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

Increasing numbers of studies are now demonstrating 'contemporary evolution' in which populations evolve very quickly, sometimes in less than 10 generations. Frequently, contemporary evolution is associated with human activities for example antibiotic resistance in bacteria, metal pollution tolerance in plants, pesticide and herbicide resistance, and changes in fish stocks in response to over-fishing. Understanding how populations adapt to rapid and sustained anthropogenic change is imperative for predicting limits to population persistence, and reducing species extinction rates.

Our traditional view of evolution suggests that adaptation occurs through offspring inheriting genes from their parents that increase their survival and reproduction (fitness) in the current environment. Genetic variation is assumed to arise through random genetic mutations. But since most random mutations decrease an organism's fitness, and even random mutations that increase fitness initially only occur in a single individual, which might fail to breed just by chance, it is hard to see how random mutations alone can explain contemporary evolution in response to rapid anthropogenic change.

If populations are large enough, an advantageous mutation may already exist in the population that can 'rescue' it from extinction. However, an emerging alternative hypothesis that this study will focus on is that populations initially evolve through a process of non-genetic inheritance, in which novel phenotypes are generated by the transmission of factors other than DNA sequence.

'Parental effects' arise when parents differentially allocate non-genetic materials to their offspring altering their behaviour, morphology, or physiology. For example, in many species females produce fewer larger offspring when they experience harsh conditions. Alternatively, 'Epigenetic inheritance' occurs when the epigenetic marks responsible for changing the way that DNA is folded in a cell is inherited from one generation to the next, changing the pattern of genes that are switched on or off at any given time. This is essentially the same mechanism that explains how distinct cell types in our bodies are maintained from one cell division to the next.

Currently we have little idea how important non-genetic inheritance is in enabling populations to evolve in response to rapid environmental change, or which mechanism(s) might be involved. This is because in sexually reproducing organisms each individual has its own unique set of genes making it difficult to separate genetic inheritance from non-genetic inheritance and secondly because studies of non-genetic inheritance must be conducted over at least 3 generations, something which is not feasible in many study systems. In this study we will overcome these problems by studying non-genetic inheritance in the water flea, Daphnia pulex; an organism that has a generation time of 10 days and reproduces clonally, meaning that all offspring are genetically identical to their mothers.

We will quantify the non-genetic inheritance generated by exposure to different common freshwater pollutants by comparing the growth, survival, reproduction and patterns of gene expression of genetically identical offspring from ancestors exposed to pollution or not. The relative importance of parental effects and epigenetic inheritance will be assessed by determining whether differences in offspring traits in exposed and non-exposed lineages are explained by differences in offspring provisioning or changes in the patterns of genes switched on or off and the epigenetic marks responsible for folding DNA molecules in the cell. Finally, we will assess the evolutionary implications of non-genetic inheritance by determining whether the exposure of ancestors to pollutants changes the outcome of competition experiments between replicated genetically identical populations.

i) Who will benefit from this research and how?

a) Commercial private sector interested in the monitoring and prevention of freshwater pollution.
By studying differences in the patterns of gene expression of clones exposed to specific environmental stressors it will be possible to develop ecotoxicological bioassays that illuminate both the mode of action of different types of pollutants, but also the degree of exposure. Such assays would have commercial and legislative value in the fields of ecotoxicology, environmental consultancy and water treatment.

b) Policy makers
Governments all around the world currently use the survival and reproduction of Daphnia as a test for determining acceptable thresholds of freshwater pollutants. The development of tests based on genomic approaches will provide a more direct assessment of the in situ pollution levels and more detail about the nature of pollutant exposure. Current tests make no provision for non-genetic inheritance, despite the fact that resistance to different stressors can occur over a number of generations. Our data will quantify this problem, enabling a re-assessment of current methodologies.

c) Wider public.
By improving the procedures and policy used to monitor freshwater pollution, and reducing the chances of pollutants entering the food chain, the project will preserve natural environments, a societal benefit, and decrease risks to human health. Furthermore, epigenetic mechanisms are increasingly being implicated with the environmental modulation of numerous diseases including aging, cancer, schizophrenia and lifestyle diseases such as heart disease, diabetes, and obesity. Understanding how the environment can alter epigenetic states, and how stable these effects are over generations, will also therefore have a direct health benefit for the wider public.

d) Wider public - public understanding of science.
Reversing the public perception that evolution is a slow process is important given that anthropogenic effects are the primary driver of rapid evolutionary change. Second, the concepts of non-genetic inheritance and epigenetics are poorly understood by the general public, although their increasing implication in the manifestation of disease process means that it is imperative that these topics enter the public domain.

e) Training of scientists
The project will train researchers in state of the art ecological genomic techniques that are transferable to other fields such as health and medicine, stem cell technology, disease biology, agriculture, conservation, and environmental sciences.

f) Other fields of academic research
Our findings will be of broad interest to a range of different disciplines including:

- Evolutionary biologists and Molecular ecologists interested in mechanisms of adaptation and resolving the debate concerning the need for broader definition of inheritance.
- Ecotoxicologists interested in understanding acclimation to pollutants and developing genomic biomarkers.
- Developmental biologists interested in developing a model system in which to study epigenetics. As a crustacean, Daphnia provides a useful comparison with Drosophila to test whether same genes are subject to epigenetic control across species.
- Medical scientists interested in studying the epigenetic mechanisms associated with cancers and other pathologies. Many of the genes involved are conserved across species, and so the study of the interaction between the environment and the epigenome in another model species may highlight novel processes of interest to medical epigenetics.
- Environmental scientists interested in the persistence of toxins in the environment and the transfer of effects from one generation to the next.