Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox

Neutral theory predicts that genetic diversity increases with population size, yet observed levels of diversity across metazoans vary only two orders of magnitude while population sizes vary over several. This unexpectedly narrow range of diversity is known as Lewontin’s Paradox of Variation (1974)....

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Main Author: Vince Buffalo
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/67509
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spelling doaj-3c05fd6eeb1046038f97da054d4c419d2021-10-01T12:04:05ZengeLife Sciences Publications LtdeLife2050-084X2021-08-011010.7554/eLife.67509Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s ParadoxVince Buffalo0https://orcid.org/0000-0003-4510-1609Institute for Ecology and Evolution, University of Oregon, Eugene, United StatesNeutral theory predicts that genetic diversity increases with population size, yet observed levels of diversity across metazoans vary only two orders of magnitude while population sizes vary over several. This unexpectedly narrow range of diversity is known as Lewontin’s Paradox of Variation (1974). While some have suggested selection constrains diversity, tests of this hypothesis seem to fall short. Here, I revisit Lewontin’s Paradox to assess whether current models of linked selection are capable of reducing diversity to this extent. To quantify the discrepancy between pairwise diversity and census population sizes across species, I combine previously-published estimates of pairwise diversity from 172 metazoan taxa with newly derived estimates of census sizes. Using phylogenetic comparative methods, I show this relationship is significant accounting for phylogeny, but with high phylogenetic signal and evidence that some lineages experience shifts in the evolutionary rate of diversity deep in the past. Additionally, I find a negative relationship between recombination map length and census size, suggesting abundant species have less recombination and experience greater reductions in diversity due to linked selection. However, I show that even assuming strong and abundant selection, models of linked selection are unlikely to explain the observed relationship between diversity and census sizes across species.https://elifesciences.org/articles/67509Lewontin's Paradoxphylogenetic comparative methodslinked selection
collection DOAJ
language English
format Article
sources DOAJ
author Vince Buffalo
spellingShingle Vince Buffalo
Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox
eLife
Lewontin's Paradox
phylogenetic comparative methods
linked selection
author_facet Vince Buffalo
author_sort Vince Buffalo
title Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox
title_short Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox
title_full Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox
title_fullStr Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox
title_full_unstemmed Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin’s Paradox
title_sort quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain lewontin’s paradox
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-08-01
description Neutral theory predicts that genetic diversity increases with population size, yet observed levels of diversity across metazoans vary only two orders of magnitude while population sizes vary over several. This unexpectedly narrow range of diversity is known as Lewontin’s Paradox of Variation (1974). While some have suggested selection constrains diversity, tests of this hypothesis seem to fall short. Here, I revisit Lewontin’s Paradox to assess whether current models of linked selection are capable of reducing diversity to this extent. To quantify the discrepancy between pairwise diversity and census population sizes across species, I combine previously-published estimates of pairwise diversity from 172 metazoan taxa with newly derived estimates of census sizes. Using phylogenetic comparative methods, I show this relationship is significant accounting for phylogeny, but with high phylogenetic signal and evidence that some lineages experience shifts in the evolutionary rate of diversity deep in the past. Additionally, I find a negative relationship between recombination map length and census size, suggesting abundant species have less recombination and experience greater reductions in diversity due to linked selection. However, I show that even assuming strong and abundant selection, models of linked selection are unlikely to explain the observed relationship between diversity and census sizes across species.
topic Lewontin's Paradox
phylogenetic comparative methods
linked selection
url https://elifesciences.org/articles/67509
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