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

Carlos Martinez-Ruiz,Yannick Wurm,Carolina Ivon Paris,Richard A Nichols,Eckart Stolle,Rodrigo Pracana

doi:10.7554/elife.55862

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.

Highlights

Selection for multiple phenotypic optima within a single species can result in intra-specific evolutionary conflict
The fixed differences in allele-specific expression across populations that we report may be consequences of recombination suppression rather than adaptations arising from evolutionary conflict
By analyzing allele-specific expression patterns between the SB and Sb variants of the fire ant supergene we found consistent differences across three populations

Summary

Introduction

Selection for multiple phenotypic optima within a single species can result in intra-specific evolutionary conflict Such conflict can lead to selection for reduced recombination between co-adapted alleles encoding the different phenotypes [1]. This selection pressure can favor the formation of supergene regions containing tightly linked alleles of up to hundreds of genes. We know that supergenes controlling ecologically important traits are widespread These include flower heterostyly in Primula [4], mating type in Mycrobotryum fungi [5], Batesian mimicry in butterflies [6, 7], mating behavior in white-throated sparrows [8, 9] or male sexual morphs in ruffs [10, 11]

Objectives

Methods

Results

Discussion

Conclusion