Abstract
The effect of small population size and gene flow on the rate ofinbreeding and loss in fitness in Bicyclus anynana populationswas quantified by means of a pedigree analysis. Laboratorymetapopulations each consisted of four subpopulations with breeding sizeof N = 6 or N = 12 and migration rate of m = 0 or m= 0.33. Pedigrees were established by individually marking about35,000 butterflies. The increase in inbreeding coefficients(F-coefficients) over time was compared to that of simulated populationswith similar N and m. In the seventh generation, the level of inbreedingin larger subpopulations did not deviate significantly from the expectedvalues, but smaller subpopulations were less inbred than expected.Individuals in the small populations still showed considerableinbreeding depression, indicating that only a small proportion of therecessive deleterious alleles had been purged by selection. Two opposingprocesses potentially affected the rate of inbreeding and fitness: (1)Inbreeding depression increased the variance in family size and reducedthe effective population size. This will accelerate the rate ofinbreeding and is expected to selectively purge deleterious recessivealleles. (2) Variance in reproductive success of families was reducedbecause individuals which had a large number of siblings in thepopulation were more likely to mate with a full-sib than individualswith a smaller number of siblings. Subsequent inbreeding depressionreduced the number of viable offspring produced by these full-sibmatings. As a consequence, natural selection purged only some of thedeleterious alleles from the butterfly populations during sevengenerations with inbreeding. These findings emphasise the potentialproblems of using only small numbers of breeding individuals (N≤10) incaptive populations for conservation purposes.
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References
Barton NH, Whitlock MC (1997) Genetic effective size of a metapopulation. In: Metapopulation Biology: Ecology, Genetics, and Evolution (eds. Hanski IA, Gilpin ME), pp. 183-210. Academic Press, London.
Bernardo R, Murigneux A, Maisonneuve JP, Johnsson C, Karaman Z (1997) RFLP-based estimates of parental contribution to F2-and BC1 derived maize inbreds. Theor. Appl. Genet., 94, 652-656.
Blackwell BF, Doerr PD, Reed JM, Walters JR (1995) Inbreeding rate and effective population size: a comparison of estimates from pedigree analysis and a demographic model. Biol. Conserv., 71, 299-304.
Borlase SC, Loebel DA, Frankham R, Nurthen RK, Briscoe DA, Daggard GE (1993) Modelling problems in conservation genetics using captive Drosophila populations: consequences of equalisation of family sizes. Conserv. Biol., 7, 122-131.
Boyce AJ (1983) Computation of inbreeding and kinship coefficients on extended pedigrees. Heredity, 74, 400-404.
Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics, 134, 1289-1303.
Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet. Res., 70, 155-174.
Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann. Rev. Ecol. Syst., 18, 237-268.
Cornelius PL, Dudley JW (1974) Effects of inbreeding by selfing and full-sib mating in a maize population. Crop Sci., 14, 815-819.
Couvet JF, Ronfort (1994) Mutation load depending on variance in reproductive success and mating system. In: Conservation Genetics (eds. Loeschcke V, Tomiuk J, Jain SK), pp. 55-68. Birkhäuser Verslag, Basel, Switzerland.
Crow JF, Kimura M (1970) An Introduction to Population Genetic Theory. Harper & Row, New York.
Ehiobu NG, Goddard ME, Taylor JF (1989) Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster. Theor. Appl. Genet., 77, 123-177.
Falconer DS, Mackay TFC (1996) Introduction to Quantitative Genetics, 4th edn. Longman, Harlow.
Fisher RA (1930) The Genetical Theory of Natural Selection. Dover, New York.
Folch P, Jordana J (1998) Demographic characterization, inbreeding and maintenance of genetic diversity in the endangered Catalonian donkey breed. Genet. Sel. Evol., 30, 195-201.
Frankham R (1995) Conservation genetics. Ann. Rev. Genet., 29, 305-327.
Good RL, Hallauer AR (1977) Inbreeding depression in maize by selfing and full-sibbing. Crop Sci., 17, 935-940.
Groen AF, Kennedy BW, Eissen JJ (1995) Potential bias in inbreeding depression estimates when using pedigree relationships to assess the degree of homozygosity for loci under selection. Theor. Appl. Genet., 91, 665-671.
Hanski IA, Pakkala T, Kuussaari M, Lei G (1995) Metapopulation persistence of an endangered butterfly in a fragmented landscape. Oikos, 72, 21-28.
Hedges LB, Olkin I (1985) Statistical Methods in Meta-Analysis. Academic Press, New York.
Hedrick PH, Gilpin ME (1997) Genetic effective size of a metapopulation. In: Metapopulation Biology: Ecology, Genetics, and Evolution (eds. Hanski IA, Gilpin ME), pp. 165-181. Academic Press, London.
Jorde LB (1989) Inbreeding in the Utah Mormons: an evaluation of estimates based on pedigrees, isonymy, and migration matrices. Ann. Hum. Genet., 53, 339-355.
Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics, 49, 561-576.
Lynch M (1996) A quantitative genetic perspective on conservation issues. In: Conservation Genetics: Case Histories from Nature (eds. Avise JC, Hamrick JL), pp. 471-501. Chapman & Hall, New York.
Lynch M, Walsh B (1998). Genetics and Analysis of Quantitative Traits. Sinauer Associates Inc., Massachusetts, USA
MacCluer JW, Boyce AJ, Dyke B, Weitkamp LR, Pfennig DW, Parsons CJ (1983) Inbreeding and pedigree structure in Standard bred horses. J. Hered., 74, 394-399.
Maruyama T, Kimura M (1980) Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Science, 77, 6710-6714.
Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet. Res., 23, 23-35.
Miller PS (1994) Is inbreeding depression more severe in a stressful environment? Zoo Biol., 13, 195-208.
Montgomery ME, Ballou JD, Nurthen RK, England PR, Briscoe DA, Frankham R (1997) Minimizing kinship in captive breeding programs. Zoo Biol., 16, 377-389.
Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution, 47, 1329-1341.
Oosterhout C van (2000) Captive Metapopulations of the Butterfly Bicyclus anynana. Ph.D. Thesis, Leiden University, The Netherlands.
Oosterhout C van, Zijlstra WG, Heuven MK van, Brakefield PM (2000) Inbreeding depression and genetic load in laboratory metapopulations of the butterfly Bicyclus anynana. Evolution, 54, 56-64.
Reed JM, Walters JR, Emigh TE, Seaman DE (1993) Effective population size in the red-cockaded woodpeckers: Population and model differences. Conserv. Biol., 7, 302-308.
Rumball W, Franklin IR, Frankham R, Sheldron BL (1994) Decline in heterozygosity under full-sib and double first cousin inbreeding in Drosophila melanogaster. Genetics, 136, 1039-1049.
Saccheri IJ, Brakefield PM, Nichols RA (1996) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution, 50, 2000-2013.
Saccheri IJ, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski IA (1998). Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491-494.
Shaw DV (1995) Comparison of ancestral and current-generation inbreeding in an experimental strawberry breeding population. Theor. Appl. Genet., 90, 237-241.
Shaw DV (1997) Trait mean depression for second-generation inbred strawberry populations with and without parent selection. Theor. Appl. Genet., 95, 261-264.
Thomas CD, Hanski IA (1997) Butterfly metapopulations. In: Metapopulation Biology: Ecology, Genetics, and Evolution (eds. Hanski IA, Gilpin ME), pp. 359-386. Academic Press, London.
Wang J, Caballero A (1999). Developments in predicting the effective size of subdivided populations. Heredity, 82, 212-226.
Witkowski Z, Adamski P, Kosior A, Plonka P (1997) Extinction and reintroduction of Parnassius Apollo in the Pieniny National Park (Polish Carpathians). Biologia, 52, 199-208.
Woodworth LM, Montgomery ME, Nurthen RK, Briscoe DA, Frankham R (1994) Modelling problems in conservation genetics using Drosophila: consequences of fluctuating population sizes. Mol. Ecol., 3, 393-399.
Wright S (1938) Size of population and breeding structure in relation to evolution. Science, 87, 430-431.
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van Oosterhout, C., Smit, G., van Heuven, M.K. et al. Pedigree analysis on small laboratory populations of the butterfly Bicyclus anynana: The effects of selection on inbreeding and fitness. Conservation Genetics 1, 321–328 (2000). https://doi.org/10.1023/A:1011586612284
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DOI: https://doi.org/10.1023/A:1011586612284