Predicting evolutionary change at the DNA level in a natural Mimulus population.

Evolution by natural selection occurs when the frequencies of genetic variants change because individuals differ in Darwinian fitness components such as survival or reproductive success. Differential fitness has been demonstrated in field studies of many organisms, but it remains unclear how well we...

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Main Authors: Patrick J Monnahan, Jack Colicchio, Lila Fishman, Stuart J Macdonald, John K Kelly
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1008945
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author Patrick J Monnahan
Jack Colicchio
Lila Fishman
Stuart J Macdonald
John K Kelly
author_facet Patrick J Monnahan
Jack Colicchio
Lila Fishman
Stuart J Macdonald
John K Kelly
author_sort Patrick J Monnahan
collection DOAJ
description Evolution by natural selection occurs when the frequencies of genetic variants change because individuals differ in Darwinian fitness components such as survival or reproductive success. Differential fitness has been demonstrated in field studies of many organisms, but it remains unclear how well we can quantitatively predict allele frequency changes from fitness measurements. Here, we characterize natural selection on millions of Single Nucleotide Polymorphisms (SNPs) across the genome of the annual plant Mimulus guttatus. We use fitness estimates to calibrate population genetic models that effectively predict allele frequency changes into the next generation. Hundreds of SNPs experienced "male selection" in 2013 with one allele at each SNP elevated in frequency among successful male gametes relative to the entire population of adults. In the following generation, allele frequencies at these SNPs consistently shifted in the predicted direction. A second year of study revealed that SNPs had effects on both viability and reproductive success with pervasive trade-offs between fitness components. SNPs favored by male selection were, on average, detrimental to survival. These trade-offs (antagonistic pleiotropy and temporal fluctuations in fitness) may be essential to the long-term maintenance of alleles. Despite the challenges of measuring selection in the wild, the strong correlation between predicted and observed allele frequency changes suggests that population genetic models have a much greater role to play in forward-time prediction of evolutionary change.
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spelling doaj.art-7f4c5c4be379445f857b0ca302e6d4ee2022-12-21T22:00:33ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-01-01171e100894510.1371/journal.pgen.1008945Predicting evolutionary change at the DNA level in a natural Mimulus population.Patrick J MonnahanJack ColicchioLila FishmanStuart J MacdonaldJohn K KellyEvolution by natural selection occurs when the frequencies of genetic variants change because individuals differ in Darwinian fitness components such as survival or reproductive success. Differential fitness has been demonstrated in field studies of many organisms, but it remains unclear how well we can quantitatively predict allele frequency changes from fitness measurements. Here, we characterize natural selection on millions of Single Nucleotide Polymorphisms (SNPs) across the genome of the annual plant Mimulus guttatus. We use fitness estimates to calibrate population genetic models that effectively predict allele frequency changes into the next generation. Hundreds of SNPs experienced "male selection" in 2013 with one allele at each SNP elevated in frequency among successful male gametes relative to the entire population of adults. In the following generation, allele frequencies at these SNPs consistently shifted in the predicted direction. A second year of study revealed that SNPs had effects on both viability and reproductive success with pervasive trade-offs between fitness components. SNPs favored by male selection were, on average, detrimental to survival. These trade-offs (antagonistic pleiotropy and temporal fluctuations in fitness) may be essential to the long-term maintenance of alleles. Despite the challenges of measuring selection in the wild, the strong correlation between predicted and observed allele frequency changes suggests that population genetic models have a much greater role to play in forward-time prediction of evolutionary change.https://doi.org/10.1371/journal.pgen.1008945
spellingShingle Patrick J Monnahan
Jack Colicchio
Lila Fishman
Stuart J Macdonald
John K Kelly
Predicting evolutionary change at the DNA level in a natural Mimulus population.
PLoS Genetics
title Predicting evolutionary change at the DNA level in a natural Mimulus population.
title_full Predicting evolutionary change at the DNA level in a natural Mimulus population.
title_fullStr Predicting evolutionary change at the DNA level in a natural Mimulus population.
title_full_unstemmed Predicting evolutionary change at the DNA level in a natural Mimulus population.
title_short Predicting evolutionary change at the DNA level in a natural Mimulus population.
title_sort predicting evolutionary change at the dna level in a natural mimulus population
url https://doi.org/10.1371/journal.pgen.1008945
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