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). 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.
All primary datasets collated by this study, including new census size and range estimates, are available on Github at HTTP://github.com/vsbuffalo/paradox_variation. An archived version of this repository is also available at Zenodo.
Why do species get a thin slice of π?10.5281/zenodo.4542480.
Nucleotide diversity estimates.10.1371/journal.pbio.1001388.s001.
Supplementary material from "Variation in recombination frequency and distribution across eukaryotes: patterns and processes"https://doi.org/10.6084/m9.figshare.c.3904942.v3.
Article and author information
NIH Office of the Director (1R01GM117241)
- Vince Buffalo
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
- Guy Sella, Columbia University, United States
- Received: February 12, 2021
- Accepted: August 16, 2021
- Accepted Manuscript published: August 19, 2021 (version 1)
- Accepted Manuscript updated: August 31, 2021 (version 2)
- Version of Record published: October 1, 2021 (version 3)
© 2021, Buffalo
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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