Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations

Magalhaes, Isabel S.; Whiting, James R.; D�Agostino, Daniele; Hohenlohe, Paul A.; Mahmud, Muayad; Bell, Michael A.; Sk�lason, Sk�li; MacColl, Andrew D.C.

Abstract

© 2020, The Author(s), under exclusive licence to Springer Nature Limited. Parallelism, the evolution of similar traits in populations diversifying in similar conditions, provides strong evidence of adaptation by natural selection. Many studies of parallelism focus on comparisons of different ecotypes or contrasting environments, defined a priori, which could upwardly bias the apparent prevalence of parallelism. Here, we estimated genomic parallelism associated with components of environmental and phenotypic variation at an intercontinental scale across four freshwater adaptive radiations (Alaska, British Columbia, Iceland and Scotland) of the three-spined stickleback (Gasterosteus aculeatus). We combined large-scale biological sampling and phenotyping with restriction site associated DNA sequencing (RAD-Seq) data from 73 freshwater lake populations and four marine ones (1,380 fish) to associate genome-wide allele frequencies with continuous distributions of environmental and phenotypic variation. Our three main findings demonstrate that (1) quantitative variation in phenotypes and environments can predict genomic parallelism; (2) genomic parallelism at the early stages of adaptive radiations, even at large geographic scales, is founded on standing variation; and (3) similar environments are a better predictor of genome-wide parallelism than similar phenotypes. Overall, this study validates the importance and predictive power of major phenotypic and environmental factors likely to influence the emergence of common patterns of genomic divergence, providing a clearer picture than analyses of dichotomous phenotypes and environments.

Citation

Magalhaes, I. S., Whiting, J. R., D’Agostino, D., Hohenlohe, P. A., Mahmud, M., Bell, M. A., Skúlason, S., & MacColl, A. D. (2020). Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations. Nature Ecology and Evolution, 5, 251–261. https://doi.org/10.1038/s41559-020-01341-8

• Journal Article Type: Article
• Acceptance Date: Oct 5, 2020
• Online Publication Date: Nov 30, 2020
• Publication Date: Nov 30, 2020
• Deposit Date: Jan 20, 2021
• Publicly Available Date: May 31, 2021
• Journal: Nature Ecology and Evolution
• Electronic ISSN: 2397-334X
• Publisher: Nature Publishing Group
• Peer Reviewed: Peer Reviewed
• Volume: 5
• Pages: 251–261
• DOI: https://doi.org/10.1038/s41559-020-01341-8
• Public URL: https://nottingham-repository.worktribe.com/output/5122791
• Publisher URL: https://www.nature.com/articles/s41559-020-01341-8
• Additional Information: Received: 4 December 2019; Accepted: 5 October 2020; First Online: 30 November 2020; : The authors declare no competing interests.