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.

The Genomic Architecture and Evolutionary Fates of Supergenes

“…Although there is some evidence for elevated d N / d S ratios on the Sb haplotype relative to levels outside of the social supergene (Yan et al 2020), tentatively suggesting a lower efficacy of purifying selection, the lack of major loss-of-function mutations or gene expression loss suggests that there has not yet been rampant genic degeneration or silencing of genes on the Sb haplotype ( Wang et al 2013 ; Stolle et al 2019 ). However, careful analyses have now begun to detect evidence of reduced expression of Sb -linked alleles and corresponding dosage compensation at SB alleles ( Martinez-Ruiz et al 2020 ).…”

Parameter exploration improves the accuracy of long-read genome assembly

“…To make the best assembly suitable for use as the reference assembly for the red fire ant, we corrected residual sequencing errors [41] and replaced rare alleles in the assembly [42] by mapping short read population-sequencing datasets (270x genome coverage) [29,36] to the assembly and substituting the most common variant at each locus [43]. Additionally, we removed contigs that appeared to be from bacteria, fungi or plants (Table S2).…”

“…To remove residual sequencing errors and rare alleles from the best assembly, we used eighteen Illumina whole-genome sequence datasets along with the Pacbio reads used for assembly. The Illumina datasets included all thirteen "bigB" labelled SRA runs from BioProject PRJNA542606 [36], and all five "bigB" labelled SRA runs from BioProject PRJNA396161 [29]. We cleaned the Illumina reads (Supplementary text, Additional file 1) and mapped them to the assembly using default parameters of bwa-mem (version 0.7.17) [51].…”

“…To assign the polished and filtered contigs to one of the sixteen fire-ant chromosomes, we generated genetic maps from RAD sequencing (RADseq) of seven fire ant families [32]. We further derived contig connectivity information from Bionano optical maps [29] and RNA sequencing (RNA-seq) of various tissue types and developmental stages: all SRA runs from BioProjects PRJNA542606 [36], PRJNA422376 [57], PRJNA266847, and PRJNA393960. We provided these as input to ALLMAPS (version 0.8.12) [58], assigning them equal weight to reduce the propagation of biases of any one dataset.…”

“…The draft genome assembly for this species [28] has been cited more than 350 times despite its high fragmentation (69,511 sequences) and capturing only 79% of the genome [29]. Importantly, the fragmentation and the missing sequences affect genomic regions involved in environmental perception [30,31], and complex behavioral and developmental traits [32][33][34][35][36]. To compare the generated assemblies, we used four complementary metrics that characterize assembly contiguity, completeness, and accuracy.…”