Journal Article

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

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

2020

Overview

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. Red fire ants ( Solenopsis invicta ) are native to South America, but the species has spread to North America, Australia and New Zealand where it can be an invasive pest. A reason for this species’ invasiveness types of colonies : one with a single egg-laying queen and another with several queens. However, it is not possible to simply add more queens to a colony with one queen. Instead, the number of queens in a colony is controlled genetically, by a chromosome known as the ‘social chromosome’. Like many other animals, red fire ants are diploid: their cells have two copies of each chromosome, which can carry two different versions of each gene. The social chromosome is no different, and it comes in two variants, SB and Sb. Each ant can therefore have either two SB chromosomes, leading to a colony with a single queen; or one SB chromosome and one Sb chromosome, leading to a colony with multiple queens. Ants with two copies of the Sb variant die when they are young, so the Sb version is inherited in a similar way to how the Y chromosome is passed on in humans. However, the social chromosome in red fire ants appeared less than one million years ago, making it much younger than the human Y chromosome, which is 180 million years old. This makes the social chromosome a good candidate for examining the early evolution of special chromosome variants that are only inherited. How differences between the SB and the Sb chromosomes are evolving is an open question, however. Perhaps each version of the social chromosome has been optimised through natural selection to one colony type. Another suggestion is that the Sb chromosome has degenerated over time because its genes cannot be ‘reshuffled’ as they would be on normal chromosomes. Martinez-Ruiz et al. compared genetic variants on the SB and Sb chromosomes, along with their expression in different types of ant colonies. The analysis showed that the Sb variant is in fact breaking down because of the lack of gene shuffling. This loss is compensated by intact copies of the same genes found on the SB variant, which explains why ants with the Sb variant can only survive if they also carry the SB version. Only a handful of genes on the social chromosomes appear to have been optimised by natural selection. Therefore Martinez-Ruiz et al. concluded the differences between the two chromosomes that lead to different colony types are collateral effects of Sb’s inability to reshuffle its genes. This work reveals how a special chromosome similar to the Y chromosome in humans evolved. It also shows how multiple complex evolutionary forces can shape a species’ genetic makeup and social forms.

• Publisher: eLife Sciences Publications, Ltd,eLife Sciences Publications Ltd
• Subject: allele-specific expression / Alleles / Animals / antagonistic selection / ants / Ants - genetics / Behavior, Animal / Biological Evolution / Chromosomes - genetics / Chromosomes and Gene Expression / Evolution, Molecular / Evolutionary Biology / Gene Expression / Genomics / Selection, Genetic - genetics / Social Behavior / social evolution / Solenopsis invicta / supergenes