1. Evolutionary Biology
Download icon

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
Research Article
  • Cited 22
  • Views 2,754
  • Annotations
Cite this article as: eLife 2017;6:e23907 doi: 10.7554/eLife.23907

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.

Reviewing Editor

  1. Molly Przeworski, Columbia University, United States

Publication history

  1. Received: December 4, 2016
  2. Accepted: June 28, 2017
  3. Accepted Manuscript published: June 30, 2017 (version 1)
  4. Version of Record published: July 24, 2017 (version 2)

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

  • 2,754
    Page views
  • 296
    Downloads
  • 22
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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)

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

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

Categories and tags

Further reading

    1. Chromosomes and Gene Expression
    2. Evolutionary Biology

    High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

    Mathias Scharmann et al.
    Research Article Updated

    Differences between males and females are usually more subtle in dioecious plants than animals, but strong sexual dimorphism has evolved convergently in the South African Cape plant genus Leucadendron. Such sexual dimorphism in leaf size is expected largely to be due to differential gene expression between the sexes. We compared patterns of gene expression in leaves among 10 Leucadendron species across the genus. Surprisingly, we found no positive association between sexual dimorphism in morphology and the number or the percentage of sex-biased genes (SBGs). Sex bias in most SBGs evolved recently and was species specific. We compared rates of evolutionary change in expression for genes that were sex biased in one species but unbiased in others and found that SBGs evolved faster in expression than unbiased genes. This greater rate of expression evolution of SBGs, also documented in animals, might suggest the possible role of sexual selection in the evolution of gene expression. However, our comparative analysis clearly indicates that the more rapid rate of expression evolution of SBGs predated the origin of bias, and shifts towards bias were depleted in signatures of adaptation. Our results are thus more consistent with the view that sex bias is simply freer to evolve in genes less subject to constraints in expression level.

    1. Evolutionary Biology
    2. Neuroscience

    A small, computationally flexible network produces the phenotypic diversity of song recognition in crickets

    Jan Clemens et al.
    Research Article Updated

    How neural networks evolved to generate the diversity of species-specific communication signals is unknown. For receivers of the signals, one hypothesis is that novel recognition phenotypes arise from parameter variation in computationally flexible feature detection networks. We test this hypothesis in crickets, where males generate and females recognize the mating songs with a species-specific pulse pattern, by investigating whether the song recognition network in the cricket brain has the computational flexibility to recognize different temporal features. Using electrophysiological recordings from the network that recognizes crucial properties of the pulse pattern on the short timescale in the cricket Gryllus bimaculatus, we built a computational model that reproduces the neuronal and behavioral tuning of that species. An analysis of the model’s parameter space reveals that the network can provide all recognition phenotypes for pulse duration and pause known in crickets and even other insects. Phenotypic diversity in the model is consistent with known preference types in crickets and other insects, and arises from computations that likely evolved to increase energy efficiency and robustness of pattern recognition. The model’s parameter to phenotype mapping is degenerate – different network parameters can create similar changes in the phenotype – which likely supports evolutionary plasticity. Our study suggests that computationally flexible networks underlie the diverse pattern recognition phenotypes, and we reveal network properties that constrain and support behavioral diversity.

    1. Evolutionary Biology

    Ovipositor and mouthparts in a fossil insect support a novel ecological role for early orthopterans in 300 million years old forests

    Lu Chen et al.
    Research Article

    A high portion of the earliest known insect fauna is composed of the so-called ‘lobeattid insects’, whose systematic affinities and role as foliage feeders remain debated. We investigated hundreds of samples of a new lobeattid species from the Xiaheyan locality using a combination of photographic techniques, including reflectance transforming imaging, geometric morphometrics, and biomechanics to document its morphology, and infer its phylogenetic position and ecological role. Ctenoptilus frequens sp. nov. possessed a sword-shaped ovipositor with valves interlocked by two ball-and-socket mechanisms, lacked jumping hind-legs, and certain wing venation features. This combination of characters unambiguously supports lobeattids as stem relatives of all living Orthoptera (crickets, grasshoppers, katydids). Given the herein presented and other remains, it follows that this group experienced an early diversification and, additionally, occurred in high individual numbers. The ovipositor shape indicates that ground was the preferred substrate for eggs. Visible mouthparts made it possible to assess the efficiency of the mandibular food uptake system in comparison to a wide array of extant species. The new species was likely omnivorous which explains the paucity of external damage on contemporaneous plant foliage.