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.
Reviewing Editor
- Dieter Ebert, University of Basel, Switzerland
Publication history
- Received: February 8, 2020
- Accepted: August 7, 2020
- Accepted Manuscript published: August 10, 2020 (version 1)
- Version of Record published: September 7, 2020 (version 2)
- Version of Record updated: November 11, 2020 (version 3)
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
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To synchronize flowering time with spring, many plants undergo vernalization, a floral-promotion process triggered by exposure to long-term winter cold. In Arabidopsis thaliana, this is achieved through cold-mediated epigenetic silencing of the floral repressor, FLOWERING LOCUS C (FLC). COOLAIR, a cold-induced antisense RNA transcribed from the FLC locus, has been proposed to facilitate FLC silencing. Here, we show that C-repeat (CRT)/dehydration-responsive elements (DREs) at the 3′-end of FLC and CRT/DRE-binding factors (CBFs) are required for cold-mediated expression of COOLAIR. CBFs bind to CRT/DREs at the 3′-end of FLC, both in vitro and in vivo, and CBF levels increase gradually during vernalization. Cold-induced COOLAIR expression is severely impaired in cbfs mutants in which all CBF genes are knocked-out. Conversely, CBF-overexpressing plants show increased COOLAIR levels even at warm temperatures. We show that COOLAIR is induced by CBFs during early stages of vernalization but COOLAIR levels decrease in later phases as FLC chromatin transitions to an inactive state to which CBFs can no longer bind. We also demonstrate that cbfs and FLCΔCOOLAIR mutants exhibit a normal vernalization response despite their inability to activate COOLAIR expression during cold, revealing that COOLAIR is not required for the vernalization process.