1. Chromosomes and Gene Expression
  2. Evolutionary Biology

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

  1. Carlos Martinez-Ruiz  Is a corresponding author
  2. Rodrigo Pracana
  3. Eckart Stolle
  4. Carolina Ivon Paris
  5. Richard A Nichols
  6. Yannick Wurm  Is a corresponding author
  1. Queen Mary University of London, United Kingdom
  2. Universidad de Buenos Aires, Argentina
https://doi.org/10.7554/eLife.55862
Share this article
Cite this article
  1. Carlos Martinez-Ruiz
  2. Rodrigo Pracana
  3. Eckart Stolle
  4. Carolina Ivon Paris
  5. Richard A Nichols
  6. Yannick Wurm
(2020)
Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants
eLife 9:e55862.
https://doi.org/10.7554/eLife.55862
  2. Download BibTeX
  3. Download .RIS

Abstract

Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young "social" supergene of fire ants, a powerful system for disentangling the effects of evolutionary antagonism and suppressed recombination. We hypothesize that gene degeneration and social antagonism shaped the evolution of the fire ant supergene, resulting in distinct patterns of gene expression. We test these ideas by identifying allelic differences between supergene variants, characterizing allelic expression across populations, castes and body parts, and contrasting allelic expression biases with differences in expression between social forms. We find strong signatures of gene degeneration and gene-specific dosage compensation. On this background, a small portion of the genes has the signature of adaptive responses to evolutionary antagonism between social forms.

Data availability

We deposited genomic and transcriptomic reads we generated from South American Solenopsis invicta on NCBI SRA (PRJNA542606). All analysis scripts used are available at https://github.com/wurmlab/2019-11-allelic_bias_in_fire_ant_supergene

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Carlos Martinez-Ruiz

    Department of Organismal Biology, Queen Mary University of London, London, United Kingdom
    For correspondence
    c.martinezruiz@qmul.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4817-0565

  2. Rodrigo Pracana

    Department of Organismal Biology, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  3. Eckart Stolle

    Department of Organismal Biology, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  4. Carolina Ivon Paris

    Departamento Ecología, Genética y Evolución, Universidad de Buenos Aires, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.

  5. Richard A Nichols

    Department of Organismal Biology, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

  6. Yannick Wurm

    Department of Organismal Biology, Queen Mary University of London, London, United Kingdom
    For correspondence
    y.wurm@qmul.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3140-2809

Funding

NERC (NE/L00626X/1)

  • Yannick Wurm

NERC (NE/L002485/1)

  • Carlos Martinez-Ruiz

DAAD (570704 83)

  • Yannick Wurm

European Commission Marie Curie Actions (PIEF-GA-2013-623713)

  • Yannick Wurm

BBSRC (BB/K004204/1)

  • Yannick Wurm

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

Ethics

Animal experimentation: We snap froze field-collected ants into liquid nitrogen. Ethical guidelines typically do not consider such invertebrates. However, we performed the experiments in a manner that minimized potential harm.

Copyright

© 2020, Martinez-Ruiz 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

  • 2,942
    views
  • 376
    downloads
  • 20
    citations

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

Download links

Share this article

https://doi.org/10.7554/eLife.55862

Categories and tags

Further reading

    1. Chromosomes and Gene Expression
    2. Evolutionary Biology

    The domesticated transposon protein L1TD1 associates with its ancestor L1 ORF1p to promote LINE-1 retrotransposition

    Gülnihal Kavaklioglu, Alexandra Podhornik ... Christian Seiser
    Research Article

    Repression of retrotransposition is crucial for the successful fitness of a mammalian organism. The domesticated transposon protein L1TD1, derived from LINE-1 (L1) ORF1p, is an RNA-binding protein that is expressed only in some cancers and early embryogenesis. In human embryonic stem cells, it is found to be essential for maintaining pluripotency. In cancer, L1TD1 expression is highly correlative with malignancy progression and as such considered a potential prognostic factor for tumors. However, its molecular role in cancer remains largely unknown. Our findings reveal that DNA hypomethylation induces the expression of L1TD1 in HAP1 human tumor cells. L1TD1 depletion significantly modulates both the proteome and transcriptome and thereby reduces cell viability. Notably, L1TD1 associates with L1 transcripts and interacts with L1 ORF1p protein, thereby facilitating L1 retrotransposition. Our data suggest that L1TD1 collaborates with its ancestral L1 ORF1p as an RNA chaperone, ensuring the efficient retrotransposition of L1 retrotransposons, rather than directly impacting the abundance of L1TD1 targets. In this way, L1TD1 might have an important role not only during early development but also in tumorigenesis.

    1. Chromosomes and Gene Expression

    Nuclear Argonaute protein NRDE-3 switches small RNA partners during embryogenesis to mediate temporal-specific gene regulatory activity

    Shihui Chen, Carolyn Marie Phillips
    Research Article

    RNA interference (RNAi) is a conserved pathway that utilizes Argonaute proteins and their associated small RNAs to exert gene regulatory function on complementary transcripts. While the majority of germline-expressed RNAi proteins reside in perinuclear germ granules, it is unknown whether and how RNAi pathways are spatially organized in other cell types. Here, we find that the small RNA biogenesis machinery is spatially and temporally organized during Caenorhabditis elegans embryogenesis. Specifically, the RNAi factor, SIMR-1, forms visible concentrates during mid-embryogenesis that contain an RNA-dependent RNA polymerase, a poly-UG polymerase, and the unloaded nuclear Argonaute protein, NRDE-3. Curiously, coincident with the appearance of the SIMR granules, the small RNAs bound to NRDE-3 switch from predominantly CSR-class 22G-RNAs to ERGO-dependent 22G-RNAs. NRDE-3 binds ERGO-dependent 22G-RNAs in the somatic cells of larvae and adults to silence ERGO-target genes; here we further demonstrate that NRDE-3-bound, CSR-class 22G-RNAs repress transcription in oocytes. Thus, our study defines two separable roles for NRDE-3, targeting germline-expressed genes during oogenesis to promote global transcriptional repression, and switching during embryogenesis to repress recently duplicated genes and retrotransposons in somatic cells, highlighting the plasticity of Argonaute proteins and the need for more precise temporal characterization of Argonaute-small RNA interactions.