Can phenotypic plasticity and DNA methylation promote adaptive radiation?

How do living things adapt to a new environment? In the long-run this will need genetic (or occasionally cultural) changes, but biologists are beginning to take seriously the idea that the genome has evolved to allow an organism's development to be responsive to the environment. This process may operate at a fundamental level, with chemical changes to the structure of the DNA itself in the form of 'epigenetic' marks which can enhance or inhibit the expression of individual genes. Mostly, these are short-term changes that vary among tissues and life-stages in an individual organism as part of the normal process of development, but it is now known that sometimes they can be induced by the environment and occasionally even persist across generations. Can this type of epigenetic change help organisms cope with new environmental challenges or even lead to them evolving into new species through later genetic changes, a process called 'genetic assimilation'?

These are important questions for understanding the origins of biodiversity and its maintenance in a changing world. We aim to investigate these questions focussing on a small fish- the Eastern Happy- which belongs to one of the most spectacular examples of explosive evolutionary diversification, the African Great Lakes cichlid fishes, which have evolved into thousands of species in a few million years. Cichlid fishes have a second set of (pharyngeal) jaws in their throats that they use for processing their food, while the external (oral) jaws are specialised for capturing prey. Many closely-related cichlid species have subtly different jaw structures allowing them to feed on different things. This helps populations adapt to different environments, and allows different species to live together, exploiting different resources.

We plan to look at three closely-related pairs of populations of the Eastern Happy: in each pair one population feeds mostly on soft food- plankton or plant material, but the other includes hard-shelled prey such snails in its diet, and this is reflected in their more powerful jaws. We aim to see how much of these difference in jaw structures can be explained by environmentally-induced flexibility and how much is genetic. We will test live fish in aquaria to see whether the anatomical differences among populations really do improve how they capture and process different kinds of prey. We will see whether genetic differences cause anatomical variation in the same direction as the environmentally-induced changes. We will investigate the structure of the genomes to see whether epigenetic changes are associated with divergent diets and structures, and try to determine if different population pairs are diverging in similar ways. We aim to test if the activities of key genes in the jaws are associated with epigenetic changes. These experiments will be based around investigations of fish reared in research aquaria, fed on different diets to mimic the hard and soft-diets they experience in the wild. This allows us to feed fish from soft-diet populations on hard diets and vice versa. Particularly good insights will come from splitting a single brood of fish after 6th months and rearing one half on hard diet and the other half on a soft diet, thus controlling for the effects of genetics. By rearing several generations in this way, we will be able to see whether epigenetic changes to the genome can persist over several generations.

This study has the potential to reveal exciting new insights at the most fundamental level into how organisms adapt rapidly to their environments. The findings and techniques will have applications across a range of species and situations and perhaps cast light on how species will respond to the challenges of the environmental changes being caused by humans, through climate change, pollution and the introduction of alien species.

The main beneficiaries will be 1) the UK general public and 2) Researchers and policy makers in Africa.

1) The UK public has a keen interest in natural history and evolutionary biology and would be keen to learn more about how new species arise. Cichlids are an exotic and charismatic group of fishes, exhibiting a diverse array of colourful body shapes in varied habitats and are thus a useful study system to capture the imagination of the general public, especially children, and illustrate general principles of ecology and evolution. We will aim to reach out to the public through science events, including the Bristol Festival of Nature, the Bangor Science Festival and at least one other UK event, to maximize the demographic range of the target audiences. For these events we will develop a unique display demonstrating the diversity of craniofacial phenotypes found in Lake Malawi cichlid fishes, using X-ray computerised tomography scans and 3D printed models. We also aim to generate an interactive exhibit demonstrating how natural selection can lead to evolutionary change. Linking to these, we aim to develop a series of short you-tube style videos of the diversity of cichlids, explaining craniofacial jaw function and describing how this is related to diet and habitat use in this diverse group of species. Our research findings will be shared with a broad range of the public through press releases, social media and subsequent media contacts. This will be facilitated by the University of Bristol and Bangor University press teams.

2) Researchers and policy makers in Africa. Although the research has potential for far reaching academic benefits, the work relies on Lake Malawi cichlids. We aim to add applied value to the project by incorporating a training and capacity building element with our project partners the Fisheries Research Unit (Malawi) and TAFIRI (Tanzania). We will do this through a program of joint fieldwork, that we use an opportunity to link with researchers suitable for postgraduate training through schemes such as Commonwealth Scholarships. We will hold capacity-building workshops in each country aimed to sharing results of this project, and other relevant work on the fishes of the lake region. As part of this workshop there will be sessions dedicated to horizon scanning for future research needs and routes to securing funding. The workshop will be augmented by training for early career staff in useful skills for the collection, analysis and interpretation of ecological and genomic data.