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Research

Limits to adaptation

In order to mitigate, or even effectively manage, human-induced evolutionary change we must understand what limits the evolutionary potential of populations and what impact this has on biodiversity. In this NERC Highlight grant, we independently manipulated genetic diversity, non-genetic variation and phenotypic plasticity in D. magna populations in order to tease apart the impact that different components of a population’s evolutionary potential has on ecological and evolutionary dynamics.

Our specific objectives were:

1) To quantify variation in phenotypic plasticity across two environmental gradients within and between populations.
2) To understand how adaptive and non-adaptive plasticity, genetic diversity and epigenetics determine the evolutionary potential of populations.
3) To understand how limitations in the evolutionary potential of populations alter community dynamics and ecosystem function.

Our results show that repeated heatwaves induce the same transient life history responses each time but no evolutionary change in D. magna populations, regardless of their manipulated evolutionary potential. The manipulated genetic diversity and temperature-induced life history plasticity in D.magna populations also had no persistent effect on zooplankton community dynamics, demonstrating that the ecological role of this important grazer was stable across the different population set-ups. Our results contrast with earlier studies that have repeatedly demonstrated rapid adaptation in response to more artificial baseline temperature shifts in this species. This shows that paying closer attention to the nature and duration of the stresses generated by climate change may be critical when evaluating the likelihood of populations adapting or not.

The Brian Moss Mesocosm facility at Ness Botanic Gardens

Does phenotypic plasticity help or hinder rapid adaptation in novel and natural environments?

Background: Phenotypic plasticity is the ability of a single genotype to make different phenotypes in response to environmental variation. If all genotypes in a population respond to an environmental change in the same way plasticity can diminish the heritable phenotypic variation that selection acts on and slow down adaptation. In contrast, if all genotypes respond in very different ways, plasticity may speed up rapid adaptation. Whether or not plasticity helps or hinders adaptation therefore depends on the time that selection has had to shape the plastic responses of a population to the stressor it is facing. In this context, the effect that plasticity has on rapid adaptation could be quite different for populations adapting to aspects of climate change that have always been part of a population’s evolutionary history, compared with adaptation to ’novel’ anthropogenic environments such as pollutants. Although there is some laboratory evidence that novel environments expose cryptic genetic variation to selection, we still have no idea how relevant this is in natural populations where phenotypes depend on adaptive and non-adaptive plastic responses to many environmental heterogeneities. Understanding these interactions will be critical for predicting how populations respond to environmental change.

Clonal organisms allow us to test this hypothesis because we can expose the same genomes to different environments and compare the effect that they have on individuals, populations and communities.NERC DTP student Camille Riley is testing the hypothesis that plastic responses to climate-related stressors slows down adaptation whereas plastic responses to ’novel’ environments speeds it up.

Multidimensional scaling plot of 2543 DM CpGs sites. Confidence ellipses (95%) are drawn around treatment groups. All pollutant treatments separate from water controls along the first dimension, whereas differences between pollutants (particularly Cd and Np in the switch treatment) separate from one another along the second dimension.

Non-genetic inheritance

It has been hypothesized that the effects of pollutants on phenotypes can be passed to subsequent generations through epigenetic inheritance, affecting populations long after the removal of a pollutant. But there is still little evidence that pollutants can induce persistent epigenetic effects in animals. In an earlier NERC grant we demonstrated that even low doses of commonly used pollutants could induce genome-wide differences in cytosine methylation in the freshwater crustacean Daphnia pulex. Although some direct changes to methylation were only present in the continually exposed populations, others were present in both the continually exposed and switched to clean water treatments, suggesting that these modifications had persisted for 7 months (>15 generations). We also identified modifications that were only present in the populations that had switched to clean water, indicating a long-term legacy of pollutant exposure distinct from the persistent effects (see Figure). We also confirmed that sublethal doses of the same pollutants generate effects on life histories for at least three generations following the removal of the pollutant. Our results demonstrate that even low doses of pollutants can induce transgenerational epigenetic effects that are stably transmitted over many generations.

Harney E, Paterson S, Collin H, Chan BHK, Bennett D, Plaistow SJ (2022) Pollution induces epigenetic effects that are stably transmitted across multiple generations. Evol Lett, 6: 118–135

In an earlier paper we investigated the effects that non-genetic inheritance has on rates of agin in Daphnia pulex. Parental age reduces the life span of offspring in a diverse array of taxa but has not been explained from an evolutionary perspective. We quantified the effect that maternal age had on the growth and maturation decisions, life history, rates of senescence, and life span of offspring from three Daphnia pulex clones collected from different populations. Three generations of breeding from young or old mothers produced dramatic differences in the life histories of fourth-generation offspring, including significant reductions in lifespan. The magnitude of the effect differed between clones, which suggests that genetic and nongenetic factors ultimately underpin trait inheritance and shape patterns of aging. Our results provide a clear example of the need to consider multiple inheritance mechanisms when studying trait evolution.

Plaistow SJ, Shirley C, Collin H, Cornell SJ, Harney ED (2015) Offspring Provisioning Explains Clone-Specific Maternal Age Effects on Life History and Life Span in the Water Flea, Daphnia pulex. Am Nat, 186: 376–389

Research grants

Evolutionary resistance: Does adaptation stabilise plant community structure and function under climate change?

NATURAL ENVIRONMENT RESEARCH COUNCIL

August 2018 - May 2022

Limits to Adaptation

NATURAL ENVIRONMENT RESEARCH COUNCIL

May 2016 - September 2021

Evolution on ecological timescales: a role for non-genetic inheritance in adapting to novel anthropogenic stressors?

NATURAL ENVIRONMENT RESEARCH COUNCIL

February 2012 - August 2015

Population Dynamics and the evolution of phenotypic plasticity : Experimental Adaptive Dynamics

NATURAL ENVIRONMENT RESEARCH COUNCIL

October 2007 - March 2009

    Research collaborations

    Dr Daimark Bennett

    1) Evolution on ecological timescales: a role for non-genetic inheritance in adapting to novel anthropogenic stressors? NERC standard grant, 2011-2014.

    Dr Tom van Dooren

    Ecole Normal Superier, Paris

    Development of maturation rate models for measuring probabilistic maturation reaction norms.

    Dr John Colbourne

    Indiana University

    Epigenetics and maternal effects

    Dr Phil Watts

    NERC small grant application (Sept round) the genetic architecture of phenotypic divergence in Mnais damselflies.

    Dr Steve Paterson

    1) Evolution on ecological timescales: a role for non-genetic inheritance in adapting to novel anthropogenic stressors? NERC standard grant, 2011-2014. 2) Epigenetic inheritance and the control of offspring development (NERC MGF grant 2009). NERC MGF grant (>£5000) to carry out some preliminary microarray work examine to what extent epigenetic inheritance can explain transgenerational plasticity. This work has also led to the establishment of an international collaboration with Dr. John Colbourne (Indiana), the head of the Daphnia Genomics consortium.

    Prof. Yoshitaka Tsubaki

    Kyoto University

    I continue to collaborate with Prof. Y. Tsubaki (Kyoto) on the evolution of the genetic polymorphism in the damselfly, Mnais costalis. I have secured a 3-month visiting position in Kyoto for 2011, on the basis of a proposal designed to test ideas surrounding developmental character release and its role in speciation processes. A related NERC small grant (in collaboration with Dr Phil Watts) has also been submitted in order to fund genome scans on the material collected next year. This work will provide preliminary data for larger grant applications involving Watts, Tsubaki, and Prof. Siva-Jothy (Sheffield).