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

  1. Vince Buffalo  Is a corresponding author
  1. University of Oregon, United States

Abstract

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.

Data availability

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 An archived version of this repository is also available at Zenodo.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Vince Buffalo

    Institute for Ecology and Evolution, University of Oregon, Eugene, United States
    For correspondence
    vsbuffalo@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4510-1609

Funding

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.

Reviewing Editor

  1. Guy Sella, Columbia University, United States

Publication history

  1. Received: February 12, 2021
  2. Accepted: August 16, 2021
  3. Accepted Manuscript published: August 19, 2021 (version 1)
  4. Accepted Manuscript updated: August 31, 2021 (version 2)
  5. Version of Record published: October 1, 2021 (version 3)

Copyright

© 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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  1. Vince Buffalo
(2021)
Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin's paradox
eLife 10:e67509.
https://doi.org/10.7554/eLife.67509
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