All Title Author
Keywords Abstract

PLOS ONE  2006 

Selection for Heterozygosity Gives Hope to a Wild Population of Inbred Wolves

DOI: 10.1371/journal.pone.0000072

Full-Text   Cite this paper   Add to My Lib


Recent analyses have questioned the usefulness of heterozygosity estimates as measures of the inbreeding coefficient (f), a finding that may have dramatic consequences for the management of endangered populations. We confirm that f and heterozygosity is poorly correlated in a wild and highly inbred wolf population. Yet, our data show that for each level of f, it was the most heterozygous wolves that established themselves as breeders, a selection process that seems to have decelerated the loss of heterozygosity in the population despite a steady increase of f. The markers contributing to the positive relationship between heterozygosity and breeding success were found to be located on different chromosomes, but there was a substantial amount of linkage disequilibrium in the population, indicating that the markers are reflecting heterozygosity over relatively wide genomic regions. Following our results we recommend that management programs of endangered populations include estimates of both f and heterozygosity, as they may contribute with complementary information about population viability.


[1]  Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16: 629–636.
[2]  Gilpin ME, Soulé ME (1986) Conservation Biology: the science of scarcity and diversity,. Soulé ME, editor. (Sinauer Associates). pp. 19–34.
[3]  Garner A, Rachlow JL, Hicks JF (2005) Patterns of genetic diversity and its loss in mammalian populations. Conservation Biology 19: 1215–1221.
[4]  Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17: 230–241.
[5]  Pemberton J (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19: 613–615.
[6]  Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 13: 3021–3031.
[7]  Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, et al. (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93: 255–265.
[8]  Leary RF, Allendorf FW, Knudsen KL (1987) Differences in inbreeding coefficients do not explain the association between heterozygosity at allozyme loci and developmental stability in rainbow trout. Evolution 41: 1413–1415.
[9]  Bierne N, Launey S, Naciri-Graven Y, Bonhomme F (1998) Early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae. Genetics 148: 1893–1906.
[10]  Hansson B, Westerdahl H, Hasselquist D, ?kesson M, Bensch S (2004) Does linkage disequilibria generate heterozygosity-fitness correlations in great reed warblers? Evolution 58: 870–879.
[11]  Markert JA, Grant PR, Grant BR, Keller LF, Coombs JL, et al. (2004) Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandens). Heredity 92: 306–315.
[12]  Liberg O, Andrén H, Pedersen H-C, Sand H, Sejberg D, et al. (2005) Severe inbreeding depression in a wild wolf (Canis lupus) population. Biol. Lett. 1: 17–20.
[13]  R?ikk?nen J, Bignert A, Mortensen P, Fernholm B (2006) Congenital defects in a highly inbred wild wolf population (Canis lupus). Mammalian Biology 71: 65–73.
[14]  Wabakken P, Aronson ?, Stromseth TH, Sand H, Kojola I (2005) The wolf in Scandinavia: Status report of the 2004–2005 winter. H?gskolan i Hedmark, Oppdragsrapport nr.. 6–2005. (in Norwegian with English summary).
[15]  Flagstad O, Walker CW, Vila C, Sundquist A-K, Fernholm B, et al. (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.
[16]  Vila C, Sundquist A-K, Flagstad O, Seddon J, Bj?rnerfeldt S, et al. (2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc. R. Soc. Lond. B 270: 91–97.
[17]  Kimura M (1983) The Neutral Theory of Molecular Evolution. Cambridge: Cambridge University Press.
[18]  David P (1998) Heterozygosity-fitness correlations: new perspective on old problems. Heredity 80: 531–537.
[19]  Lacy RC (1995) VORTEX – a stochastic simulation of the extinction process. 7.0. Chicago Zoological Society.
[20]  Andrén H (2006) Genetic aspects of viability in small wolf populations - with emphasis on the Scandinavian wolf population,. Liberg O, editor. Stockholm: (Naturv?rdsverket - Swedish Environmental Protection Agency. pp. 59–61.
[21]  Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size. Queensland Government, Department of Primary Industries and Fisheries.
[22]  Leonard JA, Vila C, Wayne RK (2005) Legacy lost: genetic variability and population size of extirpated US grey wolves (Canis lupus). Mol. Ecol. 14: 9–17.
[23]  Aspi J, Roininen E, Ruokonen M, Kojola I, Vila C (2006) Genetic diversity, population structure, effective population size and demographic history of the Finnish wolf population. Mol. Ecol. 15: 1561–1576.
[24]  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.
[25]  Ellegren H (1999) Inbreeding and relatedness in Scandinavian grey wolves Canis lupus. Hereditas 130: 239–244.
[26]  Keller LF, Arcese P, Smith JNM, Hochachka WM, Stearns SC (1994) Selection against inbred song sparrows during a natural population bottleneck. Nature 372: 356–357.
[27]  Jimenez JA, Hughes KA, Alaks G, Graham L, Lacy RC (1994) An experimental study of inbreeding depression in a natural habitat. Science 266: 271–273.
[28]  Ralls K, Ballou JD, Templeton A (1988) Estimates of Lethal Equivalents and the cost of inbreeding in mammals. Conservation Biology 2: 185–193.
[29]  Kalinowski ST, Hedrick PW, Miller PS (1999) No inbreeding depression observed in Mexican and red wolf captive breeding programs. Conservation Biology 13: 1371–1377.
[30]  McKusick VA (2000) Ellis-van Creveld syndrome and the Amish. Nature Genetics 24: 203–204.
[31]  Hartl DL, Clark AG (1997) Principles of population genetics. Sunderland, Massachusetts: Sinauer Associates Inc..
[32]  Dunning AM, Durocher F, Healey CS, Teare MD, McBride SE, et al. (2000) The extent of linkage disequilibrium in four populations with distinct demographic histories. Am. J. Hum. Genet. 67: 1544–1554.
[33]  Sutter NB, Eberle MA, Parker HG, Pullar BJ, Kirkness EF, et al. (2004) Extensive and breeding-specific linkage disequilibrium in Canis familiaris. Genome Research 14: 2388–2396.
[34]  McRae AF, McEwan JC, Dodds KG, Wilson T, Crawford AM, et al. (2002) Linkage disequilibrium in domestic sheep. Genetics 160: 1113–1122.
[35]  Otto SP, Whitlock MC (1997) The probability of fixation in populations of changing size. Genetics 146: 723–733.
[36]  Wabakken P, Sand H, Liberg O, Bj?rvall A (2001) The recovery, distribution, and population dynamics of wolves on the Scandinavian peninsula, 1978–1998. Can. J. Zool. 79: 710–725.
[37]  Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol. Evol. 14: 323–327.
[38]  Morton NE, Crow JF, Muller HJ (1956) An estimate of the mutational damage in man from data on consanguineous marriages. Proc. Natl. Acad. Sci. USA 42: 855–863.
[39]  Kalinowski ST, Hedrick PW (1998) An improved method for estimating inbreeding depression in pedigrees. Zoo Biology 17: 481–497.
[40]  Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, et al. (2001) The strength of phenotypic selection in natural populations. Am. Nat. 157: 245–261.
[41]  Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37: 1210–1226.
[42]  Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Essex: Longman Group Ltd.
[43]  Schluter D, Smith JNM (1986) Natural selection on beak and body size in the song sparrow. Evolution 40: 221–231.


comments powered by Disqus