Adaptation of a globally important coccolithophore to ocean warming and acidification

Schlüter, Lothar; Lohbeck, Kai T.; Gutowska, Magdalena A.; Gröger, Joachim Paul; Riebesell, Ulf; Reusch, Thorsten B. H.

doi:10.1038/nclimate2379

Cited by 208 publications

(251 citation statements)

References 47 publications

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“…A small number of experiments have investigated the plastic and evolutionary responses to multiple drivers thus far (7,(9)(10)(11)(12). These studies consistently show that both plastic and evolutionary responses to pairs of drivers differ from responses to either single driver.…”

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confidence: 99%

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Brennan

Colegrave

Collins

2017

Proc. Natl. Acad. Sci. U.S.A.

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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.

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confidence: 99%

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Brennan

Colegrave

Collins

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In addition to being an experimental manipulation method, the dilution treatment can be useful for other applications, such as long-term phytoplankton evolution experiments. In these experiments, researchers use semicontinuous culturing approaches where each new culture is established as a (diluted) inoculum of the former (Lohbeck et al, 2012;Schlüter et al, 2014). For these types of experiments, the tested levels of dilution allow to estimate the potential loss of genotypes at each step.…”

Section: Effects Of Dilutionmentioning

confidence: 99%

Manipulation of Non-random Species Loss in Natural Phytoplankton: Qualitative and Quantitative Evaluation of Different Approaches

et al. 2017

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Ecological research in recent decades revealed that species loss has a predominantly negative effect on ecosystem functioning and stability. Most of these studies were based on random species loss scenarios, but extinctions in nature are not random. Recent experimental studies using macroscopic communities largely advanced knowledge about the effects of non-random species loss. However, in microscopic communities like the phytoplankton, implementing realistic species loss scenarios is challenging and experimental data are scarce. Creating more realistic experiments to study the role of phytoplankton diversity for ecosystem functioning is particularly important, as they provide up to 50% of global primary productivity, form the basis of all pelagic food webs, and are important for biogeochemical cycling. In this study, we experimentally tested and evaluated three methods for non-random species loss in a natural marine phytoplankton community. Dilution, filtration, and heat stress removed the targeted rare, large, and sensitive species, respectively. All these species groups are extremely vulnerable to extinction in future climate scenarios and play important roles in the communities. Dilution and filtration with a fine mesh additionally decreased initial biomass, which increased the variability of species left in the respective replicates. The methods tested in this study can be used to non-randomly manipulate phytoplankton species diversity in communities used for experiments. However, in studies where species identities are more important than species richness, the dilution and filtration methods should be modified to eliminate the effect of decreasing initial biomass.

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“…Second, there is evolutionary adaptation through mutation that changes genotypes. Evolution by mutation in phytoplankton reared in laboratory conditions over hundreds to thousands of generations has been documented in several studies (Collins and Bell, 2004;Collins et al, 2006;Collins, 2011;Lohbeck et al, 2012;Schlüter et al, 2014). The speed of evolutionary adaptation is expected to be inversely proportional to generation time: most microbes in the ocean have generation times of a day or less, so experience thousands of generations in a decade.…”

Section: Introductionmentioning

confidence: 99%

“…The objective of this paper is to develop a model at the trait level of genetic mutation by the coccolithophorid Emiliania huxleyi based on observations taken over 4 years of laboratory culture experiments (Schlüter et al, 2014). Litchman and Klausmeier (2008) and Litchman et al (2012) described a framework for a trait-based approach to investigate the evolutionary responses of phytoplankton to global environmental change.…”

Section: Introductionmentioning

confidence: 99%

“…Several laboratories have grown phytoplankton cultures for hundreds to thousands of generations and demonstrated that they have changed genetic makeup. In particular Schlüter et al (2014) grew replicates derived from a single cell of Emiliania huxleyi, a coccolithophorid with broad geographical and thermal range, for 3 years (∼1250 generations) at 15 • C, and then for a year at 26.3 • C, near their upper thermal limit. During the last year the intrinsic growth rate increased more or less linearly, which the authors attribute to genetic mutation.…”

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confidence: 99%

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A Model Simulation of the Adaptive Evolution through Mutation of the Coccolithophore Emiliania huxleyi Based on a Published Laboratory Study

Denman

2017

Front. Mar. Sci.

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We expect the structure and functioning of marine ecosystems to change over this century in response to changes in key ocean variables associated with a changing climate. Organisms with generation times from years to decades have the capacity to adapt to changing environmental conditions over a few generations by selecting from existing genotypes/phenotypes, but it is unlikely that evolution through mutation will be a major factor for organisms with generation times of years to decades. However, phytoplankton and other microbes, with generation times of days or less, experience hundreds of generations each year, allowing the possibility for favorable mutations (i.e., those that produce organisms with fitness maxima nearer to the environmental conditions at that time) to dominate existing genotypes and survive in a changing climate. Several laboratories have grown phytoplankton cultures for hundreds to thousands of generations and demonstrated that they have changed genetic makeup. In particular Schlüter et al. (2014) grew replicates derived from a single cell of Emiliania huxleyi, a coccolithophorid with broad geographical and thermal range, for 3 years (∼1250 generations) at 15 • C, and then for a year at 26.3 • C, near their upper thermal limit. During the last year the intrinsic growth rate increased more or less linearly, which the authors attribute to genetic mutation. Here we simulate genetic mutation of a single trait (intrinsic growth rate), both for the control phase and the warm phase of their study. We consider sensitivities to frequency of mutation, changes with temperature in intrinsic growth rate, and use the experimental setup and results to place constraints on the way mutations occur. In particular, all numerical experiments with mutation result in a lag time ∼30-140 generations before a significant increase in realized growth rate occurs. This lag after a favorable mutation results from the number of generations required for a single favorable mutant cell to reach a significant fraction of the ∼10 5 cells in the culture. A numerical experiment that includes a simple plastic response formulation shows that plasticity could remove this lag and yield results more in agreement with those observed in the laboratory study.

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Adaptation of a globally important coccolithophore to ocean warming and acidification

Cited by 208 publications

References 47 publications

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Evolutionary consequences of multidriver environmental change in an aquatic primary producer

Manipulation of Non-random Species Loss in Natural Phytoplankton: Qualitative and Quantitative Evaluation of Different Approaches

A Model Simulation of the Adaptive Evolution through Mutation of the Coccolithophore Emiliania huxleyi Based on a Published Laboratory Study

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