Inbreeding depression (ID) has since long been recognized as a significant factor in evolutionary biology. It is mainly the consequence of (partially) recessive deleterious mutations maintained by mutation-selection balance in large random mating populations. When population size is reduced, recessive alleles are increasingly found in homozygous condition due to drift and inbreeding and become more prone to selection. Particularly at slow rates of drift and inbreeding, selection will be more effective in purging such alleles, thereby reducing the amount of ID. Here we test assumptions of the efficiency of purging in relation to the inbreeding rate and the experimental conditions for four traits in D. melanogaster. We investigated the magnitude of ID for lines that were inbred to a similar level, F ≈ 0.50, reached either by three generations of full-sib mating (fast inbreeding), or by 12 consecutive generations with a small population size (slow inbreeding). This was done on two different food media. We observed significant ID for egg-to-adult viability and heat shock mortality, but only for egg-to-adult viability a significant part of the expressed inbreeding depression was effectively purged under slow inbreeding. For other traits like developmental time and starvation resistance, however, adaptation to the experimental and environmental conditions during inbreeding might affect the likelihood of purging to occur or being detected. We discuss factors that can affect the efficiency of purging and why empirical evidence for purging may be ambiguous.
Subscribe to Journal
Get full journal access for 1 year
only $33.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
All data presented in the paper are deposited in Dryad https://doi.org/10.5061/dryad.rfj6q579k.
Angeloni F, Vergeer P, Wagemaker CAM, Ouborg NJ (2014) Within and between population variation in inbreeding depression in the locally threatened perennial Scabiosa columbaria. Conserv Genet 15:331–342
Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242
Ashburner M, Thompson JN (1978) The laboratory culture of Drosophila. In: Ashburner M, Wright TRF (eds) The Genetics and Biology of Drosophila, vol. 2a. Academic Press, NewYork, NY, p 2–109
Bakker J (2008) Genetic diversity in experimental metapopulations. Ph.D. thesis, University of Groningen, The Netherlands
Ballou JD (1997) Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. J Heredity 88:169–178
Bates D, Maechler M, Bolker B, Walker S (2014). lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-5. http://cran.r-project.org/package=lme4
Bechsgaard JS, Hoffmann AA, Sgró C, Loeschcke V, Bilde T, Kristensen TN (2013) A comparison of inbreeding depression in tropical and widespread Drosophila species. PLoS ONE 8:e51176
Bersabé D, García-Dorado A (2013) On the genetic parameter determining the efficiency of purging: an estimate for Drosophila egg-to-pupae viability. J Evol Biol 26:375–385
Bijlsma R, Bundgaard J, Van Putten WF (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J Evol Biol 12:1125–1137
Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J Evol Biol 13:502–514
Bijlsma R, Loeschcke V (2012) Genetic erosion impedes adaptive responses to stressful environments. Evol Appl 5:117–129
Byers D, Waller D (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst 30:479–513
Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796
Cheptou PO, Donohue K (2011) Environment-depend inbreeding depression: its ecological and evolutionary significance. N Phytol 189:395–407
Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358
Dahlgaard J, Krebs RA, Loeschcke V (1995) Heat-shock tolerance and inbreeding in Drosophila buzzatii. Heredity 74:157–163
Dobzhansly T, Levene H (1955) Genetics of natural populations. XXIV. Developmental homeostasis in natural populations of Drosophila pseudoobscura. Genetics 40:797–808
Ehiobu NG, Goddard ME, Taylor JF (1989) Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster. Theor Appl Genet 77:123–127
Enders LS, Nunney L (2016) Reduction in the cumulative effects of stress-induced inbreeding depression due to intragenerational purging in Drosophila melanogaster. Heredity 116:304–313
Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258
Frankham R, Gilligan DM, Morris D, Briscoe DA (2001) Inbreeding and extinction: effects of purging. Conserv Genet 2:279–285
García-Dorado A (2012) Understanding and predicting the fitness decline of shrunk populations: inbreeding, purging, mutation, and standard selection. Genetics 190:1461–1476
Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678–2687
Hedrick PW (1994) Purging inbreeding depression and the probability of extinction—full-sib mating. Heredity 73:363–372
Hedrick PW (2005). Genetics of populations, 3rd edn. Jones and Bartlett Publishers, Sudbury, MA, p 368
Hedrick PW, García-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol Evol 31:940–952
Hoffmann AA, Hallas R, Sinclair C, Mitrovski P (2001) Levels of variation in stress resistance in Drosophila among strains, population, and geographic regions: patterns for desiccation, starvation, cold resistance, and associated traits. Evolution 55:1621–163
Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge
Kristensen TN, Knudsen MR, Loeschcke V (2011) Slow inbred lines of Drosophila melanogaster express as much inbreeding depression as fast inbred lines under semi-natural conditions. Genetica 139:441–451
Kristensen TN, Henningsen AK, Aastrup C, Bech-Hansen B, Hoberg Bjerre LB, Carlsen B et al. (2016) Fitness components of Drosophila melanogaster developed on a standard laboratory diet or a typical natural food source. Insect Sci 23:771–779
Leberg PL, Firmin BD (2008) Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol Ecol 17:334–343
Lee KP, Jang T (2014) Exploring the nutritional basis for starvation resistance in Drosophila melanogaster. Funct Ecol 28:1144–1155
Lohr JN, Haag CR (2015) Genetic load, inbreeding depression, and hybrid vigor covary with population size: an empirical evaluation of theoretical predictions. Evolution 69:3109–3122
Lopez-Cortegano E, Vilas A, Caballero A, García-Dorado A (2016) Estimation of genetic purging under competitive conditions. Evolution 70:1856–1870
Lynch M, Conery J, Buerger R (1995) Mutation accumulation and the extinction of small populations. Am Nat 146:489–518
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits, chapter 10. Sinnauer Associates: Sunderland, MA
Mikkelsen K, Loeschcke V, Kristensen TN (2010) Trait specific consequences of fast and slow inbreeding: lessons from captive populations of Drosophila melanogaster. Conserv Genet 11:479–488
Morton NE, Crow JF, Muller HJ (1956) An estimate of the mutational damage in man from data on consanguineous marriages. Proc Nat Acad Sci USA 42:855–863
Nunney L (1993) The influence of mating system and overlapping generations on effective population-size. Evolution 47:1329–1341
Pedersen KS, Kristensen TN, Loeschcke V (2005) Effect of inbreeding and rate of inbreeding in Drosophila melanogaster—Hsp70 expression and fitness. J Evol Biol 18:756–762
Pedersen LD, Pedersen AR, Bijlsma R, Bundgaard J (2011) The effects of inbreeding and heat stress on male sterility in Drosophila melanogaster. Bio J Linn Soc 104:432–442
Pekkala N, Knott KE, Kotiaho JS, Puurtinen M (2012) Inbreeding rates modifies the dynamics of genetic load in small populations. Ecol Evol 2:1791–1804
Pekkala N, Knott KE, Kotiaho JS, Nissinen K, Puurtinen M (2014) The effect of inbreeding rate on fitness, inbreeding depression and heterosis over a range of inbreeding coefficients. Evol Appl 7:1107–1119
Peripolli E, Munari DP, Silva MVGB, Lima ALF, Irgangand R, Baldi F (2017) Runs of homozygosity: current knowledge and applications in livestock. Anim Genet 48:255–271
R Core Team (2015) R: a language and environment for statistical computing. http://www.r-project.org/
Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 3:405–410
Rion S, Kawecki TJ (2007) Evolutionary biology of starvation resistance: what we have learned from Drosophila. J Evol Biol 20:1655–1664
Schou MF, Kristensen TN, Kellermann V, Schlötterer C, Loeschcke V (2014) Drosophila laboratory evolution experiment points to low evolutionary potential under increased temperatures likely to be experienced in the future. J Evol Biol 27:1859–1868
Schou MF, Loeschcke V, Kristensen TN (2015) Inbreeding depression across a nutritional stress continuum. Heredity 115:56–62
Schou MF, Loeschcke V, Schlötterer C, Bechsgaard J, Kristensen TN (2017). Unexpected high genetic diversity in small populations suggests maintenance by associative overdominance. Mol Ecol (in press). https://doi.org/10.1111/mec.14262
Schrieber K, Lachmuth S (2017) The genetic paradox of invasions revisited: the potential role of inbreeding x environment interactions in invasion success. Biol Rev 29:939–952
Simmons MJ, Crow JF (1977) Mutations affecting fitness in Drosophila populations. Ann Rev Genet 11:49–78
Swillen I, Vanoverbeke J, De Meester L (2015) Evolution of carbaryl resistance in the water flea Daphnia: complex interactions between inbreeding, stress, and selection. Hydrobiologica 743:199–209
Swindel WR, Bouzat JL (2006a) Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 60:1014–1022
Swindell WR, Bouzat JL (2006b) Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution 60:762–766
Valtonen TM, Roff DA, Rantala MJ (2011) Analysis of the effects of inbreeding on lifespan and starvation resistance in Drosophila melanogaster. Genetica 139:525–533
Vermeulen CJ, Bijlsma R (2004) Changes in mortality patterns and temperature dependence of lifespan in Drosophila melanogaster caused by inbreeding. Heredity 92:275–281
Vermeulen CJ, Bijlsma R, Loeschcke V (2008) QTL mapping of inbreeding-related cold sensitivity and conditional lethality in Drosophila melanogaster. J Evol Biol 21:1236–1244
Wang JL, Hill WG, Charlesworth D, Charlesworth B (1999) Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet Res 74:165–178
Willis JH (1999) The role of genes of large effect on inbreeding depression in Mimilus gutatus. Evolution 53:1678–1691
Wright S (1969) Evolution and the genetics of populations. Vol. 2, The theory of genetic frequencies. University of Chicago Press, Chicago and London
Zwaan BJ, Bijlsma R, Hoekstra RF (1991) On the developmental theory of ageing. 1. Starvation resistance and longevity in Drosophila melanogaster in relation to pre-adult breeding conditions. Heredity 66:29–39
We are grateful to Doth Andersen and Annemarie Højmark for technical help, and the Danish Natural Sciences Research Council (FNU, grant 4002-00113B) for financial support to VL. We thank three reviewers for their constructive comments on an earlier version of the paper.
Conflict of interest
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Associate editor: Darren Obbard
About this article
Cite this article
Bundgaard, J., Loeschcke, V., Schou, M.F. et al. Detecting purging of inbreeding depression by a slow rate of inbreeding for various traits: the impact of environmental and experimental conditions. Heredity (2021). https://doi.org/10.1038/s41437-021-00436-7