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
Further reading
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- Evolutionary Biology
- Genetics and Genomics
Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for the maintenance of inversion polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one of which has negative frequency-dependent fitness. These conditions yield a form of frequency-dependent disruptive selection, favoring two predominant haplotypes segregating alleles that favor opposing antagonistic phenotypes. An inversion associated with one haplotype can reduce the fitness load incurred by generating recombinant offspring, reinforcing its linkage to the haplotype and enabling both haplotypes to accumulate more antagonistic variants than expected otherwise. We develop and apply a forward simulator to examine these dynamics under a tradeoff between survival and male display. These simulations indeed generate inversion-associated haplotypes with opposing sex-specific fitness effects. Antagonism strengthens with time, and can ultimately yield karyotypes at surprisingly predictable frequencies, with striking genotype frequency differences between sexes and between developmental stages. To test whether this model may contribute to well-studied yet enigmatic inversion polymorphisms in Drosophila melanogaster, we track inversion frequencies in laboratory crosses to test whether they influence male reproductive success or survival. We find that two of the four tested inversions show significant evidence for the tradeoff examined, with In(3 R)K favoring survival and In(3 L)Ok favoring male reproduction. In line with the apparent sex-specific fitness effects implied for both of those inversions, In(3 L)Ok was also found to be less costly to the viability and/or longevity of males than females, whereas In(3 R)K was more beneficial to female survival. Based on this work, we expect that balancing selection on antagonistically pleiotropic traits may provide a significant and underappreciated contribution to the maintenance of natural inversion polymorphism.
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- Evolutionary Biology
Wolbachia are maternally transmitted bacterial symbionts that are ubiquitous among arthropods. They can hijack host reproduction in various ways, including male-killing (MK), where the sons of infected mothers are killed during development. The recent discovery of MK-associated Wolbachia genes, i.e., oscar in Ostrinia moths and wmk in Drosophila flies, stimulates our interest in the diversity and commonality of MK mechanisms, which remain largely unclear. We recently discovered that a Wolbachia symbiont of the moth Homona magnanima carries an MK-associated prophage region encoding homologs of oscar (Hm-oscar) and wmk (wmk-1–4). Here, we investigated the effects of these genes in the native host. Upon transient overexpression, Hm-oscar, but not wmk, induced male lethality in H. magnanima, in contrast to our observations in Drosophila, where the wmk homologs, but not Hm-oscar, killed the males. Hm-oscar disrupted sex determination in male embryos by inducing a female-type doublesex splicing and impaired dosage compensation, recapitulating the Wolbachia phenotype. Cell-based transfection assays confirmed that Hm-oscar suppressed the function of masculinizer, the primary male sex determinant involved in lepidopteran dosage compensation. Our study highlights the conserved roles of oscar homologs in Wolbachia-induced lepidopteran MK and argues that Wolbachia have evolved multiple MK mechanisms in insects.
