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Inbreeding reduces long-term growth of Alpine ibex populations

Abstract

Many studies document negative inbreeding effects on individuals, and conservation efforts to preserve rare species routinely employ strategies to reduce inbreeding. Despite this, there are few clear examples in nature of inbreeding decreasing the growth rates of populations, and the extent of population-level effects of inbreeding in the wild remains controversial. Here, we take advantage of a long-term dataset of 26 reintroduced Alpine ibex (Capra ibex ibex) populations spanning nearly 100 years to show that inbreeding substantially reduced per capita population growth rates, particularly for populations in harsher environments. Populations with high average inbreeding (F ≈ 0.2) had population growth rates reduced by 71% compared with populations with no inbreeding. Our results show that inbreeding can have long-term demographic consequences even when environmental variation is large and deleterious alleles may have been purged during bottlenecks. Thus, efforts to guard against inbreeding effects in populations of endangered species have not been misplaced.

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Fig. 1: Two representative Alpine ibex populations analyzed in this study.
Fig. 2: Visualization of the effect of inbreeding on population growth.
Fig. 3: Visualization of the estimated interaction effects of inbreeding and summer precipitation on population growth.

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Data availability

The data that support the findings of this study have been deposited in Dryad Digital Repository52.

References

  1. Hedrick, P. W. & Garcia-Dorado, A. Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol. Evol. 31, 940–952 (2016).

    Article  PubMed  Google Scholar 

  2. Wallace, B. Hard and soft selection revisited. Evolution 29, 465–473 (1975).

    Article  PubMed  Google Scholar 

  3. Agrawal, A. F. & Whitlock, M. C. Mutation load: the fitness of individuals in populations where deleterious alleles are abundant. Annu. Rev. Ecol. Evol. Syst. 43, 115–135 (2012).

    Article  Google Scholar 

  4. Johnson, H. E., Mills, L. S., Wehausen, J. D., Stephenson, T. R. & Luikart, G. Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep. Conserv. Biol. 25, 1240–1249 (2011).

    Article  PubMed  Google Scholar 

  5. Reed, T. E., Grotan, V., Jenouvrier, S., Saether, B.-E. & Visser, M. E. Population growth in a wild bird is buffered against phenological mismatch. Science 340, 488–491 (2013).

    Article  CAS  PubMed  Google Scholar 

  6. Agrawal, A. F. & Whitlock, M. C. Environmental duress and epistasis: how does stress affect the strength of selection on new mutations? Trends Ecol. Evol. 25, 450–458 (2010).

    Article  PubMed  Google Scholar 

  7. Creel, S. Recovery of the Florida panther—genetic rescue, demographic rescue, or both? Response to Pimm et al. (2006). Anim. Conserv. 9, 125–126 (2006).

    Article  Google Scholar 

  8. Wootton, J. T. & Pfister, C. A. Processes affecting extinction risk in the laboratory and in nature. Proc. Natl Acad. Sci. USA 112, E5903 (2015).

    Article  CAS  PubMed  Google Scholar 

  9. Hufbauer, R. A. et al. Reply to Wootton and Pfister: the search for general context should include synthesis with laboratory model systems. Proc. Natl Acad. Sci. USA 112, E5904– (2015).

    Article  CAS  PubMed  Google Scholar 

  10. Kardos, M., Taylor, H. R., Ellegren, H., Luikart, G. & Allendorf, F. W. Genomics advances the study of inbreeding depression in the wild. Evol. Appl. 9, 1205–1218 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Stuwe, M. & Nievergelt, B. Recovery of Alpine ibex from near extinction: the result of effective protection, captive breeding, and reintroductions. Appl. Anim. Behav. Sci. 29, 379–387 (1991).

    Article  Google Scholar 

  12. Grotan, V., Saether, B. E., Filli, F. & Engen, S. Effects of climate on population fluctuations of ibex. Glob. Change Biol. 14, 218–228 (2008).

    Article  Google Scholar 

  13. Biebach, I. & Keller, L. F. A strong genetic footprint of the re-introduction history of Alpine ibex (Capra ibex ibex). Mol. Ecol. 18, 5046–5058 (2009).

    Article  PubMed  Google Scholar 

  14. Biebach, I. & Keller, L. F. Genetic variation depends more on admixture than number of founders in reintroduced Alpine ibex populations. Biol. Conserv. 147, 197–203 (2012).

    Article  Google Scholar 

  15. Biebach, I. & Keller, L. F. D. Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes. Conserv. Genet. 11, 527–538 (2010).

    Article  Google Scholar 

  16. Crow, J. F. in Statistics and Mathematics in Biology (eds Kempthome, O. et al.) 543–556 (Iowa State Univ. Press, 1954).

  17. Jacquard, A. in The Genetic Structure of Populations (ed. Jacquard, A.) 160–219 (Springer, 1974).

  18. Vitalis, R., Dawson, K. & Boursot, P. Interpretation of variation across marker loci as evidence of selection. Genetics 158, 1811–1823 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Weir, B. S. & Goudet, J. A unified characterization of population structure and relatedness. Genetics 206, 2085–2103 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Holsinger, K. E. & Weir, B. S. Genetics in geographically structured populations: defining, estimating and interpreting F ST. Nat. Rev. Genet. 10, 639–650 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Vitalis, R. & Couvet, D. Estimation of effective population size and migration rate from one- and two-locus identity measures. Genetics 157, 911–925 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Fuller, W. A. Measurement Error Models (John Wiley & Sons, 1987).

  23. Muff, S., Riebler, A., Held, L., Rue, H. & Saner, P. Bayesian analysis of measurement error models using integrated nested Laplace approximations. J. R. Stat. Soc. Ser. C 64, 231–252 (2015).

    Article  Google Scholar 

  24. Yun, L. & Agrawal, A. F. Variation in the strength of inbreeding depression across environments: effects of stress and density dependence. Evolution 68, 3599–3606 (2014).

    Article  PubMed  Google Scholar 

  25. Gilpin, M. E. & Soulé, M. E. in Conservation Biology, the Science of Scarcity and Diversity (ed. Soulé, M. E.) 19–34 (Sinauer Assiocates, 1986).

  26. Wright, S. Size of population and breeding structure in relation to evolution. Science 87, 430–431 (1938).

    Google Scholar 

  27. Beaumont, M. A. Estimation of population growth or decline in genetically monitored populations. Genetics 164, 1139–1160 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Facon, B. et al. Inbreeding depression is purged in the invasive insect armonia axyridis. Curr. Biol. 21, 424–427 (2011).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  30. Glemin, S. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57, 2678–2687 (2003).

    Article  PubMed  Google Scholar 

  31. Kirkpatrick, M. & Jarne, P. The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155, 154–167 (2000).

    Article  PubMed  Google Scholar 

  32. Whiteley, A. R., Fitzpatrick, S. W., Funk, W. C. & Tallmon, D. A. Genetic rescue to the rescue. Trends Ecol. Evol. 30, 42–49 (2015).

    Article  PubMed  Google Scholar 

  33. Saccheri, I. et al. Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491–494 (1998).

    Article  CAS  Google Scholar 

  34. O’Grady, J. J. et al. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 133, 42–51 (2006).

    Article  Google Scholar 

  35. Goldberg, E. E. et al. Species selection maintains self-incompatibility. Science 330, 493–495 (2010).

    Article  CAS  PubMed  Google Scholar 

  36. Nievergelt, B. Der Alpensteinbock (Capra Ibex L.) in Seinem Lebensraum (Verlag Paul Parey, 1966).

  37. Abderhalden, W. D. Raumnutzung und Sexuelle Segregation (Albert-Ludwigs-Universität Freiburg i. Brsg., 2004).

  38. Saether, B. E., Lillegard, M., Grotan, V., Filli, F. & Engen, S. Predicting fluctuations of reintroduced ibex populations: the importance of density dependence, environmental stochasticity and uncertain population estimates. J. Anim. Ecol. 76, 326–336 (2007).

    Article  PubMed  Google Scholar 

  39. Jaquiery, J., Guillaume, F. & Perrin, N. Predicting the deleterious effects of mutation load in fragmented populations. Conserv. Biol. 23, 207–218 (2009).

    Article  CAS  PubMed  Google Scholar 

  40. Ciofi, C., Beaumont, M. A., Swingland, I. R. & Bruford, M. W. Genetic divergence and units for conservation in the Komodo dragon Varanus komodoensis. Proc. R. Soc. Lond. B 266, 2269–2274 (1999).

    Article  Google Scholar 

  41. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016); http://www.R-project.org

  42. Grossen, C., Biebach, I., Angelone-Alasaad, S., Keller, L. F. & Croll, D. Population genomics analyses of European ibex species show lower diversity and higher inbreeding in reintroduced populations. Evol. Appl. 11, 123–139 (2018).

    Article  CAS  PubMed  Google Scholar 

  43. Aeschbacher, A. Das Brunftverhalten des Alpensteinwildes (Rentsch, 1978).

  44. Harvey, A. C. Forecasting, Structural Time Series Models and the Kalman Filter (Cambridge Univ. Press, 1989).

  45. Schooler, S. S., Salau, B., Julien, M. H. & Ives, A. R. Alternative stable states explain unpredictable biological control of Salvinia molesta in Kakadu. Nature 470, 86–89 (2011).

    Article  CAS  PubMed  Google Scholar 

  46. Dennis, B., Ponciano, J. M., Lele, S. R., Taper, M. L. & Staples, D. F. Estimating density dependence, process noise, and observation error. Ecol. Monogr. 76, 323–341 (2006).

    Article  Google Scholar 

  47. MathWorks MATLAB (The MathWorks, 2012).

  48. Kendall, M. & Stuart, A. The Advanced Theory of Statistics Vol. 2 (Griffin, 1979).

  49. Carroll, R., Ruppert, D., Stefanski, L. & Crainiceanu, C. Measurement Error in Nonlinear Models: A Modern Perspective (Chapman & Hall, 2006).

  50. Rue, H., Martino, S. & Chopin, N. Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. J. R. Stat. Soc. Ser. B 71, 319–392 (2009).

    Article  Google Scholar 

  51. Spiegelhalter, D. J., Best, N. G., Carlin, B. R. & van der Linde, A. Bayesian measures of model complexity and fit. J. R. Stat. Soc. Ser. B 64, 583–616 (2002).

    Article  Google Scholar 

  52. Bozzuto, C., Biebach, I., Muff, S., Ives, A. R. & Keller, L. F. Inbreeding reduces long-term growth of Alpine ibex populations. Dryad Digital Repository https://doi.org/10.5061/dryad.dc1s8h3 (2019).

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Acknowledgements

We thank the many people who helped us obtain genetic samples from Alpine ibex, especially the cantonal authorities and game wardens. We also thank the Swiss Federal Office for the Environment (FOEN) for the count and harvest data, and Wildtier Schweiz for access to their archives of ibex reintroduction history. We are grateful to S. Aeschbacher and B. Oberholzer for gathering information from these archives, and to T. Bucher and G. Camenisch for help in the laboratory. M. Beaumont provided important insights, and comments by J. Bascompte, E. Albert, H. Kokko, I. Saccheri and K. Strier improved the manuscript. The FOEN financially supported this project.

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I.B. and L.F.K. conceived and designed the study and collected the samples. I.B. performed the genetic analyses and compiled the demographic data. C.B. and A.R.I. analysed the time series data. S.M. performed the measurement-error modelling. All authors wrote the manuscript.

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Correspondence to Anthony R. Ives or Lukas F. Keller.

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Supplementary Figs. 1–4, Tables 1–9 and methods.

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Bozzuto, C., Biebach, I., Muff, S. et al. Inbreeding reduces long-term growth of Alpine ibex populations. Nat Ecol Evol 3, 1359–1364 (2019). https://doi.org/10.1038/s41559-019-0968-1

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