紅火蟻的社會超級基因有許多基因和跳躍子上的拷貝數變異

Abstract

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The fire ant Solenopsis invicta shows two distinct social forms (monogyne and polygyne colonies, with one and multiple queens, respectively) under genetic control of a ~12.5 to 20 Mb supergene. The supergene includes ~600 genes linked together by multiple inversions, which prevents recombination between the two variants, ‘Social B’ (SB) and ‘Social b’ (Sb). In monogyne colonies all individuals carry only the SB allele, while in polygyne colonies, some individuals carry the Sb allele (all queens are heterozygotes SB/Sb, workers can be either SB/SB or SB/Sb and haploid males SB or Sb). 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 non-recombining 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 already been silenced. Characterization of the TEs revealed showed the BEL family (LTR retrotransposons) was disproportionately duplicated in the supergene. While the presence of TEs in supergenes is well documented, little is known about duplication of non-TE genes and their possible adaptive role. Among the 115 non-TE genes with higher copy in Sb, we found genes with putative polygyne related functions, such as juvenile hormone synthesis, odorant reception, and innate immunity. Interestingly, enzymes responsible for cuticular hydrocarbon synthesis were highly represented. We identified candidate duplications, and conducted detailed examination of a desaturase and an elongase, as potentially responsible for different cuticular hydrocarbons profiles in SB/SB and SB/Sb queens. These genes, which are likely beneficial for polygyne ants and important for queen recognition, seem to have translocated into the supergene from other chromosomes and proliferated by multiple duplication events. Overall, our results suggest that gene duplications may be an important factor leading to monogyne and polygyne ant societies.