnson, F.M., Kanapi, C.G., Richardson, R.H., Wheeler, M.R., Stone, W.S., An analysis of polymorphisms among isozyme loci in dark and light Drosophila ananassae strains from America and Western Samoa, Proceedings of the National Academy of Sciences of the United States of America, 1966, 56, 119–125

Nei, M., Genetic distance between populations. American Naturalist, 1972, 106, 283–292.

Nei, M., Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America, 1973, 70, 3321–3323

Selander, R.K., Johnson, W.E., Genetic variation among vertebrate species, Annual Review of Ecology and Systematics, 1973, 4, 75–91

Parker, P.G., Snow, A.A., Schug, M.D., Booton, G.C., Fuerst, P.A., What molecules can tell us about populations: choosing and using a molecular marker. Ecology, 1998, 79(2), 361–382

Barrett, S.C.H., Kohn, J.R., Genetic and evolutionary consequences of small population size in plants: implications for conservation. In: Genetics and conservation of rare plants, Falk, D.A., Holsinger, K.E. Eds. Oxford University Press, New York, New York, USA, 1991, pp. 3–30

Mashburn, S.J., Sharitz, R.R., Smith, M.H., Genetic variation among Typha populations of the southeastern United States, Evolution, 1978, 32, 681–685

Mitton, J.B., Physiological and demographic variation associated with allozyme variation. In: Isozymes in plant biology, Soltis, D.E., Soltis, P.S. Eds. Dioscorides Press, Portland, Oregon, USA, 1989, pp. 87–105

Watt, W.B., Cassin, R.C., Swan, M.S., Adaptation at specific loci. III. Field behavior and survivorship among Colias PGI genotypes are predictable from in vitro biochemistry, Genetics 1983, 103, 725–739

Bergmann, F., The allelic distribution at an acid phosphatase locus in Norway spruce (Picea abies) along similar climatic gradients, Theoretical and Applied Genetics, 1978, 52, 57–64

Powers, D.A., Ropson, I., Brown, D.C., Van Benedon, R., Cashon, R., Gonzalez-Villansenes, L.I., DiMichele, J.A., Genetic variation in Fundulus heteroclitus: geographic distribution, American Zoologist 1986, 26, 131–144

Hartl, G.B., Markowski, J., Kovacs, G., Grillitsch, M., Willing, R., Biochemical variation and differentiation in the brown hare (Lepus europaeus) of Central Europe. Zeitschrift für Säugetierkunde, 1990, 55, 186–193

Hartl, G.B., Markowski, J., Świątecki, J., Janiszewski, T., Willing, R., Genetic diversity in the Polish brown hare Lepus europaeus Pallas, 1778: implications for conservation and management, Acta Theriologica, 1992, 37, 15 – 25

Hartl, G.B., Suchentrunk, F., Nadlinger, K., Willing, R., An integrative analysis of genetic differentiation in the brown hare Lepus europaeus based on morphology, allozymes, and mitochondrial DNA, Acta Theriologica, 1993, 38(2), 33–57

Hartl, G.B., Nadlinger, K., Willing, R. Allozymes in mammalian population genetics and systematics: Indicative function of a marker system reconsidered, In: Molecular Ecology and Evolution: Approaches and Applications, Schierwater et al. Eds. Birkhäuser Verlag, Basel, Switzerland, 1994, pp. 299–310

Sert, H., Suchentrunk, F., Erdoğan, A., Genetic diversity within Anatolian brown hares (Lepus europaeus Pallas, 1778) and differentiation among Anatolian and European populations, Mammalian Biology, 2005, 70, 171–186

Suchentrunk, F., Michailov, C., Markov, G., Haiden, A., Population genetics of Bulgarian brown hares Lepus europaeus: allozymic diversity at zoogeographical crossroads, Acta Theriologica, 2000, 45(1), 1-12

Suchentrunk, F., Jaschke, C., and Haiden, A., Little allozyme and mtDNA variability in brown hares (Lepus europaeus) from New Zealand and Britain - A legacy of bottlenecks? Mammalian Biology, 2001, 66, 48–59

Suchentrunk, F., Mamuris, Z., Sfougaris, A.I., Stamatis, C., Biochemical genetic variability in brown hares (Lepus europaeus) from Greece, Biochemical Genetics, 2003, 41, 127–140

Suchentrunk, F., Polster, K., Giacometti, M., Ratti, P., Thulin, C.-G., Ruhlé, C., Vasiľev, A.G., Slotta-Bachmayr, L. Spatial partitioning of allozyme variability in European mountain hares (Lepus timidus): gene pool divergence across a disjunct distributional range? Zeitschrift für Säugetierkunde 1999, 64, 1-11

Vapa, M., Selmic, V., Obreht, D., Vapa, L., Allozyme variability in the natural population of hares. Proc. Nat. Sci., Matica Srpska 1999, 97, 85-91

Amos, B., Schlötterer, C., Tautz, D., Social structure of pilot whales revealed by analytical DNA profiling, Science, 1993, 260, 670–672

King, D.G., Morris, Soller, M., Kashi, Y., Evolutionary tuning knobs, Endeavour 1997, 21(l), 36 – 40

Mengoni C. Phylogeny and genetic diversity of Italian species of hares (genus Lepus). PhD Thesis - Università di Bologna, Italy, 2011

Deka, R., Shriver, M. D., Yu, L. M., Conservation of human chromosome 13 polymorphic microsatellite (CA)n repeats in chimpanzees, Genomics 1994, 22, 226–230

Ellegren, H., Polymerase-Chain-Reaction (PCR) analysis of microsatellites - a new approach to studies of genetic relationships in birds, Auk, 1992, 109, 886–895

Primmer, C.R., Møller, A.P., Ellegren, H., A widerange survey of cross-species microsatellite amplification in birds, Molecular Ecology, 1996, 5, 365–378

Ben Slimen, H., Suchentrunk, F., Stamatis, C., Mamuris, Z., Sert, H., Alves, P.C., Kryger, U., Shahin, A.B., Ben Ammar Elgaaied, A., Population genetics of cape and brown hares (Lepus capensis and L. europaeus): A test of Petter's hypothesis of conspecificity, Biochemical Systematics and Ecology 2008, 36, 22-39

Fickel, J., Schmidt, A., Putze, M., Spittler, H., Ludwig, A., Streich, W.J., Pitra C., Genetic structure of populations of European brown hare: Implications for management, Journal of Wildlife Management 2005, 69(2), 760-770

Canu, A., Scandura, M., Luchetti, S., Cossu, A., Iacolina, L., Bazzanti, M., Apollonio, M., Influence of management regime and population history on genetic diversity and population structure of brown hares (Lepus europaeus) in an Italian province, European Journal of Wildlife Research 2013, 59, 783–793

Thulin, C.-G., Malmsten, J., Laurila, A., Differences in body mass, health status and genetic variation between insular and mainland brown hares (Lepus europaeus) in Sweden, European Journal of Wildlife Research 2012, 58, 897 – 907

Antoniou, A., Magoulas, A., Platis, P., Kotoulas, G., Assessing the genetic landscape of a contact zone: the case of European hare in northeastern Greece, Genetica, 2013, 141, 23–40

Thulin, C.-G., Fang, M., Averianov, A. O., Introgression from Lepus europaeus to L. timidus in Russia revealed by mitochondrial single nucleotide polymorphisms and nuclear microsatellites, Hereditas, 2006, 143, 68-76

Gissi, C., Iannelli, F., Pesole, G., Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species, Heredity, 2008, 101, 301-320

Galtier, N., Nabholz, B., Glémin, S., Hurst, G. D. D., Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 2009, 18, 4541–4550

Hurst, G.D.D., Jiggins, F.M., Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts, Proceedings of the Royal Society B, 2005, 272, 1525–1534

Jansen, T., Forster, P., Levine, M.A., Oelke, H., Hurles, M., Renfrew, C., Weber, J., Olek, K., Mitochondrial DNA and the origins of the domestic horse, Proceedings of the National Academy of Sciences of the United States of America 2002, 99, 10905–10910

Kasapidis, P., Suchentrunk, F., Magoulas, A., Kotoulas, G., The shaping of mitochondrial DNA phylogeographic patterns of the brown hare (Lepus europaeus) under the combined influence of Late Pleistocene climatic fluctuations and anthropogenic translocations, Molecular Phylogenetics and Evolution, 2005, 34, 55–66

Stamatis, C., Suchentrunk, F., Moutou, K. A., Giacometti, M., Haerer, G., Djan, M., Vapa, L., Vukovic, M., Tvrtković, N., Sert, H., Alves, P. C., Mamuris, Z., Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south-eastern Mediterranean refugia? Journal of Biogeography 2009, 36, 515–528

Alves, P.C., Ferrand, N., Suchentrunk, F., Harris, D.J., Ancient introgression of Lepus timidus mtDNA into L. granatensis and L. europaeus in the Iberian Peninsula, Molecular Phylogenetics and Evolution 2003, 27, 70–80

Breton, S., Beaupré, H.D., Stewart, D.T., Hoeh, W.R., Blier, P.U., The unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough? Trends in Genetics 2007, 23, 465–474

Pereira, F., Carneiro, J., van Asch, B., A Guide for Mitochondrial DNA Analysis in Non-Human Forensic Investigations, The Open Forensic Science Journal 2010, 3, 33-44

Sato, M. and Sato, K.: Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos, Science, 2011, 334(6059), 1141-1144

Al Rawi S., Louvet-Vallée, S., Djeddi, A., Sachse, M., Culetto, E., Hajjar, C., Boyd, L., Legouis, R., Galy, V., Postfertilization Autophagy of Sperm Organelles Prevents Paternal Mitochondrial DNA Transmission, Science, 2011, 334, 1144-1147

Djan, M., Obreht, D., Vapa, L., Polymorphism of mtDNA regions in brown hare (Lepus europaeus) populations from Vojvodina (Serbia and Montenegro), European Journal of Wildlife Research 2006, 52, 288–291

Mamuris, Z., Moutou, K.A., Stamatis, C., Sarafidou, Th., Suchentrunk F., Y DNA and mitochondrial lineages in European and Asian populations of the brown hare (Lepus europaeus), Mammalian Biology 2010, 75, 233–242

Flux, J.E.C., Angermann, R., The Hares and Jackrabbits. In: Rabbits, Hares and Pikas: Status Survey and Conservation Action Plan, Chapman, J.A., Flux, J.E.C. Eds. The World Conservation Union, Gland, Switzerland, 1990, pp. 61-94.

Koutsogiannouli, E. A., Moutou, K. A., Stamatis, C., Mamuris, Z., Analysis of MC1R genetic variation in Lepus species in Mediterranean refugia, Mammalian Biology, 2012, 77(6), 428–433.

Moore, W. S., Inferring phylogenies from mtDNA variation: mitochondrial – gene trees versus nuclear-gene trees, Evolution, 1995, 49(4), 718-726

Hulbert, I.A.R., Iason, G.R., Elston, D.A., Racey, P.A., Homerange sizes in a stratified upland landscape of two lagomorphs with different feeding strategies. Journal of Applied Ecology 1996, 33, 1479–1488

Reitz, F., Léonard, Y., Characteristics of European hare Lepus europaeus use of space in a French agricultural region of intensive farming, Acta Theriologica, 1994, 39(2), 143-157

Mamuris, Z., Sfougaris, A.I., Stamatis, C., Genetic structure of Greek brown hare (Lepus europaeus) populations as revealed by mtDBNA RFLP-PCR analysis: Implications for conserving genetic diversity, Biological Conservation 2001, 101(2), 187-196

Thulin, C.-G., Jaarola, M., Tegelström, H., The occurrence of mountain hare mitochondrial DNA in wild brown hares, Molecular Ecology, 1997, 6, 463–467

Pierpaoli, M., Riga, F., Trocchi, V., Randi, E., Species distinction and evolutionary relationships of the Italian hare (Lepus corsicanus) as described by mitochondrial DNA sequencing, Molecular Ecology 1999, 8, 1805–1817

Pérez-Suárez, G., Palacios, F., Boursot, P., Speciation and paraphyly in western Mediterranean Hares (Lepus castroviejoi, L. europaeus, L. granatensis and L. capensis) revealed by mitochondrial DNA phylogeny, Biochemical Genetics, 1994, 32, 423-436

Morin, P. A., Luikart, G., Wayne, R. K. et al., SNPs in ecology, evolution and conservation, Trends in Ecology & Evolution 2004, 19, 208-216

Brumfield, R.T., Beerli, P., Nickerson, D.A., Edwards, S.V., The utility of single nucleotide polymorphisms in inferences of population history, TRENDS in Ecology and Evolution 2003, 18(5), 249-256

Pitra, C., Lieckfeldt, D., Alonso, J.C., Population subdivision in Europe’s great bustard inferred from mitochondrial and nuclear DNA sequence variation, Molecular Ecology, 2000, 9, 1165–1170

Lindgren, G., Backstrom, N., Swinburne, J., Hellborg, L., Einarsson, A., Sandberg, K., Cathran, G., Vila, C., Binns, M., Ellegren, H., Limited number of patrilines in horse domestication, Nature Genetics 2004, 36, 335–336

Putze, M., Nürnberg, S., Fickel, J., Y-chromosomal markers for the European brown hare (Lepus europaeus, Pallas 1778). European Journal of Wildlife Research 2007, 53, 257 – 264

Fickel, J.: Molekularbiologie und Phylogenie von Lepus europaeus Pallas, 1778 - und anderen europäischen Lepus-Arten (in German). In: Handbuch der Säugetiere Band 3/II: hasentiere Lagomorpha, Krapp, F., Ed. Aula-Verlag Wiebelsheim, Germany, 2003, pp. 27–34

Fickel, J., Lieckfeldt, D., Pitra, C., Analysis of genetic diversity and structure in neighbouring populations of the European brown hare (Lepus europaeus, Pallas 1778), Zeitschrift Für Jagdwissenschaft 1999, 45, 230–237

Burton, C., Krebs, C.J., Taylor, E.B., Population genetic structure of the cyclic snowshoe hare (Lepus americanus) in southwestern Yukon, Canada, Molecular Ecology, 2002, 11, 1689–1701

Fickel, J., Hohmann, U., A methodological approach for noninvasive sampling for population size estimates in wild boars (Sus scrofa), European Journal of Wildlife Research, 2006, 52, 28–33

Lünser, K., Fickel, J., Lehnen, A., Speck, S., Ludwig, A., Low level of genetic variability in European bisons (Bison bonasus) from the Bialowieza National Park in Poland, European Journal of Wildlife Research 2005, 51, 84 – 87

Li, Y-C., Korl, A.B., Fahima, T., Beiles, A., Nevo, E., Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Molecular Ecology, 2002, 11, 2452–2465

Valdes, A.M., Slatkin, M., Freimer, N.B., Allele frequencies at microsatellite loci: the stepwise mutation model revisited, Genetics 1993, 133, 737–749

Schaffner, S.F., The X chromosome in population genetics. Nature Reviews Genetics, 2004, 5, 43–51.

Cavalli-Sforza, L.L., Feldman, M.W., The application of molecular genetic approaches to the study of human evolution, Nature Genetics, 2003, 33, 266–275

Rozen, S., Skaletsky, H., Marszalek, J.D., Minx, P.J., Cordum, H.S., Waterson, R.H., Wilson, R.K., Page, D.C., Abundant gene conversion between arms of palindromes inhuman and ape Y chromosomes, Nature 2003, 423, 873–876

Graves, J.A.M., The degenerate Y chromosome – can conversion save it?, Reproduction Fertility and Development, 2004, 16, 527–534

Bachtrog D. 2008: The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179, 1513–1525.

Charlesworth, B., Charlesworth, D., The degeneration of Y chromosomes, Philosophical Transactions of the Royal Society B, 2000, 355, 1563–1572

Knower, K.C., Kelly, S., Harley, V.R., Turning on the male – SRY, Sox9 and sex determination in mammals, Cytogenetic and Genome Research, 2003, 101, 185–198

Palsbøll, P.J., Vader, A., Bakke, I., El-Gewely, M.R., Determination of gender in cetaceans by the polymerase chain reaction, Canadian Journal of Zoology 1992, 70, 2166–2170

Graves, J.A.M., Sex chromosomes and sex determination in weird mammals, Cytogenetic and Genome Research 2002, 96, 161–168

Mardon, G., Page, D.C., The sex-determining region of the mouse Y chromosome encodes a protein with a highly acidic domain and 13 zinc fingers, Cell 1989, 56, 765–770

Mitchell, R.J., Kreskas, M., Baxter, E., Buffalino, L., Van Oorschot, R.A., An investigation of sequence deletions of amelogenin (AMELY), a Y-chromosome locus commonly used for gender determination, Annals of Human Biology, 2006, 33, 227–240

Kayser, M., Sajantila, A., Mutations at Y-STR loci: implications for paternity testing and forensic analysis, Forensic Science International, 2001, 118, 116–121.

Miyata, T., Hayashida, H., Kuma, K., Yasunaga, T., Male-driven molecular evolution demonstrated by different rates of silent substitutions between autosome- and sex chromosome-linked genes, Proceedings of the Japan Academy, 1987, 63, 327–331

Wyckoff, G. J., Wang, W., Wu, C. I., Rapid evolution of male reproductive genes in the descent of man, Nature, 2000, 403, 304–309

Shen, P., Wang, F., Underhill, P.A., Franco, C., Yang, W-H., Roxas, A., Sung, R., Lin, A.A., Hyman, R.W., Vollrath, D., Davis, R.W., Cavalli-Sforza, L.L., Oefner, P.J., Population genetic implications from sequence variation in four Y chromosome genes, Proceedings of the National Academy of Sciences of the United States of America 2000, 97, 7354–7359

Stumpf, M.P., Goldstein, D.B., Genealogical and evolutionary inference with the human Y chromosome, Science, 2001, 291(5509), 1738–1742

Thomson, R., Pritchard, J.K., Shen, P., Oefner, P.J., Feldman, M.W., Recent common ancestry of human Y chromosomes: evidence from DNA sequence data, Proceedings of the National Academy of Sciences of the United States of America, 2000, 97, 7360– 7365

Tosi, A.J., Morales, J.C., Melnick, D.J., Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history, Molecular Phylogenetics and Evolution 2000, 17, 190–192

Hughes, J.F., Skaletsky, H., Pyntikova, T., Minx, P.J., Graves, T., Rozen, S., Wilson, R.K., Page, D.C., Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee, Nature, 2005, 437, 101–104

Hughes, J.F., Skaletsky, H., Pyntikova, T., Graves, T.A., van Daalen, S.K.M., Minx, P.J., Fulton, R.S., McGrath, S.D., Locke, D.P., Friedman, C., Trask, B.J., Mardis, E.R., Warren, W.C., Repping, S., Rozen, S., Wilson, R.K., Page, D.C., Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content, Nature, 2010, 463, 536-9

Wallner, B., Huber, S., Achmann, R., Non-invasive PCR sexing of rabbits (Oryctolagus cuniculus) and hares (Lepus europaeus), Mammalian Biology, 2001, 66, 190–192

Geraldes, A., Rogel-Gaillard, C., Ferrand N., High levels of nucleotide diversity in the European rabbit (Oryctolagus cuniculus) SRY gene. Animal Genetics, 2005, 36, 349–351

Geraldes, A., Carneiro, M., Delibes-Mateos, M., Villafuerte, R., Nachman, M. W., Ferrand, N., Reduced introgression of the Y chromosome between subspecies of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula, Molecular Ecology, 2008, 17, 4489–4499


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