Extremely low genetic variation in endangered Tatra chamois and evidence for hybridization with an introduced Alpine population

Conservation Genetics

Volumn 16, Issue 3, 2015, Pages 729-741

  Zemanová, Barbora ^a,b   Hájková, Petra ^a,c   Hájek, Bedřich ^d   Martínková, Natália ^a,b   Mikulíček, Peter ^a,e   Zima, Jan ^a   Bryja, Josef ^a,b  

^a INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^b MASARYK UNIVERSITY   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

^d THE NATURE CONSERVANCY   (United States)

^e Faculty of Natural Sciences   (Slovakia)

Author keywords

Bottleneck; Hybrid detection; Inbreeding; Non invasive genetic sampling; Rupicapra rupicapra tatrica; Ungulate

Indexed keywords

EID: 84939960476     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-015-0696-2     Document Type: Article

References (84)

1. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622. doi:10.1016/S0169-5347(01)02290-X
2. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229
3. Anonymous (ed) (1981) Current state and prospects of introduced chamois populations in Slovakia. Dom Techniky ČSVTS, Banská Bystrica. (in Slovak)
4. Arlettaz R, Patthey P, Baltic M, Leu T, Schaub M, Palme R, Jenni-Eiermann S (2007) Spreading free-riding snow sports represent a novel serious threat for wildlife. Proc R Soc B 274:1219–1224. doi:10.1098/rspb.2006.0434
5. Aulagnier S, Giannatos G, Herrero J (2008) Rupicapra rupicapra. The IUCN Red List of Threatened Species. Version 2014.1. http://www.iucnredlist.org/details/39255/0. Accessed 07 July 2014
6. Babik W, Durka W, Radwan J (2005) Sequence diversity of the MHC DRB gene in the Eurasian beaver (Castor fiber). Mol Ecol 14:4249–4257. doi:10.1111/j.1365-294X.2005.02751.x
7. Bačkor P (2008) Migrations of chamois (Rupicapra rupicapra Linnaeus 1758) in Slovakia. Nat Carp XLIX:195-204. (in Slovak with English summary)
8. Bačkor P, Urban P (2009) The Tatra chamois in the National Park Nízke Tatry Mts. Folia Venat 38–39:47–64 (in Slovak with English summary)
9. Bačkor P, Velič E (2008) Restitution Tatra chamois (Rupicapra rupicapra tatrica Blahout 1971) to the Nízke Tatry Mts (Central Slovakia). Nat Conserv 65:17–25
10. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
11. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier
12. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300
13. Blahout M (1972) Zur Taxonomie der Population von Rupicapra rupicapra (Linné, 1785) in der Hohen Tatra. Zoologické listy 21:115–132 (in German with English summary)
14. Bryja J, Galan M, Charbonnel N, Cosson J-F (2005) Analysis of major histocompatibility complex class II gene in water voles using capillary electrophoresis-single stranded conformation polymorphism. Mol Ecol Notes 5:173–176. doi:10.1111/j.1471-8286.2004.00855.x
15. Buzan EV, Bryja J, Zemanová B, Kryštufek B (2013) Population genetics of chamois in the contact zone between the Alps and the Dinaric Mountains: uncovering the role of habitat fragmentation and past management. Conserv Genet 14:401–412. doi:10.1007/s10592-013-0469-8
16. Cavallero S, Marco I, Lavín S, D’Amelio S, López-Olvera JR (2012) Polymorphisms at MHC class II DRB1 exon 2 locus in Pyrenean chamois (Rupicapra pyrenaica pyrenaica). Infect Genet Evol 12:1020–1026. doi:10.1016/j.meegid.2012.02.017
17. th anniversary of the Tatra National Park declaration. Štrbské Pleso, 18–19 December 2008, pp. 105–126. (in Slovak)
18. Čížková D, de Bellocq JG, Baird SJE, Piálek J, Bryja J (2011) Genetic structure and contrasting selection pattern at two major histocompatibility complex genes in wild house mouse populations. Heredity 106:727–740. doi:10.1038/hdy.2010.112
19. Corander J, Marttinen P, Sirén J, Tang J (2008a) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9:539. doi:10.1186/1471-2105-9-539
20. Corander J, Sirén J, Arjas E (2008b) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129. doi:10.1007/s00180-007-0072-x
21. Corlatti L, Lorenzini R, Lovari S (2011) The conservation of the chamois Rupicapra spp. Mamm Rev 41:163–174. doi:10.1111/j.1365-2907.2011.00187.x
22. Crestanello B, Pecchioli E, Vernesi C, Mona S, Martínková N, Janiga M, Hauffe HC, Bertorelle G (2009) The genetic impact of translocations and habitat fragmentation in chamois (Rupicapra) spp. J Hered 100:691–708. doi:10.1093/jhered/esp053
23. e) from genetic data. Mol Ecol Resour 14:209–214. doi:10.1111/1755-0998.12157
24. Douzery E, Randi E (1997) The mitochondrial control region of Cervidae: evolutionary patterns and phylogenetic content. Mol Biol Evol 14:1154–1166
25. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7
26. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
27. Forrest JL, Wikramanayake E, Shrestha R, Areendran G, Gyeltshen K, Maheshwari A, Mazumdar S, Naidoo R, Thapa GJ, Thapa K (2012) Conservation and climate change: assessing the vulnerability of snow leopard habitat to treeline shift in the Himalaya. Biol Conserv 150:129–135. doi:10.1016/j.biocon.2012.03.001
28. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140. doi:10.1016/j.biocon.2005.05.002
29. Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475. doi:10.1111/j.1523-1739.2011.01662.x
30. Garner A, Rachlow JL, Hicks JF (2005) Patterns of genetic diversity and its loss in mammalian populations. Conserv Biol 19:1215–1221. doi:10.1111/j.1523-1739.2005.00105.x
31. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318. doi:10.1046/j.1365-294X.2001.01190.x
32. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm. Updated from Goudet (1995). Accessed 15 July 2014
33. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162. doi:10.1016/S0003-3472(80)80103-5
34. Hájková A (2011) Neutral genetic variation and structure of chamois populations in Slovakia. Diploma thesis, Charles University in Prague. (in Slovak with English summary, available at https://is.cuni.cz/webapps/zzp/detail/51053/)
35. Hansen MM, Olivieri I, Waller DM, Nielsen EE, The GeM Working Group (2012) Monitoring adaptive genetic responses to environmental change. Mol Ecol 21:1311–1329. doi:10.1111/j.1365-294X.2011.05463.x
36. Hedrick PW (2013) Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol 22:4606–4618. doi:10.1111/mec.12415
37. Hurta V (2009) Distribution range and habitat use of Alpine chamois in Veľká Fatra Mts. Diploma thesis, University of Matej Bel, Banská Bystrica. (in Slovak with English summary)
38. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. doi:10.1093/bioinformatics/btm233
39. Janiga M, Zámečníková H (2002) Zoological characteristics of the historical data on chamois (Rupicapra rupicapra tatrica Blahout, 1971) as a base for the evaluation of their current abundance in the Tatra Mountains. In: Janiga M, Švajda J (eds) Chamois Protection. TANAP—Tatranská Štrba, NAPANT—Banská Bystrica, IHAB—Tatranská Javorina, pp. 99–182. (in Slovak with English summary)
40. Jurdíková N (2000) The decline of the Tatra chamois. Caprinae Newsletter of the IUCN/SSC Caprinae Specialist Group, December 2000:4–6
41. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. doi:10.1016/S0169-5347(02)02489-8
42. Koreň M, Radúch J, Chovancová B, Šturcel M, Kováč J, Gašinec I, Ksiažek J, Vančura V, Hummel M, Ondruš S (2001) Action plan for Tatra chamois for years 2001–2005. Tatranská Lomnica. (in Slovak)
43. Kováč J (2002) The history of the care and protection of the Tatra Chamois (Rupicapra rupicapra tatrica Blahout, 1971) in TANAP. In: Janiga M, Švajda S (eds) Chamois Protection. TANAP—Tatranská Štrba, NAPANT—Banská Bystrica, IHAB—Tatranská Javorina, pp. 197–204. (in Slovak with English summary)
44. Loison A, Jullien J-M, Menaut P (1999) Subpopulation structure and dispersal in two populations of chamois. J Mammal 80:620–632
45. Mannen H, Nagata Y, Tsuji S (2001) Mitochondrial DNA reveal that domestic goat (Capra hircus) are genetically affected by two subspecies of bezoar (Capra aegagurus). Biochem Genet 39:145–154. doi:10.1023/A:1010266207735
46. Martínková N, Zemanová B, Kranz A, Giménez MD, Hájková P (2012) Chamois introductions to Central Europe and New Zealand. Folia Zool 61:239–245
47. Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics 163:1153–1167
48. Mona S, Crestanello B, Bankhead-Dronnet S, Pecchioli E, Ingrosso S, D’Amelio S, Rossi L, Meneguz PG, Bertorelle G (2008) Disentangling the effects of recombination, selection, and demography on the genetic variation at a major histocompatibility complex class II gene in the alpine chamois. Mol Ecol 17:4053–4067. doi:10.1111/j.1365-294X.2008.03892.x
49. Morin PA, Chambers KE, Boesch C, Vigilant L (2001) Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10:1835–1844. doi:10.1046/j.0962-1083.2001.01308.x
50. Nielsen EE, Bach LA, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6:971–973. doi:10.1111/j.1471-8286.2006.01433.x
51. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x
52. Pérez T, Albornoz J, Domínguez A (2002) Phylogeography of chamois (Rupicapra spp.) inferred from microsatellites. Mol Phylogenet Evol 25:524–534. doi:10.1016/S1055-7903(02)00296-8
53. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. doi:10.1093/jhered/90.4.502
54. Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544. doi:10.1016/j.biocon.2009.07.026
55. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
56. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109. doi:10.1146/annurev.ecolsys.27.1.83
57. Rodríguez F, Hammer S, Pérez T, Suchentrunk F, Lorenzini R, Michallet J, Martinkova N, Albornoz J, Domínguez A (2009) Cytochrome b phylogeography of chamois (Rupicapra spp.). Population contractions, expansions and hybridizations governed the diversification of the genus. J Hered 100:47–55. doi:10.1093/jhered/esn074
58. Rodríguez F, Pérez T, Hammer SE, Albornoz J, Domínguez A (2010) Integrating phylogeographic patterns of microsatellite and mtDNA divergence to infer the evolutionary history of chamois (genus Rupicapra). BMC Evol Biol 10:222. doi:10.1186/1471-2148-10-222
59. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x
60. Rossi L, Fraquelli C, Vesco U, Permunian R, Sommavilla GM, Carmignola G, Da Pozzo R, Meneguz PG (2007) Descriptive epidemiology of a scabies epidemic in chamois in the Dolomite Alps, Italy. Eur J Wildl Res 53:131–141. doi:10.1007/s10344-006-0067-x
61. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:10.1093/bioinformatics/btg359
62. Schaschl H, Goodman SJ, Suchentrunk F (2004) Sequence analysis of the MHC class II DRB alleles in Alpine chamois (Rupicapra r. rupicapra). Dev Comp Immunol 28:265–277. doi:10.1016/j.dci.2003.08.003
63. Schaschl H, Suchentrunk F, Hammer S, Goodman SJ (2005) Recombination and the origin of sequence diversity in the DRB MHC class II locus in chamois (Rupicapra spp.). Immunogenetics 57:108–115. doi:10.1007/s00251-005-0784-4
64. Schaschl H, Suchentrunk F, Morris DL, Ben Slimen H, Smith S, Arnold W (2012) Sex-specific selection for MHC variability in Alpine chamois. BMC Evol Biol 12:20. doi:10.1186/1471-2148-12-20
65. Seddon JM, Ellegren H (2004) A temporal analysis shows major histocompatibility complex loci in the Scandinavian wolf population are consistent with neutral evolution. Proc R Soc B 271:2283–2291. doi:10.1098/rspb.2004.2869
66. Shafer ABA, Fan CW, Côté SD, Coltman DW (2012) Lack of) genetic diversity in immune genes predates glacial isolation in the North American mountain goat (Oreamnos americanus. J Hered 103:371–379. doi:10.1093/jhered/esr138
67. Sindičić M, Polanc P, Gomerčić T, Jelenčič M, Huber Đ, Trontelj P, Skrbinšek T (2013) Genetic data confirm critical status of the reintroduced Dinaric population of Eurasian lynx. Conserv Genet 14:1009–1018. doi:10.1007/s10592-013-0491-x
68. Skrbinšek T, Jelenčič M, Waits L, Kos I, Jerina K, Trontelj P (2012) Monitoring the effective population size of a brown bear (Ursus arctos) population using new single-sample approaches. Mol Ecol 21:862–875. doi:10.1111/j.1365-294X.2011.05423.x
69. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264. doi:10.1073/pnas.0403809101
70. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B 277:979–988. doi:10.1098/rspb.2009.2084
71. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc B 64:479–498. doi:10.1111/1467-9868.00346
72. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24:3189–3194. doi:10.1093/nar/24.16.3189
73. Valière N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379. doi:10.1046/j.1471-8286.2002.00228.x-i2
74. Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res (Camb) 89:135–153. doi:10.1017/S0016672307008798
75. Wang J (2011) Coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145. doi:10.1111/j.1755-0998.2010.02885.x
76. Wang J (2014) Marker-based estimates of relatedness and inbreeding coefficients: an assessment of current methods. J Evol Biol 27:518–530. doi:10.1111/jeb.12315
77. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184. doi:10.1007/s10592-005-9100-y
78. e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evolut Appl 3:244–262. doi:10.1111/j.1752-4571.2009.00104.x
79. Waples RS, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769-U603. doi: 10.1534/genetics.114.164822
80. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
81. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191
82. Zemanová B, Hájková P, Wandeler P, Bryja J et al. Use of real-time PCR for detection of factors influencing PCR success and genotyping error rates in faecal DNA analysis of a mountain ungulate. In preparation
83. Zemanová B, Hájková P, Bryja J, Zima J Jr, Hájková A, Zima J (2011) Development of multiplex microsatellite sets for noninvasive population genetic study of the endangered Tatra chamois. Folia Zool 60:70–80
84. Zima J, Kožená I, Hubálek Z (1990) Non-metrical variation and divergence between autochthonous and introduced populations of chamois (Rupicapra rupicapra). Folia Zool 39:237–248 http://spravatanap.sk/web/index.php/11-aktualne/282-jesenne-scitanie-kamzikov. Accessed 16 January 2015