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Do bottlenecks increase additive genetic variance?

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Abstract

Because of anthropogenic factors many populations have been at least temporarily reduced to a very small population size. Such reductions could potentially decrease genetic variation and increase the probability of extinction. Analysis of molecular markers has shown a decrease in genetic variation but in many cases this has not reduced the ability of the population to recover from the bottleneck. This apparent paradox is resolved by a consideration of how population bottlenecks can affect additive genetic variance, the relevant measure of ability to respond to selective factors. A bottleneck has the potential to increase additive genetic variance in a population. This may result in an increase in fitness, particularly in populations of conservation concern that are small and lack genetic variation. Here we present a meta-analysis of experimental tests of this prediction using models designed to fit data that is strictly additive and data that has non-additive components. This analysis shows that additive genetic variance in a dataset dominated by morphological traits increases, on average, after a bottleneck event when the inbreeding coefficient is less than 0.3, but neither of the theoretical models alone can adequately explain this result. Because of our inability at present to predict the results of a population bottleneck in a specific case and the probability of extinction associated with small population size we caution against using bottlenecks to increase genetic variance, and thus the fitness, of endangered populations.

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References

  • Alves DA, Imperatriz-Fonseca VL, Francoy TM, Santos-Filho PS, Billen J, Wenseleers T (2011) Successful maintenance of a stingless bee population despite a severe genetic bottleneck. Conserv Genet 12:647–658

    Article  Google Scholar 

  • Andersson S, Ellmer M, Jorgensen TH, Palme A (2010) Quantitative genetic effects of bottlenecks: experimental evidence from a wild plant species, Nigella degenii. J Hered 101:298–307

    Article  PubMed  Google Scholar 

  • Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Turelli M (2004) Effects of genetic drift on variance components under a general model of epistasis. Evolution 58:2111–2132

    PubMed  CAS  Google Scholar 

  • Bellinger MR, Johnson JA, Toepfer J, Dunn P (2003) Loss of genetic variation in Greater Prairie Chickens following a population bottleneck in Wisconsin, USA. Conserv Biol 17:717–724

    Article  Google Scholar 

  • Bonnell ML, Selander RK (1974) Elephant seals: genetic variation and near extinction. Science 184:908–909

    Article  Google Scholar 

  • Briggs WH, Goldman IL (2006) Genetic variation and selection response in model breeding populations of Brassica rapa following a diversity bottleneck. Genetics 172:457–465

    Article  PubMed  CAS  Google Scholar 

  • Bryant EH, Meffert LM (1993) The effect of serial founder-flush cycles on quantitative genetic-variation in the housefly. Heredity 70:122–129

    Article  Google Scholar 

  • Bryant EH, Meffert LM (1995) An analysis of selectional response in relation to a population bottleneck. Evolution 49:626–634

    Article  Google Scholar 

  • Bryant EH, Meffert LM (1996) Nonadditive genetic structuring of morphometric variation in relation to a population bottleneck. Heredity 77:168–176

    Article  Google Scholar 

  • Bryant EH, McCommas SA, Combs LM (1986) The effect of an experimental bottleneck upon quantitative genetic-variation in the housefly. Genetics 114:1191–1211

    PubMed  CAS  Google Scholar 

  • Cardoso MJ, Eldridge MDB, Oakwood M, Rankmore B, Sherwin WB, Firestone KB (2009) Effects of founder events on the genetic variation of translocated island populations: implications for conservation management of the northern quoll. Conserv Genet 10:1719–1733

    Article  Google Scholar 

  • Chan C-H, Robertson HA, Saul EK, Nia LV, Vy Phuong L, Kong X, Zhao Y, Chambers GK (2011) Genetic variation in the kakerori (Pomarea dimidiata), an endangered endemic bird successfully recovering in the Cook Islands. Conserv Genet 12:441–447

    Article  Google Scholar 

  • Cheverud JM, Routman EJ (1996) Epistasis as a source of increased additive genetic variance at population bottlenecks. Evolution 50:1042–1051

    Article  Google Scholar 

  • Cheverud JM, Vaughn TT, Pletscher LS, King-Ellison K, Bailiff J, Adams E, Erickson C, Bonislawski A (1999) Epistasis and the evolution of additive genetic variance in populations that pass through a bottleneck. Evolution 53:1009–1018

    Article  Google Scholar 

  • Cockerham CC, Tachida H (1988) Permanency of response to selection for quantitative characters in finite populations. Proc Natl Acad Sci USA 85:1563–1565

    Article  PubMed  CAS  Google Scholar 

  • Consuegra S, Verspoor E, Knox D, de Leaniz CG (2005) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genet 6:823–842

    Article  CAS  Google Scholar 

  • Corti P, Shafer ABA, Coltman DW, Festa-Bianchet M (2011) Past bottlenecks and current population fragmentation of endangered huemul deer (Hippocamelus bisulcus): implications for preservation of genetic diversity. Conserv Genet 12:119–128

    Article  Google Scholar 

  • Crnokrak P, Roff DA (1995) Dominance variance—associations with selection and fitness. Heredity 75:530–540

    Article  Google Scholar 

  • Crow JF, Kimura M (1970) Introduction to theoretical population genetics. Harper and Row, New York

    Google Scholar 

  • Culver M, Hedrick PW, Murphy K, O’Brien S, Hornocker MG (2008) Estimation of the bottleneck size in Florida panthers. Anim Conserv 11:104–110

    Article  Google Scholar 

  • DeRose MA, Roff DA (1999) A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53:1288–1292

    Article  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  PubMed  CAS  Google Scholar 

  • Dobson AJ (1983) An Introduction to statistical modelling. Chapman and Hall, London

    Google Scholar 

  • Durrant CJ, Beebee TJC, Greenaway F, Hill DA (2009) Evidence of recent population bottlenecks and inbreeding in British populations of Bechstein’s bat, Myotis bechsteinii. Conserv Genet 10:489–496

    Article  Google Scholar 

  • Earl DA, Louie KD, Bardeleben C, Swift CC, Jacobs DK (2010) Range wide microsatellite phylogeography of the endangered tidewater goby, Eucyclogobius newberryi (Teleostei: Gobiidae), a genetically subdivided coastal fish with limited marine dispersal. Conserv Genet 11:103–114

    Article  Google Scholar 

  • Fenderson LE, Kovach AI, Litvaitis JA, Litvaitis MK (2011) Population genetic structure and history of fragmented remnant populations of the New England cottontail (Sylvilagus transitionalis). Conserv Genet 12:943–958

    Article  Google Scholar 

  • Fernandez A, Toro MA, Lopez-Fanjul C (1995) The effect of inbreeding on the redistribution of genetic variance of fecundity and viability in Tribolium castaneum. Heredity 75:376–381

    Article  Google Scholar 

  • Fernandez J, Rodriguez-Ramilo ST, Perez-Figueroa A, Lopez-Fanjul C, Caballero A (2003) Lack of nonadditive genetic effects on early fecundity in Drosophila melanogaster. Evolution 57:558–565

    PubMed  CAS  Google Scholar 

  • Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258

    Article  PubMed  Google Scholar 

  • Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675

    Article  Google Scholar 

  • Frankham R, Lees K, Montgomery ME, England PR, Lowe EH, Briscoe DA (1999) Do population size bottlenecks reduce evolutionary potential? Anim Conserv 2:255–260

    Article  Google Scholar 

  • Funk WC, Forsman ED, Johnson M, Mullins TD, Haig SM (2010) Evidence for recent population bottlenecks in northern spotted owls (Strix occidentalis caurina). Conserv Genet 11:1013–1021

    Article  Google Scholar 

  • Garcia N, Lopez-Fanjul C, Garcia-Dorado A (1994) The genetics of viability in Drosophila melanogaster—effects of inbreeding and artificial selection. Evolution 48:1277–1285

    Article  Google Scholar 

  • Goodnight CJ (1987) On the effect of founder events on epistatic genetic variance. Evolution 41:80–91

    Article  Google Scholar 

  • Goodnight CJ (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42:441–454

    Article  Google Scholar 

  • Griffen BD, Drake JM (2008) A review of extinction in experimental populations. J Anim Ecol 77:1274–1287

    Article  PubMed  Google Scholar 

  • Groombridge JJ, Dawson DA, Burke T, Prys-Jones R, MdL Brooke, Shah N (2009) Evaluating the demographic history of the Seychelles kestrel (Falco araea): genetic evidence for recovery from a population bottleneck following minimal conservation management. Biol Conserv 142:2250–2257

    Article  Google Scholar 

  • Haanes H, Roed KH, Flagstad O, Rosef O (2010) Genetic structure in an expanding cervid population after population reduction. Conserv Genet 11:11–20

    Article  Google Scholar 

  • Habel JC, Zachos FE, Finger A, Meyer M, Louy D, Assmann T, Schmitt T (2009) Unprecedented long-term genetic monomorphism in an endangered relict butterfly species. Conserv Genet 10:1659–1665

    Article  Google Scholar 

  • Hawley DM, Briggs J, Dhondt AA, Lovette IJ (2008) Reconciling molecular signatures across markers: mitochondrial DNA confirms founder effect in invasive North American house finches (Carpodacus mexicanus). Conserv Genet 9:637–643

    Article  Google Scholar 

  • Heber S, Briskie JV (2010) Population bottlenecks and increased hatching failure in endangered birds. Conserv Biol 24:1674–1678

    Article  PubMed  Google Scholar 

  • Hoelzel AR (1999) Impact of population bottlenecks on genetic variation and the importance of life-history; a case study of the northern elephant seal. Biol J Linn Soc 68:23–39

    Article  Google Scholar 

  • Hoelzel AR, Fleischer RC, Campagna C, Le Boeuf BJ, Alvord G (2002) Impact of a population bottleneck on symmetry and genetic diversity in the northern elephant seal. J Evol Biol 15:567–575

    Article  Google Scholar 

  • Jacquemyn H, Roldan-Ruiz I, Honnay O (2010) Evidence for demographic bottlenecks and limited gene flow leading to low genetic diversity in a rare thistle. Conserv Genet 11:1979–1987

    Article  Google Scholar 

  • Kalinowski ST, Muhlfeld CC, Guy CS, Cox B (2010) Founding population size of an aquatic invasive species. Conserv Genet 11:2049–2053

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kristensen TN, Sorensen AC, Sorensen D, Pedersen KS, Sorensen JG, Loeschcke V (2005) A test of quantitative genetic theory using Drosophila—effects of inbreeding and rate of inbreeding on heritabilities and variance components. J Evol Biol 18:763–770

    Article  PubMed  CAS  Google Scholar 

  • Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Philos Trans R Soc B 359:873–890

    Article  Google Scholar 

  • Kuro-o M, Yonekawa H, Saito S, Eda M, Higuchi H, Koike H, Hasegawa H (2010) Unexpectedly high genetic diversity of mtDNA control region through severe bottleneck in vulnerable albatross Phoebastria albatrus. Conserv Genet 11:127–137

    Article  CAS  Google Scholar 

  • Lande R (1980) Genetic variation and phenotypic evolution during allopatric speciation. Am Nat 116:463–479

    Article  Google Scholar 

  • Lande R, Engen S, Saether B (2003) Stochastic population dynamics in ecology and conservation. Oxford University Press, New York

    Book  Google Scholar 

  • Leinonen T, O’Hara RB, Cano JM, Merila J (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J Evol Biol 21:1–17

    PubMed  CAS  Google Scholar 

  • Lints FA, Bourgois M (1984) Population crash, population flush and genetic-variability in cage populations of Drosophila melanogaster. Genet Sel Evol 16:45–55

    Article  Google Scholar 

  • Lopez-Fanjul C, Villaverde A (1989) Inbreeding increases genetic variance for viability in Drosophila melanogaster. Evolution 43:1800–1804

    Article  Google Scholar 

  • Lopez-Fanjul C, Guerra J, Garcia A (1989) Changes in the distribution of the genetic variance of a quantitative trait in small populations of Drosophila melanogaster. Genet Sel Evol 21:159–168

    Article  Google Scholar 

  • Meffert LM (1995) Bottleneck effects on genetic variance for courtship repertoire. Genetics 139:365–374

    PubMed  CAS  Google Scholar 

  • Meimberg H, Hammond JI, Jorgensen CM, Park TW, Gerlach JD, Rice KJ, McKay JK (2006) Molecular evidence for an extreme genetic bottleneck during introduction of an invading grass to California. Biol Invasions 8:1355–1366

    Article  Google Scholar 

  • Merila J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903

    Article  Google Scholar 

  • Miller KA, Towns DR, Allendorf FW, Ritchie PA, Nelson NJ (2011) Genetic structure and individual performance following a recent founding event in a small lizard. Conserv Genet 12:461–473

    Article  Google Scholar 

  • Moritz RFA, Haddad N, Bataieneh A, Shalmon B, Hefetz A (2010) Invasion of the dwarf honeybee Apis florea into the near East. Biol Invasions 12:1093–1099

    Article  Google Scholar 

  • Munoz-Fuentes V, Green AJ, Negro JJ, Sorenson MD (2005) Population structure and loss of genetic diversity in the endangered white-headed duck, Oxyura leucocephala. Conserv Genet 6:999–1015

    Article  Google Scholar 

  • Neumann K, Jansman H, Kayser A, Maak S, Gattermann R (2004) Multiple bottlenecks in threatened western European populations of the common hamster Cricetus cricetus (L.). Conserv Genet 5:181–193

    Article  CAS  Google Scholar 

  • Palo JU, O’Hara RB, Laugen AT, Laurila A, Primmer CR, Merila J (2003) Latitudinal divergence of common frog (Rana temporaria) life history traits by natural selection: evidence from a comparison of molecular and quantitative genetic data. Mol Ecol 12:1963–1978

    Article  PubMed  CAS  Google Scholar 

  • Puillandre N, Dupas S, Dangles O, Zeddam JL, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain JF (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333

    Article  Google Scholar 

  • Reed DH (2010) Albatrosses, eagles and newts, Oh My!: exceptions to the prevailing paradigm concerning genetic diversity and population viability? Anim Conserv 13:448–457

    Article  Google Scholar 

  • Ricanova S, Bryja J, Cosson J-F, Csongor G, Choleva L, Ambros M, Sedlacek F (2011) Depleted genetic variation of the European ground squirrel in Central Europe in both microsatellites and the major histocompatibility complex gene: implications for conservation. Conserv Genet 12:1115–1129

    Article  Google Scholar 

  • Robertson A (1952) The effect of inbreeding on the variation due to recessive genes. Genetics 37:188–207

    Google Scholar 

  • Roff DA (1997) Evolutionary quantitative genetics. Chapman Hall, New York

    Book  Google Scholar 

  • Roff DA (1998) Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity 81:28–37

    Article  Google Scholar 

  • Roff DA (2006) Introduction to computer-intensive methods of data analysis in biology. Cambridge University Press, New York

    Book  Google Scholar 

  • Roff DA, Emerson K (2006) Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution 60:1981–1990

    PubMed  Google Scholar 

  • Russell JC, Abdelkrim J, Fewster RM (2009) Early colonisation population structure of a Norway rat island invasion. Biol Invasions 11:1557–1567

    Article  Google Scholar 

  • Saccheri IJ, Nichols RA, Brakefield PM (2001) Effects of bottlenecks on quantitative genetic variation in the butterfly Bicyclus anynana. Genet Res 77:167–181

    Article  PubMed  CAS  Google Scholar 

  • Sastre N, Vila C, Salinas M, Bologov VV, Urios V, Sanchez A, Francino O, Ramirez O (2011) Signatures of demographic bottlenecks in European wolf populations. Conserv Genet 12:701–712

    Article  Google Scholar 

  • Schoville SD, Tustall TS, Vredenburg VT, Backlin AR, Gallegos E, Wood DA, Fisher RN (2011) Conservation genetics of evolutionary lineages of the endangered mountain yellow-legged frog, Rana muscosa (Amphibia: Ranidae), in southern California. Biol Conserv 144:2031–2040

    Google Scholar 

  • Sinclair EA, Costello B, Courtenay JM, Crandall KA (2002) Detecting a genetic bottleneck in Gilbert’s Potoroo (Potorous gilbertii) (Marsupialia: Potoroidae), inferred from microsatellite and mitochondrial DNA sequence data. Conserv Genet 3:191–196

    Article  CAS  Google Scholar 

  • Swatdipong A, Primmer CR, Vasemagi A (2010) Historical and recent genetic bottlenecks in European grayling, Thymallus thymallus. Conserv Genet 11:279–292

    Article  Google Scholar 

  • Tachida H, Cockerham CC (1989a) A building block model for quantitative genetics. Genetics 121:839–844

    PubMed  CAS  Google Scholar 

  • Tachida H, Cockerham CC (1989b) Effects of identity disequilibrium and linkage on quantitative variation in finite populations. Genet Res 53:63–70

    Article  PubMed  CAS  Google Scholar 

  • Turelli M, Barton NH (2006) Will population bottlenecks and multilocus epistasis increase additive genetic variance? Evolution 60:1763–1776

    PubMed  Google Scholar 

  • Van Buskirk J, Willi Y (2006) The change in quantitative genetic variation with inbreeding. Evolution 60:2428–2434

    Article  PubMed  Google Scholar 

  • van Heerwaarden B, Willi Y, Kristensen TN, Hoffmann AA (2008) Population bottlenecks increase additive genetic variance but do not break a selection limit in rain forest Drosophila. Genetics 179:2135–2146

    Article  PubMed  Google Scholar 

  • Weber D, Stewart BS, Garza JC, Lehman N (2000) An empirical genetic assessment of the severity of the northern elephant seal population bottleneck. Curr Biol 10:1287–1290

    Article  PubMed  CAS  Google Scholar 

  • Whitlock MC, Fowler K (1999) The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics 152:345–353

    PubMed  CAS  Google Scholar 

  • Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458

    Article  Google Scholar 

  • Willis JH, Orr HA (1993) Increased heritable variation following population bottlenecks—the role of dominance. Evolution 47:949–957

    Article  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Article  Google Scholar 

  • Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9:833–843

    Article  Google Scholar 

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  1. Department of Biology, University of California, Riverside, CA, 92521, USA

    Heather R. Taft & Derek A. Roff

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Correspondence to Heather R. Taft.

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Taft, H.R., Roff, D.A. Do bottlenecks increase additive genetic variance?. Conserv Genet 13, 333–342 (2012). https://doi.org/10.1007/s10592-011-0285-y

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