Evolution under pH stress and high population densities leads to increased density-dependent fitness in the protist Tetrahymena thermophila.


Journal

Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224

Informations de publication

Date de publication:
03 2020
Historique:
received: 04 09 2019
accepted: 12 12 2019
pubmed: 17 1 2020
medline: 7 2 2021
entrez: 17 1 2020
Statut: ppublish

Résumé

Abiotic stress is a major force of selection that organisms are constantly facing. While the evolutionary effects of various stressors have been broadly studied, it is only more recently that the relevance of interactions between evolution and underlying ecological conditions, that is, eco-evolutionary feedbacks, have been highlighted. Here, we experimentally investigated how populations adapt to pH-stress under high population densities. Using the protist species Tetrahymena thermophila, we studied how four different genotypes evolved in response to stressfully low pH conditions and high population densities. We found that genotypes underwent evolutionary changes, some shifting up and others shifting down their intrinsic rates of increase (r

Identifiants

pubmed: 31944293
doi: 10.1111/evo.13921
doi:

Banques de données

Dryad
['10.5061/dryad.mpg4f4qvg']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

573-586

Subventions

Organisme : University of Zürich: University Research Priority Program Evolution In Action
Pays : International
Organisme : H2020 European Research Council
ID : 739874
Pays : International
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : 31003A_172887
Pays : International
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : PP00P3_179089
Pays : International

Informations de copyright

© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.

Références

Altermatt, F., E. A. Fronhofer, A. Garnier, A. Giometto, F. Hammes, J. Klecka, D. Legrand, E. Mächler, T. M. Massie, F. Pennekamp, et al. 2015. Big answers from small worlds: a user's guide for protist microcosms as a model system in ecology and evolution. Methods Ecol. Evol. 6:218-231.
Andrews, J. H., and D. I. Rouse. 1982. Plant pathogens and the theory of r- and K-Selection. Am. Nat. 120:283-296.
Angilletta, M. J. 2009. Thermal adaptation: a theoretical and empirical synthesis. Oxford Univ. Press, Oxford, U.K.
Bell, G., and A. Gonzalez. 2011. Adaptation and evolutionary rescue in metapopulations experiencing environmental deterioration. Science 332:1327-1330.
Beverton, R., and S. Holt. 1993. On the dynamics of exploited fish populations. Springer, Berlin, Germany.
Bijlsma, R., and V. Loeschcke. 2005. Environmental stress, adaptation and evolution: an overview. J. Evol. Biol. 18:744-749.
Blount, Z. D., R. E. Lenski, and J. B. Losos. 2018. Contingency and determinism in evolution: replaying life's tape. Science 362:eaam5979.
Bolnick, D. I., R. D. H. Barrett, K. B. Oke, D. J. Rennison, and Y. E. Stuart. 2018. (Non)Parallel Evolution. Pp. 303-330. in D. J. Futuyma, ed. Annual Review of Ecology, Evolution, and Systematics. Vol. 49. Annual Reviews, Palo Alto, CA.
Bono, L. M., L. B. Smith, D. W. Pfennig, and C. L. Burch. 2017. The emergence of performance trade-offs during local adaptation: insights from experimental evolution. BMC Mol. Biol. 26:1720-1733.
Bridle, J. R., and T. H. Vines. 2007. Limits to evolution at range margins: when and why does adaptation fail? Trends Ecol. Evol. 22:140-147.
Brito, P. H., E. Guilherme, H. Soares, and I. Gordo. 2010. Mutation accumulation in Tetrahymena. BMC Evol. Biol. 10:354.
Burns, D. A., J. Aherne, D. A. Gay, and C. M. B. Lehmann. 2016. Acid rain and its environmental effects: Recent scientific advances. Atmos. Environ. 146:1-4.
Caldeira, K., and M. E. Wickett. 2003. Anthropogenic carbon and ocean pH. Nature 425:365.
Cassidy-Hanley, D. M. 2012. Tetrahymena in the laboratory: strain resources, methods for culture, maintenance, and storage. Pp. 237-276. in Methods in cell biology. Vol. 109. Elsevier, Amsterdam, the Netherlands.
Clobert, J., M. Baguette, T. G. Benton, and J. M. Bullock. 2012. Dispersal ecology and evolution. 1st ed. Oxford Univ. Press, Oxford, U.K.
Clobert, J., E. Danchin, A. A. Dhondt, and J. D. Nichols. 2001. Dispersal. Oxford Univ. Press, Oxford, U.K.
Collins, K. 2012. Tetrahymena thermophila. Academic Press, Cambridge, MA.
Collins, S., and G. Bell. 2004. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566.
Coyne, R. S., N. A. Stovert, and W. Miao. 2012. Whole Genome Studies of Tetrahymena. Pp. 53-81. in K. Collins, ed. Tetrahymena thermophila. . Vol. 109. Elsevier Academic Press, San Diego, CA.
Derry, A. M., and S. E. Arnott. 2007. Adaptive reversals in acid tolerance in copepods from lakes recovering from historical stress. Ecol. Appl. 17:1116-1126.
Dunson, W., and J. Travis. 1991. The role of abiotic factors in community organization. Am. Nat. 138:1067-1091.
Fjerdingstad, E. J., N. Schtickzelle, P. Manhes, A. Gutierrez, and J. Clobert. 2007. Evolution of dispersal and life history strategies-Tetrahymena ciliates. BMC Evol. Biol. 7:133.
Fletcher, E., A. Feizi, M. M. M. Bisschops, B. M. Hallström, S. Khoomrung, V. Siewers, and J. Nielsen. 2017. Evolutionary engineering reveals divergent paths when yeast is adapted to different acidic environments. Metab. Eng. 39:19-28.
Flowers, T. J., H. K. Galal, and L. Bromham. 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biol. 37:604-612.
Franks, S. J., and A. A. Hoffmann. 2012. Genetics of Climate Change Adaptation. Pp. 185-208. in B. L. Bassler, ed. Annual Review of Genetics. Vol. 46. Annual Reviews, Palo Alto, CA.
Fraser, D. J., L. K. Weir, L. Bernatchez, M. M. Hansen, and E. B. Taylor. 2011. Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106:404-420.
Fronhofer, E. A., and F. Altermatt. 2015. Eco-evolutionary feedbacks during experimental range expansions. Nat. Commun. 6:6844.
Fronhofer, E. A., L. Govaert, M. I. O'Connor, S. J. Schreiber, and F. Altermatt. 2018. The shape of density dependence and the relationship between population growth, intraspecific competition and equilibrium population density. bioRxiv P. 485946.
Fronhofer, E. A., N. Nitsche, and F. Altermatt. 2017. Information use shapes the dynamics of range expansions into environmental gradients. Glob. Ecol. Biogeogr. 26:400-411.
Gallet, R., Y. Latour, B. S. Hughes, and T. Lenormand. 2014. The dynamics of niche evolution upon abrupt environmental change. Evolution 68:1257-1269.
Gattuso, J.-P., and L. Hansson. 2011. Ocean acidification. Oxford Univ. Press, Oxford, U.K.
Gelman, A., J. Hwang, and A. Vehtari. 2014. Understanding predictive information criteria for Bayesian models. Stat. Comput. 24:997-1016.
Govaert, L., E. A. Fronhofer, S. Lion, C. Eizaguirre, D. Bonte, M. Egas, A. P. Hendry, A. D. B. Martins, C. J. Melián, J. A. M. Raeymaekers, et al. 2019. Eco-evolutionary feedbacks-theoretical models and perspectives. Funct. Ecol. 33:13-30.
Gunde-Cimerman, N., A. Oren, and A. Plemenitaš. 2006. Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer Science & Business Media, Berlin, Germany.
Hangartner, S., A. Laurila, and K. Räsänen. 2011. Adaptive divergence of the moor frog (Rana arvalis) along an acidification gradient. BMC Evol. Biol. 11:366.
Harden, M. M., A. He, K. Creamer, M. W. Clark, I. Hamdallah, K. A. Martinez, R. L. Kresslein, S. P. Bush, and J. L. Slonczewski. 2015. Acid-adapted strains of Escherichia coli K-12 obtained by experimental evolution. Appl. Environ. Microbiol. 81:1932-1941.
Harmand, N., R. Gallet, G. Martin, and T. Lenormand. 2018. Evolution of bacteria specialization along an antibiotic dose gradient. Evol. Lett. 2:221-232.
Hendry, A. P. 2016. Eco-evolutionary dynamics. Princeton Univ. Press, Princeton, U.K.
HilleRisLambers, J., P. B. Adler, W. S. Harpole, J. M. Levine, and M. M. Mayfield. 2012. Rethinking community assembly through the lens of coexistence theory. Pp. 227-248. in D. J. Futuyma, ed. Annual review of ecology, evolution, and systematics. Vol. 43. Annual Reviews, Palo Alto, CA.
Hoffmann, A. A., and C. M. Sgro. 2011. Climate change and evolutionary adaptation. Nature 470:479-485.
Hughes, B. S., A. J. Cullum, and A. F. Bennett. 2007. Evolutionary adaptation to environmental pH in experimental lineages of Escheria coli. Evolution 61:1725-1734.
Jacob, S., P. Wehi, J. Clobert, D. Legrand, N. Schtickzelle, M. Huet, and A. Chaine. 2016. Cooperation-mediated plasticity in dispersal and colonization. Evolution 70:2336-2345.
Johnston, I. A., A. Clarke, R. M. Laws, and F. Franks. 1990. Cold adaptation in marine organisms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 326:655-667.
Joshi, A., N. G. Prasad, and M. Shakarad. 2001. K-selection, alpha-selection, effectiveness, and tolerance in competition: density-dependent selection revisited. J. Genet. 80:63-75.
Kawecki, T. J., and D. Ebert. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7:1225-1241.
Kelly, M. W., and G. E. Hofmann. 2013. Adaptation and the physiology of ocean acidification. Funct. Ecol. 27:980-990.
Klerks, P. L., and J. S. Weis. 1987. Genetic adaptation to heavy metals in aquatic organisms: a review. Environ. Pollut. 45:173-205.
J Kooyers, N. 2015. The evolution of drought escape and avoidance in natural herbaceous populations. Plant Sci. 234:155-162.
Leimu, R., and M. Fischer. 2008. A meta-a of local adaptation in plants. PLoS One 3:e4010.
Lenski, R. E., and M. Travisano. 1994. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl. Acad. Sci. U.S.A. 91:6808-6814.
Likens, G. E., and F. H. Bormann. 1974. Acid rain: a serious regional environmental problem. Science 184:1176-1179.
Likens, G. E., C. T. Driscoll, and D. C. Buso. 1996. Long-term effects of acid rain: response and recovery of a forest ecosystem. Science 272:244-246.
Lohbeck, K. T., U. Riebesell, and T. B. H. Reusch. 2012. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5:346-351.
S Luckinbill, L. 1978. r and K selection in experimental populations of Escherichia coli. Science 202:1201-1203.
Lytle, D. A., and N. L. Poff. 2004. Adaptation to natural flow regimes. Trends Ecol. Evol. 19:94-100.
McElreath, R. 2015. Statistical rethinking: a Bayesian course with examples in R and Stan. 1st ed. Chapman and Hall/CRC, Boca Raton, FL.
Michel, J., D. Ebert, and M. D. Hall. 2016. The trans-generational impact of population density signals on host-parasite interactions. BMC Evol. Biol. 16.
Mueller, L. D., and F. J. Ayala. 1981. Trade-off between r-selection and K-selection in Drosophila populations. Proc. Natl. Acad. Sci. U.S.A. 78:1303-1305.
Mueller, L. D., P. Z. Guo, and F. J. Ayala. 1991. Density-dependent natural selection and trade-offs in life history traits. Science 253:433-435.
Nørgaard, L. S., B. L. Phillips, and M. D. Hall. 2019. Infection in patchy populations: Contrasting pathogen invasion success and dispersal at varying times since host colonization. Evol. Lett. 3:555-566.
Padfield, D., G. Yvon-Durocher, A. Buckling, S. Jennings, and G. Yvon-Durocher. 2016. Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecol. Lett. 19:133-142.
Pelletier, F., D. Garant, and A. P. Hendry. 2009. Eco-evolutionary dynamics. Proc. R. Soc. B-Biol. Sci. 364:1483-1489.
Pennekamp, F., N. Schtickzelle, and O. L. Petchey. 2015. BEMOVI, software for extracting behavior and morphology from videos, illustrated with analyses of microbes. Ecol. Evol. 5:2584-2595.
Raven, J., K. Caldeira, H. Elderfield, O. Hoegh-Guldberg, P. S. Liss, U. Riebesell, J. Sheperd, C. Turley, and A. Watson. 2005. Ocean acidification due to increasing atmospheric carbon dioxide. Royal Society Policy Document.
Reusch, T. B. H., and P. W. Boyd. 2013. Experimental evolution meets marine phytoplankton. Evolution 67:1849-1859.
Reznick, D., M. J. Bryant, and F. Bashey. 2002. r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83:1509-1520.
Rosenbaum, B., M. Raatz, G. Weithoff, G. F. Fussmann, and U. Gaedke. 2019. Estimating parameters from multiple time deries of population dynamics using Bayesian inference. Front. Ecol. Evol. 6:234.
Sanford, E., and M. W. Kelly. 2011. Local adaptation in marine invertebrates. Annu. Rev. Mar. Sci. 3:509-535.
Schlüter, L., K. T. Lohbeck, M. A. Gutowska, J. P. Gröger, U. Riebesell, and T. B. H. Reusch. 2014. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat. Clim. Chang. 4:1024-1030.
Shaw, A. 1994. Adaptation to metals in widespread and endemic plants. Environ. Health Perspect. 102:105-108.
Stearns, S. C. 1977. The evolution of life history traits: a critique of the theory and a review of the data. Annu. Rev. Ecol. Syst. 8:145-171.
Stearns, S. C 1992. The evolution of life histories. Oxford Univ. Press, Oxford, U.K.
Stillman, J. H., and A. W. Paganini. 2015. Biochemical adaptation to ocean acidification. J. Exp. Biol. 218:1946-1955.
Sunday, J. M., P. Calosi, S. Dupont, P. L. Munday, J. H. Stillman, and T. B. H. Reusch. 2014. Evolution in an acidifying ocean. Trends Ecol. Evol. 29:117-125.
Thieme, H. R. 2003. Mathematics in population biology. Princeton Univ. Press, Princeton, U.K.
Westeberhard, M. 1989. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20:249-278.
Wood, T. E., J. M. Burke, and L. H. Rieseberg. 2005. Parallel genotypic adaptation: when evolution repeats itself. Genetica 123:157-170.
Zeebe, R. E., J. C. Zachos, K. Caldeira, and T. Tyrrell. 2008. Carbon emissions and acidification. Science 321:51-52.
Zhang, J., C. Wu, G. Du, and J. Chen. 2012. Enhanced acid tolerance in Lactobacillus casei by adaptive evolution and compared stress response during acid stress. Biotechnol. Bioprocess Eng. 17:283-289.

Auteurs

Felix Moerman (F)

Department of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.
Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, Dübendorf, CH-8600, Switzerland.
ISEM, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France.
Swiss Institute of Bioinformatics, Quartier Sorge-Bâtiment Génopode, Lausanne, 1015, Switzerland.

Angelina Arquint (A)

Department of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.

Stefanie Merkli (S)

Department of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.

Andreas Wagner (A)

Department of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.
Swiss Institute of Bioinformatics, Quartier Sorge-Bâtiment Génopode, Lausanne, 1015, Switzerland.
The Santa Fe Institute, Santa Fe, New Mexico, 87501, USA.

Florian Altermatt (F)

Department of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.
Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, Dübendorf, CH-8600, Switzerland.

Emanuel A Fronhofer (EA)

Department of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.
Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, Dübendorf, CH-8600, Switzerland.
ISEM, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France.

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