Genetic structure and patterns of gene flow among populations of the endangered Ethiopian wolf
Corresponding Author
D. Gottelli
Institute of Zoology, Zoological Society of London, London, UK
Correspondence
Dada Gottelli, Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
Email: [email protected]
Search for more papers by this authorC. Sillero-Zubiri
Wildlife Conservation Research Unit, Zoology Department, University of Oxford, Tubney, UK
Search for more papers by this authorJ. Marino
Wildlife Conservation Research Unit, Zoology Department, University of Oxford, Tubney, UK
Search for more papers by this authorJ. Wang
Institute of Zoology, Zoological Society of London, London, UK
Search for more papers by this authorCorresponding Author
D. Gottelli
Institute of Zoology, Zoological Society of London, London, UK
Correspondence
Dada Gottelli, Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK
Email: [email protected]
Search for more papers by this authorC. Sillero-Zubiri
Wildlife Conservation Research Unit, Zoology Department, University of Oxford, Tubney, UK
Search for more papers by this authorJ. Marino
Wildlife Conservation Research Unit, Zoology Department, University of Oxford, Tubney, UK
Search for more papers by this authorJ. Wang
Institute of Zoology, Zoological Society of London, London, UK
Search for more papers by this authorAbstract
Populations of endangered mammals are often small, fragmented and have low genetic variability that can reduce the ability to evolve in response to environmental changes. The endangered Ethiopian wolf (Canis simensis) is a habitat specialist restricted to six small, isolated pockets of Afroalpine habitat, with a total population of fewer than 500 adult animals. The degradation of the Ethiopian highlands because of human expansion is ever increasing, potentially leading to further population fragmentation and local extinctions. In order to assist Ethiopian wolf conservation management, we quantified the genetic diversity, population structure and patterns of gene flow of the species using up to 14 microsatellite loci. FST, analysis of molecular variance, principal coordinates analysis and Bayesian clustering analyses revealed geographic population structuring delimited by three mountain ranges, in concert with a previous study based on mitochondrial DNA. Bayesian analysis showed that current gene flow is low, unidirectional and limited to geographically proximate populations. Given the small census size and strong population structuring with low gene flow, demographic stochasticity is likely to be the highest threat to the long-term persistence of this species. The protection of the remaining suitable habitat, especially narrow ridges linking habitat patches within mountain blocks, is therefore essential. The genetic survey presented by this study provides vital and much needed information for the future effective management of Ethiopian wolf populations.
Supporting Information
Filename | Description |
---|---|
acv591-sup-0001-si.docx23.7 KB |
Figure S1. Correlation of the posterior probability between two independent MCMC analyses using BayesAss. Analysis settings were 3 million iterations plus 1 million burnin iterations, sample freq 2000 and Delta of 0.15. Only modern samples were included in the analysis. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Allendorf, F.W., Hohenlohe, P.A. & Luikart, G. (2010). Genomics and the future of conservation genetics. Genetics 11, 697–709.
- Anderson, E.C. & Dunham, K.K. (2008). The influence of family groups on inferences made with the program Structure. Mol. Ecol. 8, 1219–1229.
- Ashenafi, Z.T., Coulson, T., Sillero-Zubiri, C. & Leader-Williams, N. (2005). Behaviour and ecology of the Ethiopian wolf (Canis simensis) in a human-dominated landscape outside protected areas. Anim. Conserv. 8, 113–121.
- Aspi, J., Roininen, M., Kiiskila, J., Ruokonen, M., Kojola, I., Bljudnik, L., Danilov, P., Heikkinen, S. & Pulliainen, E. (2009). Genetic structure of the northwestern Russian wolf populations and gene flow between Russia and Finland. Conserv. Genet. 10, 815–826.
- Bruzzi, M.L., Eizirik, E., Garda, A.A., da Fontoura-Rodrigues, M.L., Guimarães Rodrigues, F.H. & Marinho-Filho, J.S. (2011). Conservation genetics of maned wolves in a highly impacted area of the Brazilian Cerrado biome. Genetica 139, 369–381.
- Carmichael, L.E., Nagy, J.A., Larter, N.C. & Strobeck, C. (2001). Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Mol. Ecol. 10, 2787–2798.
- Cockerham, C.C. & Weir, B.S. (1993). Estimation of gene flow from F-statistics. Evolution 47, 855–863.
- Cornuet, J.M. & Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.
- Crandall, K.A., Binida-Edmonds, O.R.P., Mace, G.M. & Wayne, R.K. (2000). Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15, 290–295.
- de Beaux, O. (1922). Mammiferi Abyssini e Somali. Atti della Societ Italiana di Sciencia Naturale da Milano 61, 21–34.
- Di Rienzo, A., Peterson, A.C. & Garza, J.C. (1994) Mutational processes of simple sequence repeat loci in human populations. Proc Natl Acad Sci USA 91, 3166–3170.
- Earl, D.A. & vonHoldt, B.M. (2011). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons. Gen. Resour. 2, 359–361.
- 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.
- Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
- Faubet, P., Waples, R.S. & Gaggiotti, O.E. (2007). Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates. Mol. Ecol. 16, 1149–1166.
- Flagstad, Ø., Walker, C.W., Vila', C., Sundqvist, A.K., Fernholm, B., Hufthammer, A.K., Wiig, Ø., Koyola, I. & Ellegren, H. (2003). Two centuries of the Scandinavian wolf population: patterns of genetic variability and migration during an era of dramatic decline. Mol. Ecol. 12, 869–880.
- Francisco, L.V.V., Langston, A.A., Mellersh, C.S., Neal, C.L. & Ostrander, E.A. (1996). A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm. Genome 7, 359–362.
- Garnier-Gere, P. & Dillmann, C. (1992). A computer program for testing pairwise linkage disequilibria in subdivided populations. J. Hered. 83, 239–250.
- Gottelli, D., Marino, J., Sillero-Zubiri, C. & Funk, S. (2004). The effect of the last glacial age on speciation and population genetic structure of the endangered Ethiopian wolf (Canis simensis). Mol. Ecol. 13, 2275–2286.
- Grabherr, G., Gottfrier, M. & Pauli, H. (2003). High mountain environment as indicator of global change. Adv. Glob. Chan. Res. 9, 331–345.
- Guinand, B., Scribner, K.T., Page, K.S., Filcek, K., Main, L. & Burnham-Curtis, M.K. (2006). Effects of coancestry on accuracy of individual assignments to populations of origin: examples using Great Lakes lake trout (Salvelinus namaycush). Genetica 127, 329–340.
- Haydon, D.T., Randall, D.A., Matthews, D., Tallents, L.A., Gravenor, M., Williams, S., Pollinger, J., Cleaveland, S., Woolhouse, M.E., Sillero-Zubiri, C., Marino, J., Macdonald, D.W. & Laurenson, M. (2006). Low-coverage vaccination strategies for the conservation of endangered species. Nature 443, 692–695.
- Hedrick, P.W. & Fredrickson, R. (2010). Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conservation Genetics 11, 615–626.
- Hudson, R.R., Boos, D.D. & Kaplan, N.L. (1992). A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 9, 138–151.
- IUCN/SSC Canid Specialist Group (2011). Strategic plan for Ethiopian wolf conservation. Oxford: IUCN/SSC Canid Specialist Group.
- Johnson, N., Mansfield, K.L., Marston, D.A., Wilson, C., Goddard, T., Selden, D., Hemson, G., Edea, L., van Kesteren, F., Shiferaw, F., Stewart, A.E., Sillero-Zubiri, C. & Fooks, A.R. (2010). A new outbreak of rabies in rare Ethiopian wolves (Canis simensis). Arch. Virol. 155, 1175–1177.
- Lucchini, V., Galov, A. & Randi, E. (2004). Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol. Ecol. 13, 523–536.
- Madsen, T., Shine, R., Olsson, M. & Wittzell, H. (1999). Restoration of an inbred adder population. Nature 402, 34–35.
- Marino, J. (2003). Critically endangered Ethiopian wolves persist in small isolated Afroalpine enclaves. Oryx 37, 62–71.
- Marino, J., Mitchel, R. & Johnson, P.J. (2010). Dietary specialization and climatic-linked variations in extant populations of Ethiopian wolves. Afri. J. Ecol. 48, 517–525.
- Marino, J., Stewart, A.E., Gordon, C.H., Gottelli, D., Tefera, Z., Laurenson, M.K. & Sillero-Zubiri, C. (2011). Status review of the Ethiopian wolf. Strategic plan for Ethiopian wolf conservation. Oxford: IUCN/SSC Canid Specialist Group.
- Moritz, C. (1995). Defining ‘evolutionary significant units’ for conservation. Trends Ecol. Evol. 9, 373–375.
- Navidi, W., Arnheim, N. & Waterman, M.S. (1992). A multiple-tube approach for accurate genotyping of very small DNA samples by using PCR: statistical considerations. American Journal of Human Statistics 50, 347–359.
- Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.
- Nei, M. & Chesser, R. (1983). Estimation of fixation indices and gene diversities. Ann. Hum. Genet. 47, 253–259.
- Ostrander, E.A., Sprague, G.F. & Rine, J. (1993). Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16, 207–213.
- Peakall, R. & Smouse, P.E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295.
- Piry, S., Luikart, G. & Cornuet, J.-M. (1999). BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90, 502–503.
- Pritchard, J.K., Stephens, M. & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
- Randall, D.A., Pollinger, J.P., Kifle, A., Macdonald, D.W., Wayne, R.K. (2010). Fine scale genetic structure in Ethiopian wolves imposed by sociality, migration and population bottlenecks. Conserv. Genet. 11, 89–101.
- Randall, D.A., Pollinger, J.P., Wayne, R.K., Tallents, L.A., Johnson, J.P. & Macdonald, D.W. (2007). Inbreeding is reduced by female-biased dispersal and mating behavior in Ethiopian wolves. Behav. Ecol. 18, 579–589.
- Randall, D.A., Williams, S.D., Kuzmin, I.V., Rupprecht, C.E., Tallents, L.A., Tefera, Z., Argaw, K., Shiferaw, F., Knobel, D.L., Sillero-Zubiri, C. & Laurenson, M.K. (2004). Rabies in endangered Ethiopian wolves. Emerg. Infect. Dis. 10, 2214–2217.
- Raymond, M. & Rousset, F. (1995). Genepop (version-1.2) – population-genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249.
- Reed, D.H. & Frankham R. (2003). Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237.
- Rice, W.R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
- Rodríguez-Ramilo, S.T. & Wang, J. (2012). The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol. Ecol. Resour. 12, 873–884.
-
Ryman, N. & Palm, S. (2006). POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol. Resour. 6, 600–602.
10.1111/j.1471-8286.2006.01378.x Google Scholar
- Sacks, B.N., Mitchell, B.R., Williams, C.L. & Ernest, H.B. (2005). Coyote movements and social structure along a cryptic population genetic subdivision. Mol. Ecol. 14, 1241–1249.
- Sastre, N., Vila, C., Salinas, M., Bologov, V.V., Urios, V., Sanchez, A., Francino, O. & Ramirez, O. (2011). Signatures of demographic bottlenecks in European wolf Populations. Conserv. Genet. 12, 701–712.
- Schneider, S., Kueffen, J.M., Roessli, D. & Excoffier, L. (1997). ARLEQUIN, version 1.1. A software for population genetic data analysis. Geneva: Genetics and Biometry Laboratory, University of Geneva.
- Shibuya, H., Collins, B.K., Huang, T.H.M. & Johnson, G.S. (1994). A polymorphic (AGGAAT)n tandem repeat in an intron of the canine von Willebrand factor gene. Anim. Genet. 25, 122–126.
- Sillero-Zubiri, C., Gottelli, D. & Macdonald, D.W. (1996a). Male philopatry, extra pack copulations and inbreeding avoidance in Ethiopian wolves. Behav. Ecol. Sociob. 38, 331–340.
- Sillero-Zubiri, C., King, A.A. & Macdonald, D.W. (1996b). Rabies and mortality in Ethiopian wolves (Canis simensis). J. Wildl. Dis. 32, 80–86.
- Sillero-Zubiri, C. & Marino, J. (2004). Ethiopian wolf. In Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan. 2nd edn. 167–174. C. Sillero-Zubiri, M. Hoffmann & D.W. Macdonald (Eds). Gland, Cambridge: IUCN.
-
Sillero-Zubiri, C., Marino, J., Gottelli, D. & Macdonald, D.W. (2004). Afroalpine ecology, solitary foraging and intense sociality amongst Ethiopian wolves. In Canid biology and conservation, Chapter 20, 311–322. D.W. Macdonald & C. Sillero-Zubiri (Eds). Oxford: Oxford University Press.
10.1093/acprof:oso/9780198515562.003.0020 Google Scholar
- Storz, J.F., Beaumont, M.A. & Alberts, S. (2002). Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol. Biol. Evol. 19, 1981–1990.
- Sugg, D.W., Chesser, R.K., Dobson, F.S. & Hoogland, J.L. (1996). Population genetics meets behavioural ecology. Trends Ecol. Evol. 11, 338–342.
- Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V. & Bouvet, J. (1996). Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res. 24, 3189–3194.
- Tallmon, D.A., Luikart, G. & Waples, R.S. (2004). The alluring simplicity and complex reality of genetic rescue. Trends Ecol. Evol. 19, 489–496.
- Vila, C., Sundqvist, A.K., Flagstad, Q., Seddon, J., Bjornerfeldt, S., Kojola, L., Casulli, A., Sand, H., Wabakken, P. & Ellegren, H. (2003). Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc. Biol. Sci. 270, 91–97.
- vonHoldt, B.M., Stahler, D.R., Bangs, E.E., Smith, D.W., Jimenez, M.D., Mack, C.M., Niemeyer, C.C., Pollinger, J.P. & Wayne, R.K. (2010). A novel assessment of population structure and gene flow in grey wolf populations of the Northern Rocky Mountains of the United States. Mol. Ecol. 19, 4412–4427.
- Wandeler, P., Funk, S.M., Largiadèr, C.R., Gloor, S. & Breitenmoser, U. (2003). The city-fox phenomenon: genetic consequences of a recent colonization of urban habitat. Mol. Ecol. 12, 647–656.
- Wang, J. (2004). Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963–1979. (doi: 10.1534/genetics.166.4.1963).
- Wang, J. & Santure, A.W. (2009). Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181, 1579–1594.
-
Waples, R.S. & Gaggiotti, O. (2006). What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol. Ecol. 15, 1365–1419.
10.1111/j.1365-294X.2006.02890.x Google Scholar
-
Wayne, R.K., Geffen, E. & Vila, C. (2004). Population and conservation genetics of canids. In Canid biology and conservation: Chapter 3, 55–84. D.W. Macdonald & C. Sillero-Zubiri (Eds). Oxford: Oxford University Press.
10.1093/acprof:oso/9780198515562.003.0003 Google Scholar
- Weir, B.S. & Cockerham, C.C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
- Wilson, G.A. & Rannala, B. (2003). Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163, 1177–1191.
- Wright, S. (1965). The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19, 395–420.
- Yalden, D.W., Largen, M.J. & Kock, D. (1980). Catalogue of the mammals of Ethiopia. 4. Carnivora. Mon. Zool. Ital. 13, 169–272.