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Eutrophication causes speciation reversal in whitefish adaptive radiations

Nature volume 482, pages 357–362 (2012)Cite this article

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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.

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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.

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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

  1. Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland,

    P. Vonlanthen, A. G. Hudson, B. Lundsgaard-Hansen, S. Di Piazza & O. Seehausen

  2. Department of Fish Ecology and Evolution, Centre of Ecology, Evolution and Biogeochemistry, EAWAG Swiss Federal Institute of Aquatic Science and Technology, Seestrasse 79, CH-6047 Kastanienbaum, Switzerland,

    P. Vonlanthen, D. Bittner, A. G. Hudson, K. A. Young, R. Müller, B. Lundsgaard-Hansen, D. Roy, S. Di Piazza & O. Seehausen

  3. Computational and Molecular Population Genetics (CMPG) Laboratory, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland,

    D. Bittner

  4. Environment Agency, Cambria House, Newport Road, Cardiff CF24 0TP, UK,

    K. A. Young

  5. Department of Biology, Dalhousie University, 1355 Oxford Street, Halifax, Nova Scotia B3H 4R2, Canada,

    D. Roy

  6. Institute of Clinical Chemistry, Inselspital University Hospital and University of Bern, Inselspital, CH-3010 Bern, Switzerland,

    C. R. Largiader

Authors
  1. P. Vonlanthen
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  10. O. Seehausen
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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.

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The authors declare no competing financial interests.

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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

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