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.

Eutrophication causes speciation reversal in whitefish adaptive radiations

Abstract

Species diversity can be lost through two different but potentially interacting extinction processes: demographic decline and speciation reversal through introgressive hybridization. To investigate the relative contribution of these processes, we analysed historical and contemporary data of replicate whitefish radiations from 17 pre-alpine European lakes and reconstructed changes in genetic species differentiation through time using historical samples. Here we provide evidence that species diversity evolved in response to ecological opportunity, and that eutrophication, by diminishing this opportunity, has driven extinctions through speciation reversal and demographic decline. Across the radiations, the magnitude of eutrophication explains the pattern of species loss and levels of genetic and functional distinctiveness among remaining species. We argue that extinction by speciation reversal may be more widespread than currently appreciated. Preventing such extinctions will require that conservation efforts not only target existing species but identify and protect the ecological and evolutionary processes that generate and maintain species.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Distribution of historical whitefish diversity and recent diversity loss.
Figure 2: Diversity loss through speciation reversal.
Figure 3: Whitefish diversity explained by environmental variables.

References

  1. Chapin, F. S. et al. Consequences of changing biodiversity. Nature 405, 234–242 (2000)

    Article  CAS  PubMed  Google Scholar 

  2. Rosenzweig, M. L. Loss of speciation rate will impoverish future diversity. Proc. Natl Acad. Sci. USA 98, 5404–5410 (2001)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. Rhymer, J. M. & Simberloff, D. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27, 83–109 (1996)

    Article  Google Scholar 

  4. Seehausen, O. Losing biodiversity by reverse speciation. Curr. Biol. 16, R334––R337 (2006)

    Article  PubMed  Google Scholar 

  5. Seehausen, O., Van Alphen, J. J. M. & Witte, F. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277, 1808–1811 (1997)

    Article  CAS  Google Scholar 

  6. Taylor, E. B. et al. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol. Ecol. 15, 343–355 (2006)

    Article  CAS  PubMed  Google Scholar 

  7. Grant, B. R. & Grant, P. R. Fission and fusion of Darwin’s finches populations. Proc. R. Soc. B 363, 2821–2829 (2008)

    Google Scholar 

  8. Gilman, R. T. & Behm, J. E. Hybridization, species collapse, and species reemergence after disturbance to premating mechanisms of reproductive isolation. Evolution 65, 2592–2605 (2011)

    Article  PubMed  Google Scholar 

  9. Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, 2000)

    Google Scholar 

  10. Coyne, J. A. & Orr, H. A. Speciation (Sinauer Associates, 2004)

    Google Scholar 

  11. Rundle, H. D. & Nosil, P. Ecological speciation. Ecol. Lett. 8, 336–352 (2005)

    Article  Google Scholar 

  12. Schluter, D. Evidence for ecological speciation and its alternative. Science 323, 737–741 (2009)

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Servedio, M. R. et al. Magic traits in speciation: ‘magic’ but not rare? Trends Ecol. Evol. 26, 389–397 (2011)

    Article  PubMed  Google Scholar 

  14. Hendry, A. P. et al. Possible human impacts on adaptive radiation: beak size bimodality in Darwin's finches. Proc. R. Soc. B 273, 1887–1894 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  15. De León, L. F. et al. Exploring possible human influences on the evolution of Darwin’s finches. Evolution. 65, 2258–2272 (2011)

    Article  PubMed  Google Scholar 

  16. Schluter, D. Ecological speciation in postglacial fishes. Proc. R. Soc.. B 351, 807–814 (1996)

    Google Scholar 

  17. Rundle, H. D., Nagel, L., Boughman, J. W. & Schluter, D. Natural selection and parallel speciation in sympatric sticklebacks. Science 287, 306–308 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Hudson, A. G., Vonlanthen, P. & Seehausen, O. Rapid parallel adaptive radiations from a single hybridogenic ancestral population. Proc. R. Soc. B 278, 58–66 (2011)

    Article  PubMed  Google Scholar 

  19. Bernatchez, L. in Evolution Illuminated (eds Hendry, A. P. & Stearns, S. C. ) 175–207 (Oxford Univ. Press, 2004)

    Google Scholar 

  20. McPhail, J. D. Ecology and evolution of sympatric sticklebacks (Gasterosteus)—origin of the species pairs. Can. J. Zool. 71, 515–523 (1993)

    Article  Google Scholar 

  21. Kottelat, M. & Freyhof, J. Handbook of European Freshwater Fishes (Kottelat, Cornol and Freyhof, 2007)

    Google Scholar 

  22. Steinmann, P. Monographie der schweizerischen koregonen. Beitrag zum problem der entstehung neuer arten. Spezieller teil. Schweiz. Z. Hydrobiol. 12, 340–491 (1950)

    Google Scholar 

  23. Vonlanthen, P. et al. Divergence along a steep ecological gradient in lake whitefish (Coregonus sp.). J. Evol. Biol. 22, 498–514 (2009)

    Article  CAS  PubMed  Google Scholar 

  24. Woods, P. J., Müller, R. & Seehausen, O. Intergenomic epistasis causes asynchronous hatch times in whitefish hybrids, but only when parental ecotypes differ. J. Evol. Biol. 22, 2305–2319 (2009)

    Article  CAS  PubMed  Google Scholar 

  25. Müller, R. & Stadelmann, P. Fish habitat requirements as the basis for rehabilitation of eutrophic lakes by oxygenation. Fish. Mgmt. Ecol. 11, 251–260 (2004)

    Article  Google Scholar 

  26. Verschuren, D. et al. History and timing of human impact on Lake Victoria, East Africa. Proc. R. Soc. B 269, 289–294 (2002)

    Article  PubMed  PubMed Central  Google Scholar 

  27. Smith, V. H. & Schindler, D. W. Eutrophication science: where do we go from here? Trends Ecol. Evol. 24, 201–207 (2009)

    Article  PubMed  Google Scholar 

  28. Straile, D. & Geller, W. The response of Daphnia to changes in trophic status and weather patterns: a case study from Lake Constance. ICES J. Mar. Sci. 55, 775–782 (1998)

    Article  Google Scholar 

  29. Jeppesen, E., Jensen, J. P., Søndergaard, M., Lauridsen, T. & Landkildehus, F. Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshwat. Biol. 45, 201–218 (2000)

    Article  CAS  Google Scholar 

  30. Blumenshine, S. C., Vadeboncoeur, Y., Lodge, D. M., Cottingham, K. L. & Knight, S. E. Benthic-pelagic links: responses of benthos to water-column nutrient enrichment. J. N. Am. Benthol. Soc. 16, 466–479 (1997)

    Article  Google Scholar 

  31. Powers, S. P. et al. Effects of eutrophication on bottom habitat and prey resources of demersal fishes. Mar. Ecol. Prog. Ser. 302, 233–243 (2005)

    Article  ADS  Google Scholar 

  32. Waples, R. S. & Do, C. Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol. Appl. 3, 244–262 (2010)

    Article  PubMed  Google Scholar 

  33. Bittner, D., Excoffier, L. & Largiader, C. R. Patterns of morphological changes and hybridization between sympatric whitefish morphs (Coregonus spp.) in a Swiss lake: a role for eutrophication? Mol. Ecol. 19, 2152–2167 (2010)

    Article  CAS  PubMed  Google Scholar 

  34. Seehausen, O. et al. Speciation through sensory drive in cichlid fish. Nature 455, 620–623 (2008)

    Article  ADS  CAS  PubMed  Google Scholar 

  35. Heath, D., Bettles, C. M. & Roff, D. Environmental factors associated with reproductive barrier breakdown in sympatric trout populations on Vancouver Island. Evol. Appl. 3, 77–90 (2010)

    Article  PubMed  Google Scholar 

  36. Brede, N. et al. The impact of human-made ecological changes on the genetic architecture of Daphnia species. Proc. Natl Acad. Sci. USA 106, 4758–4763 (2009)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  37. Harmon, L. J. et al. Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458, 1167–1170 (2009)

    Article  ADS  CAS  PubMed  Google Scholar 

  38. Goldschmidt, T., Witte, F. & Wanink, J. Cascading effects of the introduced Nile perch on the detritivorous phytoplanktivorous species in the sublittoral areas of Lake Victoria. Conserv. Biol. 7, 686–700 (1993)

    Article  Google Scholar 

  39. Seehausen, O. Speciation affects ecosystems. Nature 458, 1122–1123 (2009)

    Article  ADS  CAS  PubMed  Google Scholar 

  40. Faith, D. P. et al. Evosystem services: an evolutionary perspective on the links between biodiversity and human well-being. Curr. Opin. Env. Sust. 2, 1–9 (2010)

    Article  Google Scholar 

  41. 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 

  42. Liechti, P. Der Zustand der Seen in der Schweiz (Schriftenreihe Umwelt Nr. 237; Bundesamt für Umwelt, Wald und Landschaft, 1994)

    Google Scholar 

  43. Müller, R. Trophic state and its implications for natural reproduction of salmonid fish. Hydrobiologia 243, 261–268 (1992)

    Article  Google Scholar 

  44. Harrod, C., Mallela, J. & Kahilainen, K. K. Phenotype-environment correlations in a putative whitefish adaptive radiation. J. Anim. Ecol. 79, 1057–1068 (2010)

    Article  PubMed  Google Scholar 

  45. Latch, E. K., Dharmarajan, G., Glaubitz, J. C. & Rhodes, O. E. Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv. Genet. 7, 295–302 (2006)

    Article  Google Scholar 

  46. Wasko, A. P., Martins, C., Oliveira, C. & Foresti, F. Non-destructive genetic sampling in fish. An improved method for DNA extraction from fish fins and scales. Hereditas 138, 161–165 (2003)

    Article  PubMed  Google Scholar 

  47. Czerkies, P., Kordalski, K., Golas, T., Krysinski, D. & Luczynski, M. Oxygen requirements of whitefish and vendace (Coregoninae) embryos at final stages of their development. Aquaculture 211, 375–385 (2002)

    Article  Google Scholar 

Download references

Acknowledgements

We thank all professional fishermen who provided fish specimens. We thank M. Kugler from the Amt für Natur, Jagd und Fischerei, St. Gallen and the institute of Seenforschung and Fischereiwesen Langenargen for providing historical whitefish scales from Lake Constance. We acknowledge the Swiss Federal Institute for Aquatic Science and Technology (EAWAG), the Internationale Gewässerschutzkomission für den Bodensee (IGKB) and the Federal Office for Environment (FOEN) for providing environmental data. We also thank G. Périat, S. Mwaiko, M. Barluenga, H. Araki, M. Maan, J. Brodersen, P. Nosil, K. Wagner and all members of the Fish Ecology and Evolution laboratory for assistance in the laboratory, and for comments and suggestions on the manuscript, B. Müller for help with the analysis of the oxygen profiles, and C. Melian for help with data analyses. We acknowledge financial support by the Eawag Action Field Grant ‘AquaDiverse–understanding and predicting changes in aquatic biodiversity’ (to O.S.).

Author information

Authors and Affiliations

Authors

Contributions

P.V. contributed to conception and design of the study, collected fish, generated gill-raker and contemporary genetic data, and carried out most of the statistical analyses. D.B. collected fish, generated gill-raker, historical and contemporary genetic data. A.G.H. collected fish and generated gill-raker and geometric morphometric data. K.A.Y. participated in designing the study and writing the manuscript. R. M. collected and analysed egg data and contributed to fish collection. B.L.-H. contributed to fish, gill-raker, and genetic data collection. D.R. contributed to analyses and writing. S.D.P. contributed to collection of historical genetic data. C.R.L. supervised parts of sampling, gill-raker counting and contemporary genetic data collection. O.S. conceived and designed the project, supervised the project, and contributed to data analyses. P.V. and O.S. wrote the paper.

Corresponding author

Correspondence to O. Seehausen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data, Supplementary References Supplementary Tables 1-7 and Supplementary Figures 1-7 with legends. (PDF 870 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Vonlanthen, P., Bittner, D., Hudson, A. et al. Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature 482, 357–362 (2012). https://doi.org/10.1038/nature10824

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature10824

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing