Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Detecting purging of inbreeding depression by a slow rate of inbreeding for various traits: the impact of environmental and experimental conditions

Abstract

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: The average fraction of eggs reaching the adult stage (egg-to-adult viability) for each of the four inbreeding treatments and the control treatment tested on both Groningen (left) and Leeds medium (right).
Fig. 2: Median preadult developmental time (DT50) of males (left panel) and females (right panel) for each of the four inbreeding treatments and the control treatment tested on both Groningen and Leeds medium.
Fig. 3: Average mortality of males after a heat shock (37 °C for 2 h) for each of the four inbreeding treatments and the control treatment.
Fig. 4: Starvation resistance expressed as the average time 50% of the males tested had died (LT50) for each of the four inbreeding treatments and the control treatment.

Data availability

All data presented in the paper are deposited in Dryad https://doi.org/10.5061/dryad.rfj6q579k.

References

  1. 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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  3. 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

  4. Bakker J (2008) Genetic diversity in experimental metapopulations. Ph.D. thesis, University of Groningen, The Netherlands

  5. Ballou JD (1997) Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. J Heredity 88:169–178

    CAS  Google Scholar 

  6. 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

  7. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 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

    PubMed  Google Scholar 

  9. Bijlsma R, Bundgaard J, Van Putten WF (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J Evol Biol 12:1125–1137

    Google Scholar 

  10. 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

    Google Scholar 

  11. Bijlsma R, Loeschcke V (2012) Genetic erosion impedes adaptive responses to stressful environments. Evol Appl 5:117–129

    CAS  PubMed  Google Scholar 

  12. 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

    Google Scholar 

  13. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Google Scholar 

  14. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    CAS  PubMed  Google Scholar 

  15. Cheptou PO, Donohue K (2011) Environment-depend inbreeding depression: its ecological and evolutionary significance. N Phytol 189:395–407

    Google Scholar 

  16. Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    PubMed  Google Scholar 

  17. Dahlgaard J, Krebs RA, Loeschcke V (1995) Heat-shock tolerance and inbreeding in Drosophila buzzatii. Heredity 74:157–163

    PubMed  Google Scholar 

  18. Dobzhansly T, Levene H (1955) Genetics of natural populations. XXIV. Developmental homeostasis in natural populations of Drosophila pseudoobscura. Genetics 40:797–808

    Google Scholar 

  19. Ehiobu NG, Goddard ME, Taylor JF (1989) Effect of rate of inbreeding on inbreeding depression in Drosophila melanogaster. Theor Appl Genet 77:123–127

    CAS  PubMed  Google Scholar 

  20. 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

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  22. Frankham R, Gilligan DM, Morris D, Briscoe DA (2001) Inbreeding and extinction: effects of purging. Conserv Genet 2:279–285

    Google Scholar 

  23. García-Dorado A (2012) Understanding and predicting the fitness decline of shrunk populations: inbreeding, purging, mutation, and standard selection. Genetics 190:1461–1476

    PubMed  PubMed Central  Google Scholar 

  24. Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678–2687

    PubMed  Google Scholar 

  25. Hedrick PW (1994) Purging inbreeding depression and the probability of extinction—full-sib mating. Heredity 73:363–372

    PubMed  Google Scholar 

  26. Hedrick PW (2005). Genetics of populations, 3rd edn. Jones and Bartlett Publishers, Sudbury, MA, p 368

  27. Hedrick PW, García-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol Evol 31:940–952

    PubMed  Google Scholar 

  28. 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

    CAS  PubMed  Google Scholar 

  29. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Google Scholar 

  30. 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

    PubMed  Google Scholar 

  31. 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

    PubMed  Google Scholar 

  32. Leberg PL, Firmin BD (2008) Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol Ecol 17:334–343

    PubMed  Google Scholar 

  33. Lee KP, Jang T (2014) Exploring the nutritional basis for starvation resistance in Drosophila melanogaster. Funct Ecol 28:1144–1155

    Google Scholar 

  34. 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

    PubMed  Google Scholar 

  35. Lopez-Cortegano E, Vilas A, Caballero A, García-Dorado A (2016) Estimation of genetic purging under competitive conditions. Evolution 70:1856–1870

    CAS  PubMed  Google Scholar 

  36. Lynch M, Conery J, Buerger R (1995) Mutation accumulation and the extinction of small populations. Am Nat 146:489–518

    Google Scholar 

  37. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits, chapter 10. Sinnauer Associates: Sunderland, MA

  38. 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

    Google Scholar 

  39. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Nunney L (1993) The influence of mating system and overlapping generations on effective population-size. Evolution 47:1329–1341

    PubMed  Google Scholar 

  41. 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

    CAS  PubMed  Google Scholar 

  42. 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

    Google Scholar 

  43. 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

    PubMed  PubMed Central  Google Scholar 

  44. 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

    PubMed  PubMed Central  Google Scholar 

  45. 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

    CAS  PubMed  Google Scholar 

  46. R Core Team (2015) R: a language and environment for statistical computing. http://www.r-project.org/

  47. Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 3:405–410

    Google Scholar 

  48. Rion S, Kawecki TJ (2007) Evolutionary biology of starvation resistance: what we have learned from Drosophila. J Evol Biol 20:1655–1664

    CAS  PubMed  Google Scholar 

  49. 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

    CAS  PubMed  Google Scholar 

  50. Schou MF, Loeschcke V, Kristensen TN (2015) Inbreeding depression across a nutritional stress continuum. Heredity 115:56–62

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 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

  52. 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

    Google Scholar 

  53. Simmons MJ, Crow JF (1977) Mutations affecting fitness in Drosophila populations. Ann Rev Genet 11:49–78

    CAS  PubMed  Google Scholar 

  54. 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

    CAS  Google Scholar 

  55. Swindel WR, Bouzat JL (2006a) Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 60:1014–1022

    Google Scholar 

  56. Swindell WR, Bouzat JL (2006b) Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster. Evolution 60:762–766

    PubMed  Google Scholar 

  57. 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

    PubMed  Google Scholar 

  58. Vermeulen CJ, Bijlsma R (2004) Changes in mortality patterns and temperature dependence of lifespan in Drosophila melanogaster caused by inbreeding. Heredity 92:275–281

    CAS  PubMed  Google Scholar 

  59. 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

    CAS  PubMed  Google Scholar 

  60. 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

    CAS  PubMed  Google Scholar 

  61. Willis JH (1999) The role of genes of large effect on inbreeding depression in Mimilus gutatus. Evolution 53:1678–1691

    CAS  PubMed  Google Scholar 

  62. Wright S (1969) Evolution and the genetics of populations. Vol. 2, The theory of genetic frequencies. University of Chicago Press, Chicago and London

    Google Scholar 

  63. 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

    PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Volker Loeschcke.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate editor: Darren Obbard

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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 127, 10–20 (2021). https://doi.org/10.1038/s41437-021-00436-7

Download citation

Search

Quick links