Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants
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
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Solenopsis invicta Raw sequence readsNCBI SRA PRJNA542606.
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Solenopsis invicta VariationNCBI SRA, SRP017317.
Article and author information
Author details
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.
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Further reading
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- Chromosomes and Gene Expression
- Genetics and Genomics
Models of nuclear genome organization often propose a binary division into active versus inactive compartments yet typically overlook nuclear bodies. Here, we integrated analysis of sequencing and image-based data to compare genome organization in four human cell types relative to three different nuclear locales: the nuclear lamina, nuclear speckles, and nucleoli. Although gene expression correlates mostly with nuclear speckle proximity, DNA replication timing correlates with proximity to multiple nuclear locales. Speckle attachment regions emerge as DNA replication initiation zones whose replication timing and gene composition vary with their attachment frequency. Most facultative LADs retain a partially repressed state as iLADs, despite their positioning in the nuclear interior. Knock out of two lamina proteins, Lamin A and LBR, causes a shift of H3K9me3-enriched LADs from lamina to nucleolus, and a reciprocal relocation of H3K27me3-enriched partially repressed iLADs from nucleolus to lamina. Thus, these partially repressed iLADs appear to compete with LADs for nuclear lamina attachment with consequences for replication timing. The nuclear organization in adherent cells is polarized with nuclear bodies and genomic regions segregating both radially and relative to the equatorial plane. Together, our results underscore the importance of considering genome organization relative to nuclear locales for a more complete understanding of the spatial and functional organization of the human genome.