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.
Highlights
A longstanding mystery in evolutionary genetics is that the observed levels of genetic variation across sexual species span an unexpectedly narrow range
An impediment in resolving Lewontin’s Paradox is characterizing the relationship between diversity and census population sizes. This is difficult because census population sizes are unavailable for many taxa, especially for extremely abundant, cosmopolitan species that define the upper limit of ranges
The evidence of high phylogenetic signal found in this study suggests phylogenetic comparative methods (PCMs) are necessary when fitting the relationship between Nc and π in order to account for correlated residuals among closely-related species, and to avoid spurious results from phylogenetic pseudoreplication
Summary
A longstanding mystery in evolutionary genetics is that the observed levels of genetic variation across sexual species span an unexpectedly narrow range. Throughout the main text, I use recurrent hitchhiking and background selection models to estimate the reduction in diversity due to linked selection. Another class of linked selection models, which I refer to as quantitative genetic linked selection models (QGLS; Robertson (1961); Santiago and Caballero (1995, 1998)), can depress genome-wide diversity. These models may depress diversity at neutral sites unlinked to the regions containing fitness variation.
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