The neutral theory predicts that species with small census (and effective) population sizes are subject to greater drift (or allele frequency fluctuations), and vice versa. In other words, species with larger population sizes are expected to maintain more neutral diversity (polymorphisms). Intuitively then, the efficacy of selection in larger populations could constrain neutral genomic diversity, and vice versa. Little evidence exists however, of the maintenance of levels of neutral diversity due to population size (or drift) alone – “an old riddle” (Leffler et al. 2012), also termed Lewontin’s Paradox (Lewontin 1974). Today’s discussion of the neutralist-selectionist debate borrows thus from several concepts that I have written about over a series of posts – background selection (or negative selection at sites), and hitchhiking (or positive selection, and selective sweeps at sites), both leading to an overall reduction in genomic diversity at linked neutral sites. Diversity reduction is also correlated with site-specific recombination rates (as discussed here).
Species with large census sizes (eg. watermelon, silkmoth), versus small census sizes (orange, olive baboon). Image courtesy: http://dx.doi.org/10.1371/journal.pbio.1002113.g001
Positive correlation between the impact of natural selection and the geographic range of a species (A) – Figure 2 from Corbett-Detig et al. (2015)
In a recent publication, Corbett-Detig et al. (2015) in quite possibly the largest study of its kind, report strong evidence for the effects of natural selection in maintaining neutral diversity across multiple species. In analyzing variation across windows using genomes from 40 species of plants and animals, of varying census population sizes, the authors (a) call variants (against reference genomes), (b) estimate recombination rates, (c) fit and estimate likelihood under models of background selection, hitchhiking, and neutrality to determine genome-wide reduction in polymorphism, and (d) correlate recombination rates, and impact of selection with proxies for census population sizes (geographic range, and body size). Their analyses indicate strong evidence for the impact of natural selection on reduction of linked neutral diversity in species with large census sizes (eg. invertebrates, herbaceous plants). Conversely, species with small population sizes (eg. vertebrates, woody plants) show greater evidence of genetic drift influencing neutral genomic diversity. Significance of these findings remains when accounting for genome assembly quality, variations in genome size, recombination rates, sampling variance across chromosomes, and polymorphism levels affected by domestication. Their model also predicts that hitchhiking removes more linked neutral diversity in species with greater census population sizes, than background selection, although background selection is more prevalent among all species analyzed.
This study, while concretizing evidence for explanations to Lewontin’s paradox, also discusses violations of the neutral theory for several species (particularly those with large census population sizes).
It is therefore essential to consider selective processes when studying the distribution of genetic diversity within and between species. Incorporating selection into standard population genetic models of evolution will be a central and important challenge for evolutionary geneticists going forward.
Also see the commentary on this paper by Roland Roberts here.
Corbett-Detig RB, Hartl DL, Sackton TB (2015) Natural Selection Constrains Neutral Diversity across A Wide Range of Species. PLoS Biol 13(4):e1002112. doi:10.1371/journal.pbio.1002112
Leffler EM, Bullaughey K, Matute DR, Meyer WK, Ségurel L, et al. (2012) Revisiting an Old Riddle: What Determines Genetic Diversity Levels within Species? PLoS Biol 10(9): e1001388. doi:10.1371/journal.pbio.1001388
Lewontin RC (1974) The genetic basis of evolutionary change. New York: Columbia University Press. xiii, 346 p.
Roberts RG (2015) Lewontin’s Paradox Resolved? In Larger Populations, Stronger Selection Erases More Diversity. PLoS Biol 13(4): e1002113. doi:10.1371/journal.pbio.1002113