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

Abstract
Data availability
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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

1. Martinez-Ruiz C
2. Pracana R
3. Stolle E
4. Paris CI
5. Nichols RA
6. Wurm Y
(2019) Solenopsis invicta Raw sequence reads
NCBI SRA PRJNA542606.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA542606

The following previously published data sets were used

(2012) Solenopsis invicta Variation
NCBI SRA, SRP017317.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA182127
1. Fontana S
2. Chang NC
3. Chang T
4. Lee CC
5. Dang VD
6. Wang J
(2019) The fire ant social supergene is characterized by extensive gene and transposable element duplication
NCBI SRA, PRJNA542500.

https://www.ncbi.nlm.nih.gov/bioproject/542500
1. Morandin C
2. Tin MM
3. Abril S
4. Gómez C
5. Pontieri L
6. Schiøtt M
7. Sundström L
8. Tsuji K
9. Pedersen JS
10. Helanterä H
11. Mikheyev AS
(2015) Comparative transcriptomics reveals the conserved building blocks involved in parallel evolution of ant phenotypic traits
NCBI SRA, PRJDB4088.

https://www.ncbi.nlm.nih.gov/bioproject/PRJDB4088
1. Wurm Y et al
(2011) The genome of the fire ant Solenopsis invicta
NCBI, PRJNA49629.

https://www.ncbi.nlm.nih.gov/bioproject/PRJNA49629

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0002-4817-0565
Rodrigo Pracana

Department of Organismal Biology, Queen Mary University of London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Eckart Stolle

Department of Organismal Biology, Queen Mary University of London, London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
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.
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.
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.

"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

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.