IAP2-22-403

Identifying the genetic basis of local adaptation in a keystone freshwater species

How do animals rapidly adapt to diverse habitats? Understanding the genetic basis of adaptive phenotypic variation and ultimately fitness is a major aim of evolutionary biological research, as it helps us understand the origins of biodiversity and the ability of species to adapt to environmental changes. Rapid advances in genomics have enabled us to detect genetic signatures of selection related to local adaptation in a wide range of species, but linking such genetic changes to the phenotypes under selection and directly to fitness remains challenging (Bomblies and Peichel 2022). To date, this has only been possible in a few evolutionary model systems (Schluter et al. 2021; Lowry and Willis 2010; Barrett et al. 2019). Such studies have shown that both changes in major effect loci and polygenic backgrounds can contribute to phenotypic change and adaptation (Bomblies and Peichel 2022). Furthermore, quantitative genetic analyses of long-term study systems have highlighted substantial additive genetic variance in fitness and the potential for rapid adaptive evolution through natural selection in wild populations (Bonnet et al. 2022). Thus, by integrating state-of-the-art genomics with experimental approaches and quantitative genetics we now have the opportunity to directly map the genetic basis of local adaptation and fitness in ecologically relevant non-model systems.

Asellus aquaticus, the water louse, is an important keystone species in freshwater ecosystems that is emerging as a new model for eco-evolutionary studies (Lafuente et al. 2021). This small isopod plays a key ecological role as a detritivore and is an important food-source for many vertebrate and invertebrate predators in diverse freshwater ecosystems. A. aquaticus is widely distributed across Europe and occupies diverse habitats, such as stoney bottom and reed habitats (Lafuente et al. 2021; Sworobowicz et al. 2015; Hargeby, Johansson, and Ahnesjö 2004; Hargeby, Stoltz, and Johansson 2005). Individuals from different habitats show consistent differences in colouration, morphology, and behaviour across distinct populations (Lafuente et al. 2021; Eroukhmanoff and Svensson 2009). Such repeated phenotypic divergence between habitats suggests a role of natural selection and local adaptation (Elmer and Meyer 2011; Bolnick et al. 2018). Past research has shown that such phenotypic differences have a genetic basis and can rapidly arise within a few years in A. aquaticus (Eroukhmanoff, Hargeby, and Svensson 2009; Bakovic et al. 2021). Together, these well-documented phenotypic differences that have rapidly and repeatedly evolved across populations, the relatively short generation time, and possibility for experimental manipulation (Lürig and Matthews 2021), make A. aquaticus an excellent study system to investigate the genetic basis of local adaptation, and directly link the genotype, phenotype and fitness.

The overarching aim of this larger project is to identify the genetic basis of local adaptation and fitness in Asellus aquaticus. The PhD projects offers the opportunity to integrate different methodologies, such as population genomics of wild populations, quantitative genetics, and genetic mapping in experimental populations, and mesocosm experiments, to directly identify the genetic basis of local adaptation in a keystone species.

Methodology

To address the outlined question, the overarching project integrates different approaches, that are independent but highly integrative. Depending on the candidates’ interests, the project can focus either on the genomic, experimental and/or quantitative genetic aspects (or a combination thereof). Ideas for comprehensive work packages for this project are outlined below.

1) To identify the phenotypic and population genomic responses of adaptation to diverse habitats, A. aquaticus will be collected from different habitats in multiple freshwater systems, e.g. stone habitat, reed habitat and adjacent streams. Wild-caught individuals will be phenotyped for morphology, colouration, and behaviour. Population genomic analyses based on low-coverage whole genome sequencing (Lou et al. 2021) will offer the possibility to investigate signatures of selection within and across sites and to determine if similar or different genetic changes are associated with replicated adaptation (i.e. genomic parallelism).

2) To identify the genetic architecture of local adaptation and fitness, there is the possibility to rear individuals from different habitats and reciprocal F1 and F2 hybrid crosses under diverse semi-natural conditions in the lab. These crosses can be used for quantitative genetic analyses to investigate the genetic architecture of putatively adaptive phenotypic traits and investigate the impact of rearing environments on phenotypes and their correlations. Whole-genome sequencing of F2 hybrid individuals would also offer the possibility to map genomic regions associated with divergent phenotypic traits.

3) To discern adaptive genetic and phenotypic variation directly related to fitness (e.g. survival) under different environmental conditions, experimental F2 hybrids can be used for fitness assays in mesocosm experiments. Hybrid individuals can be kept in semi-natural habitats (stone or reed mescosms) with or without selective pressures (i.e. predators), and changes in allele frequencies (from low-coverage whole-genome sequencing) and phenotype distributions can be compared between founder populations and survivors. Adaptive alleles and phenotypes associated with fitness would be expected to show significant changes in frequency in treatment (with predators) compared to control populations (no predators).

Overall, these three independent yet integrative work packages will provide detailed insights into the phenotypic and genetic basis of local adaptation in a keystone freshwater species, and the potential to directly link these directly to variation in fitness.

Project Timeline

Year 1

– Collection of A. aquaticus from different habitats from three independent water bodies across Europe (e.g. Scotland, Germany, Slovenia).
– Phenotypic analysis of wild-caught individuals
– Generation and analysis of whole-genome resequencing data for wild-caught individuals
– Establishment of experimental populations and crosses

Year 2

– Analysis of genomic data
– Phenotyping/experimental assays of experimental populations/hybrid crosses
– Quantitative genetic analysis of experimental hybrids
– Generation of genomic data from experimental hybrids

Year 3

– Quantitative genetic analysis
– Genetic mapping of adaptive traits in experimental hybrids
– Mesocosm fitness assays of experimental populations

Year 3.5

– Finalising analysis
– Writing and editing of thesis

Training
& Skills

This project will provide wide ranging training from fieldwork to experimental design, quantitative (e.g. phenotypic analyses) and molecular approaches (e.g. DNA extraction, next generation sequencing), and analytical and bioinformatic skills (e.g. quantitative genetics, genomic analyses). The student will gain extensive skills in experimental design and project planning by providing substantial input for the direction of the project under the guidance of the supervisors. The student will also receive detailed training and guidance in diverse techniques by the supervisors, and through specific external courses, which will provide a solid basis for the student to pursue this project and future careers in diverse areas, within or outside academia. The student will be based at the School of Biodiversity, One Health and Comparative Medicine at the University of Glasgow under the supervision of Dr Arne Jacobs. Furthermore, Dr Michael Morrissey, a world-leading expert in quantitative genetics at the University of St Andrews will co-supervise the project and will provide extensive training in experimental work and the quantitative genetic analyses. Furthermore, the student will gain writing, presentation and communication skills through manuscript writing, presentations at internal seminars and national/international conferences, and public outreach training. Lastly, the student will receive general training opportunities from the broad skills training available through the University of Glasgow’s postgraduate training programmes and the specific training provided within the IAPETUS2 framework.

References & further reading

Bakovic, Vid, Maria Luisa Martin Cerezo, Andrey Höglund, Jesper Fogelholm, Rie Henriksen, Anders Hargeby, and Dominic Wright. 2021. “The Genomics of Phenotypically Differentiated Asellus Aquaticus Cave, Surface Stream and Lake Ecotypes.” Molecular Ecology 30 (14): 3530–47.

Barrett, Rowan D. H., Stefan Laurent, Ricardo Mallarino, Susanne P. Pfeifer, Charles C. Y. Xu, Matthieu Foll, Kazumasa Wakamatsu, Jonathan S. Duke-Cohan, Jeffrey D. Jensen, and Hopi E. Hoekstra. 2019. “Linking a Mutation to Survival in Wild Mice.” Science 363 (6426): 499–504.

Bolnick, Daniel I., Rowan D. H. Barrett, Krista B. Oke, Diana J. Rennison, and Yoel E. Stuart. 2018. “(Non) Parallel Evolution.” Annual Review of Ecology, Evolution, and Systematics 49: 303–30.

Bomblies, Kirsten, and Catherine L. Peichel. 2022. “Genetics of Adaptation.” Proceedings of the National Academy of Sciences of the United States of America 119 (30): e2122152119.

Bonnet, Timothée, Michael B. Morrissey, Pierre de Villemereuil, Susan C. Alberts, Peter Arcese, Liam D. Bailey, Stan Boutin, et al. 2022. “Genetic Variance in Fitness Indicates Rapid Contemporary Adaptive Evolution in Wild Animals.” Science 376 (6596): 1012–16.

Elmer, Kathryn R., and Axel Meyer. 2011. “Adaptation in the Age of Ecological Genomics: Insights from Parallelism and Convergence.” Trends in Ecology & Evolution 26 (6): 298–306.

Eroukhmanoff, Fabrice, Anders Hargeby, and Erik I. Svensson. 2009. “Rapid Adaptive Divergence between Ecotypes of an Aquatic Isopod Inferred from F-Q Analysis.” Molecular Ecology 18 (23): 4912–23.

Eroukhmanoff, Fabrice, and Erik I. Svensson. 2009. “Contemporary Parallel Diversification, Antipredator Adaptations and Phenotypic Integration in an Aquatic Isopod.” PloS One 4 (7): e6173.

Hargeby, Anders, Jonas Johansson, and Jonas Ahnesjö. 2004. “Habitat-Specific Pigmentation in a Freshwater Isopod: Adaptive Evolution over a Small Spatiotemporal Scale.” Evolution; International Journal of Organic Evolution 58 (1): 81–94.

Hargeby, A., J. Stoltz, and J. Johansson. 2005. “Locally Differentiated Cryptic Pigmentation in the Freshwater Isopod Asellus Aquaticus.” Journal of Evolutionary Biology 18 (3): 713–21.

Lafuente, Elvira, Moritz D. Lürig, Moritz Rövekamp, Blake Matthews, Claudia Buser, Christoph Vorburger, and Katja Räsänen. 2021. “Building on 150 Years of Knowledge: The Freshwater Isopod Asellus Aquaticus as an Integrative Eco-Evolutionary Model System.” Frontiers in Ecology and Evolution 9: 699.

Lou, Runyang Nicolas, Arne Jacobs, Aryn P. Wilder, and Nina Overgaard Therkildsen. 2021. “A Beginner’s Guide to Low-Coverage Whole Genome Sequencing for Population Genomics.” Molecular Ecology 30 (23): 5966–93.

Lowry, David B., and John H. Willis. 2010. “A Widespread Chromosomal Inversion Polymorphism Contributes to a Major Life-History Transition, Local Adaptation, and Reproductive Isolation.” PLoS Biology 8 (9).

Lürig, Moritz D., and Blake Matthews. 2021. “Dietary-Based Developmental Plasticity Affects Juvenile Survival in an Aquatic Detritivore.” Proceedings. Biological Sciences / The Royal Society 288 (1945): 20203136.

Schluter, Dolph, Kerry B. Marchinko, Matthew E. Arnegard, Haili Zhang, Shannon D. Brady, Felicity C. Jones, Michael A. Bell, and David M. Kingsley. 2021. “Fitness Maps to a Large-Effect Locus in Introduced Stickleback Populations.” Proceedings of the National Academy of Sciences of the United States of America 118 (3).

Sworobowicz, Lidia, Michał Grabowski, Tomasz Mamos, Artur Burzyński, Adrianna Kilikowska, Jerzy Sell, and Anna Wysocka. 2015. “Revisiting the Phylogeography ofAsellus Aquaticusin Europe: Insights into Cryptic Diversity and Spatiotemporal Diversification.” Freshwater Biology 60 (9): 1824–40.

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