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The nearly neutral theory predicts specific relations between effective population size (Ne) and patterns of divergence and polymorphism, which depend on the shape of the distribution of fitness effects (DFE) of new mutations. However, testing these relations is not straightforward, owing to the difficulty in estimating Ne. Here, we introduce an integrative framework allowing for an explicit reconstruction of the phylogenetic history of Ne, thus leading to a quantitative test of the nearly neutral theory and an estimation of the allometric scaling of the ratios of nonsynonymous over synonymous polymorphism (πN/πS) and divergence (dN/dS) with respect to Ne. As an illustration, we applied our method to primates, for which the nearly neutral predictions were mostly verified. Under a purely nearly neutral model with a constant DFE across species, we find that the variation in πN/πS and dN/dS as a function of Ne is too large to be compatible with current estimates of the DFE based on site frequency spectra. The reconstructed history of Ne shows a 10-fold variation across primates. The mutation rate per generation u, also reconstructed over the tree by the method, varies over a 3-fold range and is negatively correlated with Ne. As a result of these opposing trends for Ne and u, variation in πS is intermediate, primarily driven by Ne but substantially influenced by u. Altogether, our integrative framework provides a quantitative assessment of the role of Ne and u in modulating patterns of genetic variation, while giving a synthetic picture of their history over the clade.

Reconstructing the History of Variation in Effective Population Size along Phylogenies