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Alternative life histories: linking genes to phenotypes to demography

Periodic Reporting for period 4 - ALH (Alternative life histories: linking genes to phenotypes to demography)

Reporting period: 2019-11-01 to 2021-04-30

Many species in nature exhibit flexible migration strategies, where some individuals migrate at some stage in their lives whilst others never migrate. Relatively little is known, however, about how such flexibility is encoded at the genetic level, what environmental cues animals base their migration decisions on, how migration versus residency evolves, and what are the consequences of human activities for facultatively migratory populations. This project addressed all of these issues using brown trout (Salmo trutta) – a type of fish related to salmon and one of the most diverse vertebrates on the planet – as an excellent model system. Salmonid fishes are of major cultural, economic and ecological importance in European waters and through their migrations they connect freshwater and marine habitats. Yet many stocks are in decline, and their lifestyles and habitats are threatened by diverse human actions including hydropower, hatcheries, harvest and fish farming. Deeper insights into their basic biology are thus crucial to their effective conservation, whilst also being of interest to the aquaculture industry.
We tackled a range or inter-related questions in the ALH project using a combination of large-scale laboratory and field experiments, whilst also exploiting recent exciting technical developments in molecular biology such as whole-genome resequencing and RNAseq and ever-increasing computing power to analyse “big data” and run simulation models. Our approach focussed on obtaining synthetic understanding of key patterns and processes across different biological levels, from DNA and associated biomolecules, to the behaviour and physiology of individuals, to the joint ecological and evolutionary dynamics of populations. As well of being of academic interest from a “blue skies research” perspective, our investigations are also of applied relevance in the context of biodiversity conservation and fisheries management.
In order to explore the relative contributions of genes versus environment to alternative migratory tactics, we undertook ambitious, large-scale experiments both in the laboratory and in a wild river environment. Both were a great success and fuelled the work of two PhD students (Dr Louise Archer – now graduated, Robert Wynne – soon to submit his thesis). The lab results revealed that migration decisions are shaped by a complex interplay between extrinsic factors such as food supply and temperature, and intrinsic factors such as population background and physiological traits (Archer et al. 2019 Frontiers in Ecology and Evolution; Archer et al. 2020 Global Change Biology). Put simply: neither nature nor nurture solely account for variation among fish in their migration strategies; rather, the two are intimately intertwined. This echoes findings in other fields such as the study of complex traits in humans. Our field experiment, for which data analyses and paper writing are ongoing, was more specifically focussed on the “nature” side of the equation, where we raised fish from different genetic backgrounds in “common garden” settings in the wild, in order to test for genetic differences among populations and individuals in migration tactics and associated traits.
A second strand of this project examined how fish acquire and utilise energy and how metabolism links to migration tactics, lifestyles and environment. So far this work has resulted in a published paper (Archer et al. 2020 Conservation Physiology) and another in review with Proceedings of the Royal Society B: Biological Sciences.

A third strand focussed on molecular-level patterns and processes, where the idea was to identify genetic variants that are associated with migration tactics and to better understand the links from DNA to RNA (“gene expression”) to individual phenotypes. For example, we have shown that migratory and resident fish differ in their expression of metabolic genes in their livers, but interestingly rather few genes were differentially expressed in their brains (Wynne et al. 2021 Ecology and Evolution). To identify genetic factors influencing whether fish migrate or not, we conducted an exciting study where we compared the genomes of river-caught trout that live either above or below waterfalls – the idea being that genetic variants that cause a fish to migrate should be selected against in above-falls populations (as individuals carrying such genes migrate over the falls but cannot then get back up). A draft paper is at an advanced stage, and further spin-off papers are being underway that examine additional aspects relating to “sexual conflict”, where genetic variants increase survival or reproductive success in one sex but decrease it in another. We also published another spin-off paper that was the first to comprehensively catalogue immune genes in brown trout and explore their expression and evolution (Colgan et al. 2021 Frontiers in Immunology).

The final part of the project used computer modelling to explore how environmental change – in particular sea lice from fish farms – affects migratory trout populations in terms of interactions between genetic and ecological terms. One novel angle developed here was the role of sexual conflict in influencing outcomes, with a manuscript to be submitted soon. We foresee that this model can be adapted to address a range of other interesting questions relevant to evolutionary biology, fisheries and climate change.

In addition to the above outputs, members of the ALH group have given over 15 presentations at national and international conferences/departmental seminars/workshops and engaged extensively with the media. Finally, the PI of this project has leveraged this ERC funding to obtain a permanent Senior Lecturer position at his Host Institute, and has also reinforced and expanded his international collaborative network.
In the project we have pushed the boundaries of knowledge along several interlinked fronts simultaneously, by integrating perspectives from genetics, physiology, immunology, behaviour and ecology. The team has published high quality work in leading international journals and presented the results to a broad scientific audience and the public. Comprehensive literature reviews on the topic of facultative migration in trout were published as a book chapter and a journal review. We have successfully pulled off large scale experiments in the laboratory and in the wild under challenging conditions, and have applied exploited cutting edge developments in genomics and bioinformatics. Going forward, we now have a state-of-the-art recirculating aquaculture system and associated equipment thanks to funding from this ERC grant and additional funds leveraged from other funding bodies, which is a major asset for future experimental research. A wealth of data has been amassed that has fuelled two PhD projects and a launch pad for future projects.
In conclusion, by drawing attention to fundamentally important biological questions in an iconic species of major economic importance in Europe, this ALH project has helped train the next generation of young researchers, has aspired to enhance the wider societal impacts of evolutionary ecology research and has generated results that will be of practical utility to fisheries managers and conservation biologists.
Montage of ALH team in action and field sites