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Gene flow from domesticated escapes alters the life history of wild Atlantic salmon

Abstract

Interbreeding between domesticated and wild animals occurs in several species. This gene flow has long been anticipated to induce genetic changes in life-history traits of wild populations, thereby influencing population dynamics and viability. Here, we show that individuals with high levels of introgression (domesticated ancestry) have altered age and size at maturation in 62 wild Atlantic salmon Salmo salar populations, including seven ancestral populations to breeding lines of the domesticated salmon. This study documents widespread changes to life-history traits in wild animal populations following gene flow from selectively bred, domesticated conspecifics. The continued high abundance of escaped, domesticated Atlantic salmon thus threatens wild Atlantic salmon populations by inducing genetic changes in fitness-related traits. Our results represent key evidence and a timely warning concerning the potential ecological impacts of the globally increasing use of domesticated animals.

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Figure 1: Effect of introgression (proportion of domesticated genome) on life history.

References

  1. Kidd, A. G., Bowman, J., Lesbarreres, D. & Schulte-Hostedde, A. I. Hybridization between escaped domestic and wild American mink (Neovison vison). Mol. Ecol. 18, 1175–1186 (2009).

    Article  CAS  PubMed  Google Scholar 

  2. Verardi, A., Lucchini, V. & Randi, E. Detecting introgressive hybridization between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis. Mol. Ecol. 15, 2845–2855 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Canu, A. et al. Are captive wild boar more introgressed than free-ranging wild boar? Two case studies in Italy. Eur. J. Wildlife. Res. 60, 459–467 (2014).

    Article  Google Scholar 

  4. Lecis, R. et al. Bayesian analyses of admixture in wild and domestic cats (Felis silvestris) using linked microsatellite loci. Mol. Ecol. 15, 119–131 (2006).

    Article  CAS  PubMed  Google Scholar 

  5. Halbert, N. D. & Derr, J. N. A comprehensive evaluation of cattle introgression into US federal bison herds. J. Hered. 98, 1–12 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Glover, K. A. et al. Atlantic salmon populations invaded by farmed escapees: quantifying genetic introgression with a Bayesian approach and SNPs. BMC Genet. 14, 74 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Karlsson, S., Diserud, O. H., Fiske, P. & Hindar, K. Widespread genetic introgression of escaped farmed Atlantic salmon in wild salmon populations. ICES J. Mar. Sci. 73, 2488–2498 (2016).

    Article  Google Scholar 

  8. Taberlet, P. et al. Are cattle, sheep, and goats endangered species? Mol. Ecol. 17, 275–284 (2008).

    Article  CAS  PubMed  Google Scholar 

  9. Tufto, J. Effects of releasing maladapted individuals: a demographic-evolutionary model. Am. Nat. 158, 331–340 (2001).

    CAS  PubMed  Google Scholar 

  10. Tufto, J. Gene flow from domesticated species to wild relatives: migration load in a model of multivariate selection. Evolution 64, 180–192 (2010).

    Article  PubMed  Google Scholar 

  11. Ellstrand, N. C. Dangerous Liaisons?: When Cultivated Plants Mate with their Wild Relatives (Johns Hopkins Univ. Press, 2003).

    Google Scholar 

  12. Gjøen, H. M. & Bentsen, H. B. Past, present, and future of genetic improvement in salmon aquaculture. ICES J. Mar. Sci. 54, 1009–1014 (1997).

    Google Scholar 

  13. Gjedrem, T. The first family-based breeding program in aquaculture. Rev. Aquacult. 2, 2–15 (2010).

    Article  Google Scholar 

  14. Moen, T., Baranski, M., Sonesson, A. K. & Kjoglum, S. Confirmation and fine-mapping of a major QTL for resistance to infectious pancreatic necrosis in Atlantic salmon (Salmo salar): population-level associations between markers and trait. BMC Genom. 10, 368 (2009).

    Article  Google Scholar 

  15. Thodesen, J., Grisdale-Helland, B., Helland, S. J. & Gjerde, B. Feed intake, growth and feed utilization of offspring from wild and selected Atlantic salmon (Salmo salar). Aquaculture 180, 237–246 (1999).

    Article  Google Scholar 

  16. Solberg, M. F., Skaala, O., Nilsen, F. & Glover, K. A. Does domestication cause changes in growth reaction norms? A study of farmed, wild and hybrid Atlantic salmon families exposed to environmental stress. PLoS ONE 8, e54469 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Einum, S. & Fleming, I. A. Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J. Fish Biol. 50, 634–651 (1997).

    Article  Google Scholar 

  18. Fraser, D. J., Minto, C., Calvert, A. M., Eddington, J. D. & Hutchings, J. A. Potential for domesticated-wild interbreeding to induce maladaptive phenology across multiple populations of wild Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 67, 1768–1775 (2010).

    Article  Google Scholar 

  19. Yates, M. C., Debes, P. V., Fraser, D. J. & Hutchings, J. A. The influence of hybridization with domesticated conspecifics on alternative reproductive phenotypes in male Atlantic salmon in multiple temperature regimes. Can. J. Fish. Aquat. Sci. 72, 1–8 (2015).

    Article  Google Scholar 

  20. Debes, P. V. & Hutchings, J. A. Effects of domestication on parr maturity, growth, and vulnerability to predation in Atlantic salmon. Can. J. Fish. Aquat. Sci. 71, 1371–1384 (2014).

    Article  Google Scholar 

  21. McGinnity, P. et al. Genetic impact of escaped farmed Atlantic salmon (Salmo salar L.) on native populations: use of DNA profiling to assess freshwater performance of wild, farmed, and hybrid progeny in a natural river environment. ICES J. Mar. Sci. 54, 998–1008 (1997).

    Google Scholar 

  22. McGinnity, P. et al. Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proc. R. Soc. B 270, 2443–2450 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Fleming, I. A. et al. Lifetime success and interactions of farm salmon invading a native population. Proc. R. Soc. B 267, 1517–1523 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Skaala, O. et al. Performance of farmed, hybrid, and wild Atlantic salmon (Salmo salar) families in a natural river environment. Can. J. Fish. Aquat. Sci. 69, 1994–2006 (2012).

    Article  Google Scholar 

  25. Legendre, S. in Evolutionary Conservation Biology (eds Ferrière, R., Dieckmann, U. & Couvet, D. ) 41–58 (Cambridge Univ. Press, 2005).

    Google Scholar 

  26. Jonsson, N., Hansen, L. P. & Jonsson, B. Variation in age, size and repeat spawning of adult Atlantic salmon in relation to river discharge. J. Anim. Ecol. 60, 937–947 (1991).

    Article  Google Scholar 

  27. Hutchings, J. A. & Jones, M. E. B. Life history variation and growth rate thresholds for maturity in Atlantic salmon, Salmo salar. Can. J. Fish. Aquat. Sci. 55 (suppl.), 22–47 (1998).

    Article  Google Scholar 

  28. Fleming, I. A., Jonsson, B., Gross, M. R. & Lamberg, A. An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). J. Appl. Ecol. 33, 893–905 (1996).

    Article  Google Scholar 

  29. Jonsson, B., Jonsson, N. & Albretsen, J. Environmental change influences the life history of salmon Salmo salar in the North Atlantic Ocean. J. Fish Biol. 88, 618–637 (2016).

    Article  CAS  PubMed  Google Scholar 

  30. Beamish, R. J., Mahnken, C. & Neville, C. M. Evidence that reduced early marine growth is associated with lower marine survival of coho salmon. Trans. Am. Fish. Soc. 133, 26–33 (2004).

    Article  Google Scholar 

  31. Hansen, L. P., Jonsson, B., Morgan, R. I. G. & Thorpe, J. E. Influence of parr maturity on emigration of smolting Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 46, 410–415 (1989).

    Article  Google Scholar 

  32. Clifford, S. L., McGinnity, P. & Ferguson, A. Genetic changes in Atlantic salmon (Salmo salar) populations of northwest Irish rivers resulting from escapes of adult farm salmon. Can. J. Fish. Aquat. Sci. 55, 358–363 (1998).

    Article  Google Scholar 

  33. Crozier, W. W. Escaped farmed salmon, Salmo salar L., in the Glenarm River, Northern Ireland: genetic status of the wild population 7 years on. Fish. Manage. Ecol. 7, 437–446 (2000).

    Article  Google Scholar 

  34. Skaala, O., Wennevik, V. & Glover, K. A. Evidence of temporal genetic change in wild Atlantic salmon, Salmo salar L., populations affected by farm escapees. ICES J. Mar. Sci. 63, 1224–1233 (2006).

    Article  CAS  Google Scholar 

  35. Bourret, V., O’Reilly, P. T., Carr, J. W., Berg, P. R. & Bernatchez, L. Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees. Heredity 106, 500–510 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Glover, K. A. et al. Three decades of farmed escapees in the wild: a spatio-temporal analysis of Atlantic salmon population genetic structure throughout Norway. PLoS ONE 7, e43129 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Report of the Working Group on North Atlantic Salmon (WGNAS) ICES CM 2016/ACOM:10 (ICES 2016).

  38. Skilbrei, O. T., Heino, M. & Svasand, T. Using simulated escape events to assess the annual numbers and destinies of escaped farmed Atlantic salmon of different life stages from farm sites in Norway. ICES J. Mar. Sci. 72, 670–685 (2015).

    Article  Google Scholar 

  39. Gjedrem, T., Gjøen, H. M. & Gjerde, B. Genetic origin of Norwegian farmed Atlantic salmon. Aquaculture 98, 41–50 (1991).

    Article  Google Scholar 

  40. Bourret, V. et al. SNP-array reveals genome-wide patterns of geographical and potential adaptive divergence across the natural range of Atlantic salmon (Salmo salar). Mol. Ecol. 22, 532–551 (2013).

    Article  CAS  PubMed  Google Scholar 

  41. Baskett, M. L., Burgess, S. C. & Waples, R. S. Assessing strategies to minimize unintended fitness consequences of aquaculture on wild populations. Evol. Appl. 6, 1090–1108 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Baskett, M. L. & Waples, R. S. Evaluating alternative strategies for minimizing unintended fitness consequences of cultured individuals on wild populations. Conserv. Biol. 27, 83–94 (2013).

    Article  PubMed  Google Scholar 

  43. Huisman, J. & Tufto, J. Comparison of non-Gaussian quantitative genetic models for migration and stabilizing selection. Evolution 66, 3444–3461 (2012).

    Article  PubMed  Google Scholar 

  44. Karlsson, S., Diserud, O. H., Moen, T. & Hindar, K. A standardized method for quantifying unidirectional genetic introgression. Ecol. Evol. 4, 3256–3263 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Fraser, D. J. et al. Consequences of farmed-wild hybridization across divergent wild populations and multiple traits in salmon. Ecol. Appl. 20, 935–953 (2010).

    Article  PubMed  Google Scholar 

  46. Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015).

    Article  CAS  PubMed  Google Scholar 

  47. Schindler, D. E. et al. Population diversity and the portfolio effect in an exploited species. Nature 465, 609–612 (2010).

    Article  CAS  PubMed  Google Scholar 

  48. The State of World Fisheries and Aquaculture 2016. Contributing to Food Security and Nutrition for All (FAO, 2016).

  49. Naylor, R. et al. Fugitive salmon: assessing the risks of escaped fish from net-pen aquaculture. Bioscience 55, 427–437 (2005).

    Article  Google Scholar 

  50. Jensen, A. J. (ed.) Geographical Variation and Population Trends in Norwegian Atlantic Salmon (NINA, 2004).

    Google Scholar 

  51. Karlsson, S., Moen, T., Lien, S., Glover, K. A. & Hindar, K. Generic genetic differences between farmed and wild Atlantic salmon identified from a 7K SNP-chip. Mol. Ecol. Resour. 11, 247–253 (2011).

    Article  PubMed  Google Scholar 

  52. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Nielsen, E. E., Bach, L. A. & Kotlicki, P. HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol. Ecol. Notes 6, 971–973 (2006).

    Article  Google Scholar 

  54. Report of the Workshop on Age Determination of Salmon (WKADS) ICES CM 2011/ACOM:44 (ICES, 2011).

  55. Lund, R. A. & Hansen, L. P. Identification of wild and reared Atlantic salmon, Salmo salar L., using scale characters. Aquacult. Res. 22, 499–508 (1991).

    Article  Google Scholar 

  56. Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2003).

    Google Scholar 

  57. Kristensen, K., Nielsen, A., Berg, C. W., Skaug, H. & Bell, B. M. TMB: automatic differentiation and laplace approximation. J. Stat. Softw. 70, JSSv070i05 (2016).

    Article  Google Scholar 

  58. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016).

  59. Bates, D., Machler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, JSSv076i01 (2015).

    Article  Google Scholar 

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Acknowledgements

We thank G. M. Østborg and J. G. Jensås for scale reading, T. Balstad, L. B. Eriksen and M. H. Spets for genetic analyses and J. D. Linnell for discussion. The study was financed by the Research Council of Norway (grant 216105, QuantEscape), the Norwegian Environment Agency and the Norwegian Institute for Nature Research.

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G.H.B., K.H., O.H.D. and S.K. conceived the study. S.K. and O.H.D. generated and conducted bioinformatics on the molecular data. K.H., H.S., P.F., A.J.J., K.U., T.F.N., B.T.B., B.F.-L., H.L. and E.N. coordinated the collection of phenotypic data. G.H.B. analysed the data. G.H.B., K.H., G.R., B.J. and S.K. wrote the manuscript. All authors read and commented on the manuscript.

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Correspondence to Geir H. Bolstad.

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The authors declare no competing financial interests.

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Supplementary Figures 1,2; Supplementary Tables 1–4; Supplementary Methods; Supplementary References (PDF 484 kb)

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Bolstad, G., Hindar, K., Robertsen, G. et al. Gene flow from domesticated escapes alters the life history of wild Atlantic salmon. Nat Ecol Evol 1, 0124 (2017). https://doi.org/10.1038/s41559-017-0124

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