Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.

Centromeres are essential mediators of chromosomal segregation, but both centromeric DNA sequences and associated kinetochore proteins are paradoxically diverse across species. The selfish centromere model explains rapid evolution by both components via an arms-race scenario: centromeric DNA variant...

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Main Authors: Findley R Finseth, Thomas C Nelson, Lila Fishman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-04-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1009418
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spelling doaj-d014742c6a574cfdb74256b6c8c03e7c2021-05-14T04:31:28ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-04-01174e100941810.1371/journal.pgen.1009418Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.Findley R FinsethThomas C NelsonLila FishmanCentromeres are essential mediators of chromosomal segregation, but both centromeric DNA sequences and associated kinetochore proteins are paradoxically diverse across species. The selfish centromere model explains rapid evolution by both components via an arms-race scenario: centromeric DNA variants drive by distorting chromosomal transmission in female meiosis and attendant fitness costs select on interacting proteins to restore Mendelian inheritance. Although it is clear than centromeres can drive and that drive often carries costs, female meiotic drive has not been directly linked to selection on kinetochore proteins in any natural system. Here, we test the selfish model of centromere evolution in a yellow monkeyflower (Mimulus guttatus) population polymorphic for a costly driving centromere (D). We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years. We use quantitative genetic mapping to demonstrate that context-dependence in the strength of drive (from near-100% D transmission in interspecific hybrids to near-Mendelian in within-population crosses) primarily reflects variable vulnerability of the non-driving competitor chromosomes, but also map an unlinked modifier of drive coincident with kinetochore protein Centromere-specific Histone 3 A (CenH3A). Finally, CenH3A exhibits a recent (<1000 years) selective sweep in our focal population, implicating local interactions with D in ongoing adaptive evolution of this kinetochore protein. Together, our results demonstrate an active co-evolutionary arms race between DNA and protein components of the meiotic machinery in Mimulus, with important consequences for individual fitness and molecular divergence.https://doi.org/10.1371/journal.pgen.1009418
collection DOAJ
language English
format Article
sources DOAJ
author Findley R Finseth
Thomas C Nelson
Lila Fishman
spellingShingle Findley R Finseth
Thomas C Nelson
Lila Fishman
Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.
PLoS Genetics
author_facet Findley R Finseth
Thomas C Nelson
Lila Fishman
author_sort Findley R Finseth
title Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.
title_short Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.
title_full Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.
title_fullStr Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.
title_full_unstemmed Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.
title_sort selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2021-04-01
description Centromeres are essential mediators of chromosomal segregation, but both centromeric DNA sequences and associated kinetochore proteins are paradoxically diverse across species. The selfish centromere model explains rapid evolution by both components via an arms-race scenario: centromeric DNA variants drive by distorting chromosomal transmission in female meiosis and attendant fitness costs select on interacting proteins to restore Mendelian inheritance. Although it is clear than centromeres can drive and that drive often carries costs, female meiotic drive has not been directly linked to selection on kinetochore proteins in any natural system. Here, we test the selfish model of centromere evolution in a yellow monkeyflower (Mimulus guttatus) population polymorphic for a costly driving centromere (D). We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years. We use quantitative genetic mapping to demonstrate that context-dependence in the strength of drive (from near-100% D transmission in interspecific hybrids to near-Mendelian in within-population crosses) primarily reflects variable vulnerability of the non-driving competitor chromosomes, but also map an unlinked modifier of drive coincident with kinetochore protein Centromere-specific Histone 3 A (CenH3A). Finally, CenH3A exhibits a recent (<1000 years) selective sweep in our focal population, implicating local interactions with D in ongoing adaptive evolution of this kinetochore protein. Together, our results demonstrate an active co-evolutionary arms race between DNA and protein components of the meiotic machinery in Mimulus, with important consequences for individual fitness and molecular divergence.
url https://doi.org/10.1371/journal.pgen.1009418
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