Extremely low genetic variation in endangered Tatra chamois and evidence for hybridization with an introduced Alpine population
- 398 Downloads
- 2 Citations
Abstract
The Tatra chamois (Rupicapra rupicapra tatrica) is an endangered endemic subspecies living exclusively in the Tatra Mountains (Slovakia and southern Poland). In order to protect this evolutionary significant unit, a back-up population was established in the nearby Low Tatra Mts. in the 1970s. Before the subspecific status of Tatra chamois had been recognised, however, non-native Alpine chamois (R. r. rupicapra) were introduced to two adjacent mountain ranges. In order to assess their present conservation status, therefore, we undertook a thorough genetic analysis of all Slovak chamois populations (n = 363; 20 microsatellites, SRY gene, MHC class II DRB gene and mtDNA). We found low genetic variation and a high level of inbreeding in all populations, the least variable being the native Tatra chamois population (only one MHC allele), which we ascribe primarily to population bottlenecks. Introduced Alpine chamois showed greater variation, despite originating from few founders. One population, however, founded by just six individuals, also showed highest inbreeding. Male-biased introgressive hybridization between the back-up Low Tatra population and both introduced Alpine populations was detected using several approaches, with up to 19 % of the genome introgressed from Alpine chamois. Such hybridization can be viewed ambiguously as regards conservation in that, though it disrupts the integrity of the unique Tatra chamois genome in the back-up population it also improves its very low genetic variation and decreases inbreeding level, with no obvious signs of outbreeding depression.
Keywords
Rupicapra rupicapra tatrica Ungulate Non-invasive genetic sampling Bottleneck Inbreeding Hybrid detectionNotes
Acknowledgments
We appreciate the help of our co-workers, including Peter Bačkor, Milan Ballo, Mária Boďová, Miroslav Brezovský, Barbara Chovancová, Jozef Kormančík, Juraj Ksiažek, Miroslav Lehocký, Vladimír Mucha, Stanislav Ondruš and Ľudovít Remeník, who provided tissue samples, collected faecal samples or provided information on Slovak chamois populations; and Andrea Hájková, Pavla Křížová, Hana Konvičková, Radka Poláková and Jan Zima jr., who helped with laboratory analysis. We also thank Jozef Kormančík for preparation of the distribution figure; Stuart J. E. Baird, Bruce Rannala, Tomaž Skrbinšek and Martin Straka for useful methodological suggestions and help with computational procedures. We further thank two anonymous reviewers for valuable comments on an earlier draft of the manuscript and Kevin Roche and Jan Roleček for linguistic improvements. Bioinformatics analysis was conducted at the computation cluster at the Institute of Vertebrate Biology of the Czech Academy of Sciences in Brno. This research was financially supported through Grant no. IAA600930609 of the Grant Agency of the Czech Academy of Sciences and through institutional support RVO: 68081766.
Supplementary material
References
- 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 CrossRefGoogle Scholar
- Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229PubMedCentralPubMedGoogle Scholar
- Anonymous (ed) (1981) Current state and prospects of introduced chamois populations in Slovakia. Dom Techniky ČSVTS, Banská Bystrica. (in Slovak)Google Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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
- 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 CrossRefPubMedGoogle Scholar
- Bačkor P (2008) Migrations of chamois (Rupicapra rupicapra Linnaeus 1758) in Slovakia. Nat Carp XLIX:195-204. (in Slovak with English summary)Google Scholar
- 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)Google Scholar
- Bačkor P, Velič E (2008) Restitution Tatra chamois (Rupicapra rupicapra tatrica Blahout 1971) to the Nízke Tatry Mts (Central Slovakia). Nat Conserv 65:17–25Google Scholar
- Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
- 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, MontpellierGoogle Scholar
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
- 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)Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Chovancová B (2008) Tatra chamois (Rupicapra rupicapra tatrica Blahout 1972)—research and protection. In Koreň M (ed) Sixty years of the Tatra National Park: materials to the conference on the 60th anniversary of the Tatra National Park declaration. Štrbské Pleso, 18–19 December 2008, pp. 105–126. (in Slovak)Google Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (N e) from genetic data. Mol Ecol Resour 14:209–214. doi: 10.1111/1755-0998.12157 CrossRefPubMedGoogle Scholar
- Douzery E, Randi E (1997) The mitochondrial control region of Cervidae: evolutionary patterns and phylogenetic content. Mol Biol Evol 14:1154–1166CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedCentralPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140. doi: 10.1016/j.biocon.2005.05.002 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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
- 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 CrossRefGoogle Scholar
- 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/)
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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)Google Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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)Google Scholar
- Jurdíková N (2000) The decline of the Tatra chamois. Caprinae Newsletter of the IUCN/SSC Caprinae Specialist Group, December 2000:4–6Google Scholar
- Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. doi: 10.1016/S0169-5347(02)02489-8 CrossRefGoogle Scholar
- 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)Google Scholar
- 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)Google Scholar
- Loison A, Jullien J-M, Menaut P (1999) Subpopulation structure and dispersal in two populations of chamois. J Mammal 80:620–632CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Martínková N, Zemanová B, Kranz A, Giménez MD, Hájková P (2012) Chamois introductions to Central Europe and New Zealand. Folia Zool 61:239–245Google Scholar
- Milligan BG (2003) Maximum-likelihood estimation of relatedness. Genetics 163:1153–1167PubMedCentralPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc B 64:479–498. doi: 10.1111/1467-9868.00346 CrossRefGoogle Scholar
- 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 CrossRefPubMedCentralPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res (Camb) 89:135–153. doi: 10.1017/S0016672307008798 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary N 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 CrossRefGoogle Scholar
- 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
- Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
- Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedCentralPubMedGoogle Scholar
- 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 Google Scholar
- 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 60:70–80Google Scholar
- 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