Moderate nucleotide diversity in the Atlantic herring is associated with a low mutation rate

  1. Chungang Feng
  2. Mats Pettersson
  3. Sangeet Lamichhaney
  4. Carl-Johan Rubin
  5. Nima Rafati
  6. Michele Casini
  7. Arild Folkvord
  8. Leif Andersson  Is a corresponding author
  1. Uppsala University, Sweden
  2. Swedish University of Agricultural Sciences, Sweden
  3. University of Bergen, Norway

Abstract

The Atlantic herring is one of the most abundant vertebrates on earth but its nucleotide diversity is moderate (π=0.3%), only three-fold higher than in human. Here, we present a pedigree-based estimation of the mutation rate in this species. Based on whole-genome sequencing of four parents and 12 offspring, the estimated mutation rate is 2.0 x 10-9 per base per generation. We observed a high degree of parental mosaicism indicating that a large fraction of these de novo mutations occurred during early germ cell development. The estimated mutation rate - the lowest among vertebrates analyzed to date - partially explains the discrepancy between the rather low nucleotide diversity in herring and its huge census population size. But a species like the herring will never reach its expected nucleotide diversity because of fluctuations in population size over the millions of years it takes to build up high nucleotide diversity.

Data availability

The following data sets were generated

Article and author information

Author details

  1. Chungang Feng

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  2. Mats Pettersson

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  3. Sangeet Lamichhaney

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  4. Carl-Johan Rubin

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  5. Nima Rafati

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  6. Michele Casini

    Department of Aquatic Resources, Swedish University of Agricultural Sciences, Lysekil, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  7. Arild Folkvord

    Department of Biology, University of Bergen, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  8. Leif Andersson

    Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
    For correspondence
    leif.andersson@imbim.uu.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4085-6968

Funding

European Research Council (Bateson)

  • Leif Andersson

Norwegian Research Council (254774)

  • Arild Folkvord
  • Leif Andersson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2017, Feng 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.

Metrics

  • 3,418
    views
  • 358
    downloads
  • 70
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Chungang Feng
  2. Mats Pettersson
  3. Sangeet Lamichhaney
  4. Carl-Johan Rubin
  5. Nima Rafati
  6. Michele Casini
  7. Arild Folkvord
  8. Leif Andersson
(2017)
Moderate nucleotide diversity in the Atlantic herring is associated with a low mutation rate
eLife 6:e23907.
https://doi.org/10.7554/eLife.23907

Share this article

https://doi.org/10.7554/eLife.23907

Further reading

    1. Computational and Systems Biology
    2. Evolutionary Biology
    Pierre Barrat-Charlaix, Richard A Neher
    Research Article

    As pathogens spread in a population of hosts, immunity is built up, and the pool of susceptible individuals are depleted. This generates selective pressure, to which many human RNA viruses, such as influenza virus or SARS-CoV-2, respond with rapid antigenic evolution and frequent emergence of immune evasive variants. However, the host’s immune systems adapt, and older immune responses wane, such that escape variants only enjoy a growth advantage for a limited time. If variant growth dynamics and reshaping of host-immunity operate on comparable time scales, viral adaptation is determined by eco-evolutionary interactions that are not captured by models of rapid evolution in a fixed environment. Here, we use a Susceptible/Infected model to describe the interaction between an evolving viral population in a dynamic but immunologically diverse host population. We show that depending on strain cross-immunity, heterogeneity of the host population, and durability of immune responses, escape variants initially grow exponentially, but lose their growth advantage before reaching high frequencies. Their subsequent dynamics follows an anomalous random walk determined by future escape variants and results in variant trajectories that are unpredictable. This model can explain the apparent contradiction between the clearly adaptive nature of antigenic evolution and the quasi-neutral dynamics of high-frequency variants observed for influenza viruses.

    1. Ecology
    2. Evolutionary Biology
    Rebecca D Tarvin, Jeffrey L Coleman ... Richard W Fitch
    Research Article

    Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.