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Research Article

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Georgina L. Brennan, Nick Colegrave, and View ORCID ProfileSinéad Collins
PNAS first published August 28, 2017; https://doi.org/10.1073/pnas.1703375114
Georgina L. Brennan
aAshworth Laboratories, University of Edinburgh, Edinburgh, EH9 3FL, United Kingdom;
bMolecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor University, Bangor LL57 2UW, United Kingdom
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Nick Colegrave
aAshworth Laboratories, University of Edinburgh, Edinburgh, EH9 3FL, United Kingdom;
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Sinéad Collins
aAshworth Laboratories, University of Edinburgh, Edinburgh, EH9 3FL, United Kingdom;
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  • ORCID record for Sinéad Collins
  • For correspondence: s.collins@ed.ac.uk
  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved July 28, 2017 (received for review February 27, 2017)

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Significance

Our understanding of how primary producers at the base of aquatic ecosystems respond to complex environmental change currently depends on studies using few environmental drivers, or scenarios where drivers covary. However, we lack a general understanding of evolution in multidriver environments. We evolve a microbial primary producer in 96 different multidriver environments and find that evolutionary responses in growth are largely driven by a few drivers but that the intensity of selection is, on average, higher in multidriver environments. Functional traits (cell size, chlorophyll content) often revert to ancestral values during adaptation in multidriver environments. This expands the framework for understanding how microbial primary producers evolve under global change and the potential ramifications for their function in aquatic ecosystems.

Abstract

Climate change is altering aquatic environments in a complex way, and simultaneous shifts in many properties will drive evolutionary responses in primary producers at the base of both freshwater and marine ecosystems. So far, evolutionary studies have shown how changes in environmental drivers, either alone or in pairs, affect the evolution of growth and other traits in primary producers. Here, we evolve a primary producer in 96 unique environments with different combinations of between one and eight environmental drivers to understand how evolutionary responses to environmental change depend on the identity and number of drivers. Even in multidriver environments, only a few dominant drivers explain most of the evolutionary changes in population growth rates. Most populations converge on the same growth rate by the end of the evolution experiment. However, populations adapt more when these dominant drivers occur in the presence of other drivers. This is due to an increase in the intensity of selection in environments with more drivers, which are more likely to include dominant drivers. Concurrently, many of the trait changes that occur during the initial short-term response to both single and multidriver environmental change revert after about 450 generations of evolution. In future aquatic environments, populations will encounter differing combinations of drivers and intensities of selection, which will alter the adaptive potential of primary producers. Accurately gauging the intensity of selection on key primary producers will help in predicting population size and trait evolution at the base of aquatic food webs.

  • multiple environmental drivers
  • adaptation
  • microbial evolution
  • Chlamydomonas
  • ocean global change biology

Footnotes

  • ↵1To whom correspondence should be addressed. Email: s.collins{at}ed.ac.uk.
  • Author contributions: G.L.B., N.C., and S.C. designed research; G.L.B. performed research; G.L.B. and S.C. analyzed data; and G.L.B., N.C., and S.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The R codes and data reported in this paper have been deposited in the PANGAEA database, www.pangaea.de (doi: PANGAEA.879517).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1703375114/-/DCSupplemental.

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Evolution in multidriver environments
Georgina L. Brennan, Nick Colegrave, Sinéad Collins
Proceedings of the National Academy of Sciences Aug 2017, 201703375; DOI: 10.1073/pnas.1703375114

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Evolution in multidriver environments
Georgina L. Brennan, Nick Colegrave, Sinéad Collins
Proceedings of the National Academy of Sciences Aug 2017, 201703375; DOI: 10.1073/pnas.1703375114
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