Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)

Abstract Chromosomal inversions have been implicated in a remarkable range of natural phenomena, but it remains unclear how much they contribute to standing genetic variation. Here, we evaluate 64 inversions that segregate within a single natural population of the yellow monkeyflower (Mimulus guttat...

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Main Authors: Paris Veltsos, Luis J. Madrigal-Roca, John K. Kelly
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54534-1
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author Paris Veltsos
Luis J. Madrigal-Roca
John K. Kelly
author_facet Paris Veltsos
Luis J. Madrigal-Roca
John K. Kelly
author_sort Paris Veltsos
collection DOAJ
description Abstract Chromosomal inversions have been implicated in a remarkable range of natural phenomena, but it remains unclear how much they contribute to standing genetic variation. Here, we evaluate 64 inversions that segregate within a single natural population of the yellow monkeyflower (Mimulus guttatus). Nucleotide diversity patterns confirm low internal variation for the derived orientation (predicted by recent origin), elevated diversity between orientations (predicted by natural selection), and localized fluctuations (predicted by gene flux). Sequence divergence between orientations varies idiosyncratically by position, not following the suspension bridge pattern predicted if the breakpoints are the targets of selection. Genetic variation in gene expression is not inflated close to inversion breakpoints but is clearly partitioned between orientations. Like sequence variation, the pattern of expression variation suggests that the capture of coadapted alleles is more important than the breakpoints for the fitness effects of inversions. This work confirms several evolutionary predictions for inversion polymorphisms, but clarity emerges only by synthesizing estimates across many loci.
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spelling doaj-art-1bb9d78de6074998a7a1fd3c7b79a6902025-08-20T02:08:16ZengNature PortfolioNature Communications2041-17232024-11-0115111010.1038/s41467-024-54534-1Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)Paris Veltsos0Luis J. Madrigal-Roca1John K. Kelly2Department of Ecology and Evolutionary Biology, University of KansasDepartment of Ecology and Evolutionary Biology, University of KansasDepartment of Ecology and Evolutionary Biology, University of KansasAbstract Chromosomal inversions have been implicated in a remarkable range of natural phenomena, but it remains unclear how much they contribute to standing genetic variation. Here, we evaluate 64 inversions that segregate within a single natural population of the yellow monkeyflower (Mimulus guttatus). Nucleotide diversity patterns confirm low internal variation for the derived orientation (predicted by recent origin), elevated diversity between orientations (predicted by natural selection), and localized fluctuations (predicted by gene flux). Sequence divergence between orientations varies idiosyncratically by position, not following the suspension bridge pattern predicted if the breakpoints are the targets of selection. Genetic variation in gene expression is not inflated close to inversion breakpoints but is clearly partitioned between orientations. Like sequence variation, the pattern of expression variation suggests that the capture of coadapted alleles is more important than the breakpoints for the fitness effects of inversions. This work confirms several evolutionary predictions for inversion polymorphisms, but clarity emerges only by synthesizing estimates across many loci.https://doi.org/10.1038/s41467-024-54534-1
spellingShingle Paris Veltsos
Luis J. Madrigal-Roca
John K. Kelly
Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)
Nature Communications
title Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)
title_full Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)
title_fullStr Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)
title_full_unstemmed Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)
title_short Testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower (Mimulus guttatus)
title_sort testing the evolutionary theory of inversion polymorphisms in the yellow monkeyflower mimulus guttatus
url https://doi.org/10.1038/s41467-024-54534-1
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