Selfishly evolving centromeres bias their transmission by exploiting the asymmetry of female meiosis and preferentially segregating to the egg. Such female meiotic drive systems have the potential to be supergenes, with multiple linked loci contributing to drive costs or enhancement. Here, we explore the supergene potential of a selfish centromere ( D ) in Mimulus guttatus , which was discovered in the Iron Mountain (IM) Oregon population. In the nearby Cone Peak population, D is still a large, non-recombining and costly haplotype that recently swept, but shorter haplotypes and mutational variation suggest a distinct population history. We detected D in five additional populations spanning more than 200 km; together, these findings suggest that selfish centromere dynamics are widespread in M. guttatus . Transcriptome comparisons reveal elevated differences in expression between driving and non-driving haplotypes within, but not outside, the drive region, suggesting large-scale cis effects of D 's spread on gene expression. We use the expression data to refine linked candidates that may interact with drive, including Nuclear Autoantigenic Sperm Protein (NASP SIM3 ), which chaperones the centromere-defining histone CenH3 known to modify Mimulus drive. Together, our results show that selfishly evolving centromeres may exhibit supergene behaviour and lay the foundation for future genetic dissection of drive and its costs. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.
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Genomic architecture of supergenes: connecting form and function
Supergenes are tightly linked sets of loci that are inherited together and control complex phenotypes. While classical supergenes—governing traits such as wing patterns in Heliconius butterflies or heterostyly in Primula —have been studied since the Modern Synthesis, we still understand very little about how they evolve and persist in nature. The genetic architecture of supergenes is a critical factor affecting their evolutionary fate, as it can change key parameters such as recombination rate and effective population size, potentially redirecting molecular evolution of the supergene in addition to the surrounding genomic region. To understand supergene evolution, we must link genomic architecture with evolutionary patterns and processes. This is now becoming possible with recent advances in sequencing technology and powerful forward computer simulations. The present theme issue brings together theoretical and empirical papers, as well as opinion and synthesis papers, which showcase the architectural diversity of supergenes and connect this to critical processes in supergene evolution, such as polymorphism maintenance and mutation accumulation. Here, we summarize those insights to highlight new ideas and methods that illuminate the path forward for the study of supergenes in nature. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.
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- Award ID(s):
- 1655701
- NSF-PAR ID:
- 10348279
- Date Published:
- Journal Name:
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Volume:
- 377
- Issue:
- 1856
- ISSN:
- 0962-8436
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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 genus
Formica presents 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. francoeuri exhibits polymorphism in colony social organization and that the phenotypic polymorphism is strongly associated with genotypes within theFormica social supergene region. The distribution of supergene haplotypes inF. francoeuri differs from that of related speciesFormica selysi in 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 theFormica supergene is conserved within the genus, the mechanisms that maintain the supergene and its associated polymorphisms differ among species.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rstb.2021.0192
