A hybrid dilemma: a molecular investigation of South African bontebok (Damaliscus pygargus pygargus) and blesbok (Damaliscus pygargus phillipsi)

Springer Science and Business Media LLC - Tập 14 - Trang 589-599 - 2013
Anna M. van Wyk1, Antoinette Kotzé1,2, Ettore Randi3, Desiré L. Dalton1,2
1National Zoological Gardens of South Africa, Pretoria, South Africa
2Genetics Department, University of the Free State, Bloemfontein, South Africa
3Laboratorio di Genetica, Istituto Superiore per la Ricerca e Protezione Ambientale (ISPRA), Ozzano Emilia BO, Italy

Tóm tắt

Human-mediated hybridization poses a serious threat to the genetic integrity of threatened inter-fertile species or subspecies, such as the bontebok (Damaliscus pygargus pygargus) and blesbok (Damaliscus pygargus phillipsi) in South Africa. The identification of pure and admixed populations is key to sound biodiversity conservation management and practices. Where identification based on morphometric measurements are complex, molecular analysis can provide a tool to identify hybrids or introgression in populations. This study provides the first molecular analyses on pure bontebok and blesbok as well as putative hybrid populations and samples of unknown purity. Analysis of a panel of 13 microsatellite markers by applying a Bayesian model-based clustering programme provided evidence of clear partitioning between the two subspecies. Hybridization was detected in 33 % (40 of 121) of the samples with unknown purity. Currently, bontebok is listed as protected under the Convention on International Trade in Endangered Species of Wild Fauna and Flora and is listed as endangered under the United States of America’s Endangered Species Act. Our research found that the microsatellite markers used in this study could accurately identify pure and hybrid animals and can be used as a tool to conserve the genetic integrity of both subspecies.

Tài liệu tham khảo

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 Arnold ML, Bulger MR, Burke JM, Hampel AL, Williams JH (1999) Natural hybridisation: how low can you go and still be important. Ecology 80:371–381. doi:10.1890/0012-9658 Avise JC (2004) Molecular markers, natural history and evolution, 2nd edn. Chapman & Hall, New York Barilani M, Bernard-Laurent A, Mucci N, Tabarroni C, Kark S, Garrido JAP, Randi E (2007) Hybridisation with introduced chukars (Alectoris chukar) threatens the gene pool integrity of native rock (A. graeca) and red-legged (A. rufa) partridge populations. Biol Conserv 137:57–69. doi:10.1016/j.biocon.2007.01.014 Barnard PJ, van der Walt K (1961) Translocation of the bontebok (Damaliscus pygargus) from Bredasdorp to Swellendam. Koedoe 4:105–109 Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148. doi:10.1146/annurev.es.16.110185.000553 Bigalke R (1955) The bontebok Damaliscus pygargus with a special reference to its history and preservation. Fauna and Flora 6:95–116 Bishop MD, Kappes SM, Keele JW, Stone RT, Sunden SLF, Hawkins GA, Toldo SS, Fries R, Grosz MD, Yoo J, Beattie CW (1994) A genetic linkage map for cattle. Genetics 136:619–639 Broders HG, Mahoney SP, Montevecchi WA, Davidson WS (1999) Population genetic structure and the effect of founder events on the genetic variability of moose, Alces alces, in Canada. Mol Ecol 8:1309–1315. doi:10.1046/j.1365-294X.1999.00695.x Cordingley JE, Sundaresan SR, Fischhoff IR, Shapiro B, Ruskey J, Rubenstein DI (2009) Is the endangered grevy’s zebra threatened by hybridization? Anim Conserv 12:505–513. doi:10.1111/j.1469-1795.2009.00294.x Dalton DL, van Wyk AM, Kotzé A (2011) Isolation and characterization of species-specific microsatellite loci in the blesbok. Conservation Genet Resour 3:677–679. doi:10.1007/s12686-011-9431-6 Deyoung RW, Honeycutt RL (2005) The molecular toolbox: genetic techniques in wildlife ecology and management. J Wildl Manage 69: 1362–1384. doi:10.2193/0022-541X(2005)69[1362:TMTGTI]2.0.CO;2 Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conservation Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7 East R (1999) African Antelope Database 1998. IUCN/SSC Antelope Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK Ede AJ, Pierson CA, Crawford AM (1995) Ovine microsatellites at the OarCP9, OarCP16, OarCP20, OarCP21, OarCP23 and OarCP26 loci. Anim Genet 26:129–130. doi:10.1111/j.1365-2025.1995.tb02655.x Essop MF, Harley EH, Lloyd PH, van Hensbergen HJ (1991) Estimation of the genetic distance between bontebok and blesbok using mitochondrial DNA. S Afr J Sci 87:271–273 Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491 Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50 Fabricius C, Van Hensbergen HJ, Zucchini W (1989) A discriminant function for identifying hybrid bontebok x blesbok populations. S Afr J Wildl Res 19:61–66 Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM (1999) Introgression through rare hybridization: a genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152:355–371 Gottelli D, Sillero-Zubiri C, Applebaum GD, Roy MS, Girman DJ, Garcia-Moreno J, Ostrander EA, Wayne RK (1994) Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Mol Ecol 3:301–312. doi:10.1111/j.1365-294X.1994.tb00070.x Green WCH, Rothstein A (1998) Translocation, hybridization, and the endangered black-faced impala. Conserv Biol 12:475–480. doi:10.1111/j.1523-1739.1998.96424.x Grieg JC (1979) Principles of genetic conservation in relation to wildlife management in Southern Africa. S Afr J Wildl Res 9:57–78 Grobler JP, van der Bank FH (1995) Allozyme divergence among four representatives of the subfamily Alcelaphinae (family: Bovidae). Comp Biochem Physiol B 112:303–308 Grobler JP, Rushworth I, Brink JS, Bloomer P, Kotze A, Reilly B, Vrahimis S (2011) Management of hybridization in an endemic species: decision making in the face of imperfect information in the case of the black wildebeest–Connochaetes gnou. Eur J Wildl Res 57:997–1006. doi:10.1007/s10344-011-0567-1 Hewitt GM (1993) Postglacial distribution and species sub-structure: lessons from pollen, insects and hybrid zones. In: Lees DR, Edwards D (eds) Evolutionary Patterns and Processes. Academic Press, London, pp 97–123 Lancaster ML, Gemmell NJ, Negro S, Goldsworthy S, Sunnucks P (2006) Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Mol Ecol 15:3681–3692. doi:10.1111/j.1365-294X.2006.03041.x Lande R, Barrowclough GF (1987) Effective population size, genetic variation, and their use in population management. In: Soule ME (ed) Viable populations for conservation. Cambridge University Press, Cambridge, pp 87–123 Latch EK, Harveson LA, King JS, Hobson MD, Rhodes OE (2006) Assessing hybridization in wildlife populations using molecular markers: A case study in wild turkeys. J Wildl Manage 70:485–492. doi:10.2193/0022-541X(2006)70[485:AHIWPU]2.0.CO;2 Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16. doi:10.1046/j.1523-1739.1996.10010010.x Lloyd P, David J (2008) Damaliscus pygargus. IUCN Red List of Threatened Species. Version 2011.2. http://www.iucnredlist.org/apps/redlist/details/30208/0. Accessed 28 December 2011 Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RL, Allendorf FW (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5:328–331. doi:10.1098/rsbl.2009.0033 Oliveira R, Godinho R, Randi E, Ferrand N, Alves P (2008) Molecular analysis of hybridisation between wild and domestic cats (Felis silvestris) in Portugal: implications for conservation. Conserv Genet 9:1–11. doi:10.1007/s10592-007-9297-z Park SDE (2001). Trypanotolerance in West African cattle and the population genetic effects of selection. PhD. Dissertation, University of Dublin, Dublin Peakall R, Smouse PE (2006) GNEALEX6: 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 Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959 Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249 Remington C (1968) Suture-zones of hybrid interaction between recently joined biotas. Evol Biol 2:321–428 Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecol Syst 27:83–109 Robinson TJ, Morris DJ, Fairall N (1991) Interspecific hybridization in the Bovidae:sterility of Alcelaphus buselaphus x Damaliscus dorcas F1 Progeny. Biol Conserv 58:345–356. doi:10.1016/0006-3207(91)90100-N Rodriquez D, Cedeno-Vazquez JR, Forstner MRJ, Densmore LD (2008) Hybridization between Crocodylus acutus and Crocodylus moreletii in the Yucatan Peninsula: II. evidence from microsatellites. J Exp Zool A Ecol Genet Physiol 309A:674–686. doi:10.1002/jez.473 Senn HV, Pemberton JM (2009) Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area. Mol Ecol 18:862–876. doi:10.1111/j.1365-294X.2008.04051.x Skead CJ (1980) Historical mammal incidence in the Cape Province 1. Department of Nature and Environmental Conservation South Africa, Cape Town Skinner JD, Smithers RHN (1990) Alcelaphine. The mammals of southern African subregions. University of Pretoria Press, Pretoria Sunden SLF, Stone RT, Bishop MD, Kappes SM, Keele JW, Beattie CW (1993) A highly polymorphic bovine microsatellite locus: BM2113. Anim Genet 24:69. doi:10.1111/j.1365-2052.1993.tb00924.x Toldo SS, Fries R, Steffen P, Neibergs HL, Barendse W, Womack JE, Hetzel DJS, Stranzinger G (1993) Physically mapped, cosmid-derived microsatellite markers as anchor loci on bovine chromosomes. Mamm Genome 4:720–727. doi:10.1007/BF00357796 Trigo TC, Freitas TRO, Kunzler G, Cardoso L, Silva JCR, Johnson WE, O’brien SJ, Bonatto SL, E izirik E (2008) Inter-species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil. Mol Ecol 17:4317–4333. doi:10.1111/j.1365-294X.2008.03919.x Trotter P (2008) Cutthroat: native trout of the West, 2nd edn. In University of California Press, Berkeley, CA Vähä JP, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72. doi:10.1111/j.1365-294X.2005.02773.x Van der Merwe NJ (1986) Die bontebok. Koedoe 11:161–168 Van der Merwe P, Saayman M (2007) Determining the economic value of game farm tourism. Koedoe 46:103–112. doi:10.4102/koedoe.v46i2.59 Van der Walt JM (2002). Detection of genetic substructure and diversity in the endemic South African antelope species, Damaliscus pygargus. PhD. Dissertation, Pretoria, UP Van der Walt JM, Nel LH, Hoelzel AR (2001) Characterization of major histocompatibility complex DRB diversity in the endemic South African antelope Damaliscus pygargus: a comparison in two subspecies with different demographic histories. Mol Ecol 10:1679–1688. doi:10.1046/j.0962-1083.2001.01321.x Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x Vrba ES (1979) Phylogenetic analysis and classification of fossil and recent Alcelaphini Mammalia, Bovidae. Biol J Linn Soc 11:207–228. doi:10.1111/j.1095-8312.1979.tb00035.x Wiseman R, O’ryan C, Harley EH (2000) Microsatellite analysis reveals that domestic cat (Felis catus) and southern African wild cat (F. lybica) are genetically distinct. Anim Conserv 3:221–228. doi:10.1111/j.1469-1795.2000.tb00106.x Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053. doi:10.1046/j.1523-1739.2001.0150041039.x