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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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Large-scale mutation in the evolution of a gene complex for cryptic coloration
The types of mutations affecting adaptation in the wild are only beginning to be understood. In particular, whether structural changes shape adaptation by suppressing recombination or by creating new mutations is unresolved. Here, we show that multiple linked but recombining loci underlie cryptic color morphs of Timema chumash stick insects. In a related species, these loci are found in a region of suppressed recombination, forming a supergene. However, in seven species of Timema , we found that a megabase-size “supermutation” has deleted color loci in green morphs. Moreover, we found that balancing selection likely contributes more to maintaining this mutation than does introgression. Our results show how suppressed recombination and large-scale mutation can help to package gene complexes into discrete units of diversity such as morphs, ecotypes, or species.
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- Award ID(s):
- 1638768
- PAR ID:
- 10273100
- Date Published:
- Journal Name:
- Science
- Volume:
- 369
- Issue:
- 6502
- ISSN:
- 0036-8075
- Page Range / eLocation ID:
- 460 to 466
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1126/science.aaz4351
