Quantifying the relationship between genetic diversity and population size suggests natural selection cannot explain Lewontin's paradox
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 An archived version of this repository is also available at Zenodo.
-
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
Author details
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
- Guy Sella, Columbia University, United States
Publication history
- 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)
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.
Metrics
-
- 6,544
- Page views
-
- 614
- Downloads
-
- 14
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Evolutionary Biology
The avian palaeognath phylogeny has been recently revised significantly due to the advancement of genome-wide comparative analyses and provides the opportunity to trace the evolution of the microstructure and crystallography of modern dinosaur eggshells. Here, eggshells of all major clades of Palaeognathae (including extinct taxa) and selected eggshells of Neognathae and non-avian dinosaurs are analysed with electron backscatter diffraction. Our results show the detailed microstructures and crystallographies of (previously) loosely categorized ostrich-, rhea-, and tinamou-style morphotypes of palaeognath eggshells. All rhea-style eggshell appears homologous, while respective ostrich-style and tinamou-style morphotypes are best interpreted as homoplastic morphologies (independently acquired). Ancestral state reconstruction and parsimony analysis additionally show that rhea-style eggshell represents the ancestral state of palaeognath eggshells both in microstructure and crystallography. The ornithological and palaeontological implications of the current study are not only helpful for the understanding of evolution of modern and extinct dinosaur eggshells, but also aid other disciplines where palaeognath eggshells provide useful archive for comparative contrasts (e.g. palaeoenvironmental reconstructions, geochronology, and zooarchaeology).
-
- Evolutionary Biology
Vertebrate limb morphology often reflects the environment due to variation in locomotor requirements. However, proximal and distal limb segments may evolve differently from one another, reflecting an anatomical gradient of functional specialization that has been suggested to be impacted by the timing of development. Here we explore whether the temporal sequence of bone condensation predicts variation in the capacity of evolution to generate morphological diversity in proximal and distal forelimb segments across more than 600 species of mammals. Distal elements not only exhibit greater shape diversity, but also show stronger within-element integration and, on average, faster evolutionary responses than intermediate and upper limb segments. Results are consistent with the hypothesis that late developing distal bones display greater morphological variation than more proximal limb elements. However, the higher integration observed within the autopod deviates from such developmental predictions, suggesting that functional specialization plays an important role in driving within-element covariation. Proximal and distal limb segments also show different macroevolutionary patterns, albeit not showing a perfect proximo-distal gradient. The high disparity of the mammalian autopod, reported here, is consistent with the higher potential of development to generate variation in more distal limb structures, as well as functional specialization of the distal elements.