The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB.

Abstract

Variation in social behaviour is common, yet little is known about the genetic architectures underpinning its evolution. A rare exception is in the fire ant Solenopsis invicta: Alternative variants of a supergene region determine whether a colony will have exactly one or up to dozens of queens. The two variants of this region are carried by a pair of ‘social chromosomes’, SB and Sb, which resemble a pair of sex chromosomes. Recombination is suppressed between the two chromosomes in the supergene region. While the X‐like SB can recombine with itself in SB/SB queens, recombination is effectively absent in the Y‐like Sb because Sb/Sb queens die before reproducing. Here, we analyse whole‐genome sequences of eight haploid SB males and eight haploid Sb males. We find extensive SB–Sb differentiation throughout the >19‐Mb‐long supergene region. We find no evidence of ‘evolutionary strata’ with different levels of divergence comparable to those reported in several sex chromosomes. A high proportion of substitutions between the SB and Sb haplotypes are nonsynonymous, suggesting inefficacy of purifying selection in Sb sequences, similar to that for Y‐linked sequences in XY systems. Finally, we show that the Sb haplotype of the supergene region has 635‐fold less nucleotide diversity than the rest of the genome. We discuss how this reduction could be due to a recent selective sweep affecting Sb specifically or associated with a population bottleneck during the invasion of North America by the sampled population.