The fire ant social supergene is characterized by extensive gene and transposable element copy number variation

Abstract

In the fire ant Solenopsis invicta, a supergene composed of ~600 genes and having two variants, SB and Sb, regulates colony social form. In single queen colonies, all individuals carry only the SB allele, while in multiple queen colonies, some individuals carry the Sb allele. In this study, we characterized genes with copy number variation between SB and Sb‐carrying individuals. We showed extensive acquisition of gene duplicates in the Sb genome, with some likely involved in polygyne‐related phenotypes. We found 260 genes with copy number differences between SB and Sb, of which 239 have greater copy number in Sb. We observed transposable element (TE) accumulation on Sb, likely due to the accumulation of repetitive elements on the nonrecombining chromosome. We found a weak correlation between TE copy number and differential expression, suggesting some TEs may still be proliferating in Sb while many of the duplicated TEs have presumably been silenced. Among the 115 non‐TE genes with higher copy in Sb, enzymes responsible for cuticular hydrocarbon synthesis were highly represented. These include a desaturase and an elongase, both potentially responsible for differential queen odour and likely beneficial for polygyne ants. These genes seem to have translocated into the supergene from other chromosomes and proliferated by multiple duplication events. While the presence of TEs in supergenes is well documented, little is known about duplication of non‐TE genes and their possible adaptive role. Overall, our results suggest that gene duplications may be an important factor leading to monogyne and polygyne ant societies.

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

“…For this, we generated RNA-seq data from whole bodies of SB/Sb workers and from abdomens, thoraces, and heads of SB/Sb virgin queens collected in South America. To compare with patterns in other fire ant populations, we additionally incorporated existing RNA-seq gene expression data from pools of whole bodies of SB/Sb queens collected in the USA and Taiwan ( Wurm et al, 2011 ; Fontana et al, 2020 ). We summarize our hypotheses and results in Table 1 .…”

Genomic architecture and evolutionary conflict drive allele-specific expression in the social supergene of the red fire ant

“…We generated individual-specific RNA-seq data from whole bodies of SB/Sb workers and from abdomens, thoraces, and heads of SB/Sb virgin queens collected in South America. To add additional robustness to our analysis, we additionally incorporated existing RNA-seq gene expression data from pools of whole bodies of SB/Sb queens collected in the USA and Taiwan (41,42).…”

“…Finally, we also performed this analysis using pools of SB/Sb queens from Taiwanese populations (42) Table S3c). Out of the 374 genes analyzed, 19 showed significant allelespecific expression.…”

“…Additionally, we manually checked the resulting RNA reads for heterozygous positions at key supergene markers using the IGV gene browser v2.4.19 (63). Fontana et al (42) generated RNA-seq data from 4 samples of SB/Sb queens from multiple-queen colonies from Taiwan. Each sample is a pool of whole bodies from two virgin queens (more details in Supporting Information, Table S5a).…”

“…Preliminary analyses showed that the interaction between "variant effect" and "body part" had no significant effect in any of the genes, and consequently, only the main "variant effect" was considered as the factor of interest for this analysis. The model formula for both the Wurm et al (41) and the Fontana et al (42) RNA-seq datasets included only whole bodies of queens. We thus used "sample" as a blocking factor and "variant effect" as variable of interest.…”