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Abstract Most supergenes discovered so far are young, occurring in one species or a few closely related species. An ancient supergene in the ant genusFormicapresents an unusual opportunity to compare supergene‐associated phenotypes and the factors that influence the persistence of polymorphism in different species. We investigate the genetic architecture of social organization inFormica francoeuri, an ant species native to low‐ and mid‐elevation semiarid regions of southern California, and describe an efficient technique for estimating mode of social organization using population genomic data. Using this technique, we show thatF. francoeuriexhibits polymorphism in colony social organization and that the phenotypic polymorphism is strongly associated with genotypes within theFormicasocial supergene region. The distribution of supergene haplotypes inF. francoeuridiffers from that of related speciesFormica selysiin that colonies with multiple queens contain almost exclusively workers that are heterozygous for alternative supergene haplotypes. Moreover, heterozygous workers exhibit allele‐specific expression of the polygyne‐associated haplotype at the candidate geneKnockout,which is thought to influence social organization. We also report geographic population structure and variation in worker size across a large fraction of the species range. Our results suggest that, although theFormicasupergene is conserved within the genus, the mechanisms that maintain the supergene and its associated polymorphisms differ among species.
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The maintenance of polymorphism in an ancient social supergene
Abstract Supergenes, regions of the genome with suppressed recombination between sets of functional mutations, contribute to the evolution of complex phenotypes in diverse systems. Excluding sex chromosomes, most supergenes discovered so far appear to be young, being found in one species or a few closely related species. Here, we investigate how a chromosome harbouring an ancient supergene has evolved over about 30 million years (Ma). TheFormicasupergene underlies variation in colony queen number in at least five species. We expand previous analyses of sequence divergence on this chromosome to encompass about 90 species spanning theFormicaphylogeny. Within the nonrecombining region, the geneknockoutcontains 22 single nucleotide polymorphisms (SNPs) that are consistently differentiated between two alternative supergene haplotypes in divergent EuropeanFormicaspecies, and we show that these same SNPs are present in mostFormicaclades. In these clades, including an early diverging NearcticFormicaclade, individuals with alternative genotypes atknockoutalso have higher differentiation in other portions of this chromosome. We identify hotspots of SNPs along this chromosome that are present in multipleFormicaclades to detect genes that may have contributed to the emergence and maintenance of the genetic polymorphism. Finally, we infer three gene duplications on one haplotype, based on apparent heterozygosity within these genes in the genomes of haploid males. This study strengthens the evidence that this supergene originated early in the evolution ofFormicaand that just a few loci in this large region of suppressed recombination retain strongly differentiated alleles across contemporaryFormicalineages.
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- PAR ID:
- 10370262
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 30
- Issue:
- 23
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 6246-6258
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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