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

  • 2,947
    views
  • 377
    downloads
  • 20
    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. 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

Share this article

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

Categories and tags

Further reading

    1. Chromosomes and Gene Expression

    SFSWAP is a negative regulator of OGT intron detention and global pre-mRNA splicing

    Ashwin Govindan, Nicholas K Conrad
    Research Article

    O-GlcNAcylation is the reversible post-translational addition of β-N-acetylglucosamine to serine and threonine residues of nuclear and cytoplasmic proteins. It plays an important role in several cellular processes through the modification of thousands of protein substrates. O-GlcNAcylation in humans is mediated by a single essential enzyme, O-GlcNAc transferase (OGT). OGT, together with the sole O-GlcNAcase OGA, form an intricate feedback loop to maintain O-GlcNAc homeostasis in response to changes in cellular O-GlcNAc using a dynamic mechanism involving nuclear retention of its fourth intron. However, the molecular mechanism of this dynamic regulation remains unclear. Using an O-GlcNAc responsive GFP reporter cell line, we identify SFSWAP, a poorly characterized splicing factor, as a trans-acting factor regulating OGT intron detention. We show that SFSWAP is a global regulator of retained intron splicing and exon skipping that primarily acts as a negative regulator of splicing. In contrast, knockdown of SFSWAP leads to reduced inclusion of a ‘decoy exon’ present in the OGT retained intron which may mediate its role in OGT intron detention. Global analysis of decoy exon inclusion in SFSWAP and UPF1 double knockdown cells indicate altered patterns of decoy exon usage. Together, these data indicate a role for SFSWAP as a global negative regulator of pre-mRNA splicing and positive regulator of intron retention.

    1. Cell Biology
    2. Chromosomes and Gene Expression

    Treacle’s ability to form liquid-like phase condensates is essential for nucleolar fibrillar center assembly, efficient rRNA transcription and processing, and rRNA gene repair

    Artem K Velichko, Nadezhda V Petrova ... Omar L Kantidze
    Research Article

    We investigated the role of the nucleolar protein Treacle in organizing and regulating the nucleolus in human cells. Our results support Treacle’s ability to form liquid-like phase condensates through electrostatic interactions among molecules. The formation of these biomolecular condensates is crucial for segregating nucleolar fibrillar centers from the dense fibrillar component and ensuring high levels of ribosomal RNA (rRNA) gene transcription and accurate rRNA processing. Both the central and C-terminal domains of Treacle are required to form liquid-like condensates. The initiation of phase separation is attributed to the C-terminal domain. The central domain is characterized by repeated stretches of alternatively charged amino acid residues and is vital for condensate stability. Overexpression of mutant forms of Treacle that cannot form liquid-like phase condensates compromises the assembly of fibrillar centers, suppressing rRNA gene transcription and disrupting rRNA processing. These mutant forms also fail to recruit DNA topoisomerase II binding protein 1 (TOPBP1), suppressing the DNA damage response in the nucleolus.