Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci
- Uppsala University, Sweden
- Texas A&M University, United States
- Technical University of Denmark, Denmark
- University of Bergen, Norway
- Swedish University of Agricultural Sciences, Sweden
- Institute of Marine Research, Norway
- University College Dublin, Ireland
Abstract
Atlantic herring is widespread in North Atlantic and adjacent waters and is one of the most abundant vertebrates on earth. This species is well suited to explore genetic adaptation due to minute genetic differentiation at selectively neutral loci. Here we report hundreds of loci underlying ecological adaptation to different geographic areas and spawning conditions. Four of these represent megabase inversions confirmed by long read sequencing. The genetic architecture underlying ecological adaptation in herring deviates from expectation under a classical infinitesimal model for complex traits because of large shifts in allele frequencies at hundreds of loci under selection.
Data availability
Data availability statement. The sequence data generated in this study is available in Bioproject PRJNA642736.Code availability statement. The analyses of data have been carried out with publicly available software and all are cited in the Methods section. Custom scripts used are available in Github (https://github.com/Fan-Han/Population-analysis-with-pooled-data)
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Re-sequencing of Atlantic Herring populations and individualsNCBI Bioproject, PRJNA642736.
Article and author information
Author details
Funding
Knut och Alice Wallenbergs Stiftelse (KAW scholar)
- Leif Andersson
Vetenskapsrådet (Senior professor)
- Leif Andersson
Research Council of Norway (254774)
- Arild Folkvord
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2020, Han et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci
eLife 9:e61076.
https://doi.org/10.7554/eLife.61076
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Copy number variants (CNVs) are an important source of genetic variation underlying rapid adaptation and genome evolution. Whereas point mutation rates vary with genomic location and local DNA features, the role of genome architecture in the formation and evolutionary dynamics of CNVs is poorly understood. Previously, we found the GAP1 gene in Saccharomyces cerevisiae undergoes frequent amplification and selection in glutamine-limitation. The gene is flanked by two long terminal repeats (LTRs) and proximate to an origin of DNA replication (autonomously replicating sequence, ARS), which likely promote rapid GAP1 CNV formation. To test the role of these genomic elements on CNV-mediated adaptive evolution, we evolved engineered strains lacking either the adjacent LTRs, ARS, or all elements in glutamine-limited chemostats. Using a CNV reporter system and neural network simulation-based inference (nnSBI) we quantified the formation rate and fitness effect of CNVs for each strain. Removal of local DNA elements significantly impacts the fitness effect of GAP1 CNVs and the rate of adaptation. In 177 CNV lineages, across all four strains, between 26% and 80% of all GAP1 CNVs are mediated by Origin Dependent Inverted Repeat Amplification (ODIRA) which results from template switching between the leading and lagging strand during DNA synthesis. In the absence of the local ARS, distal ones mediate CNV formation via ODIRA. In the absence of local LTRs, homologous recombination can mediate gene amplification following de novo retrotransposon events. Our study reveals that template switching during DNA replication is a prevalent source of adaptive CNVs.
