A neutral explanation for the correlation of diversity with recombination rates in humans

Abstract

One of the most striking findings to emerge from the study of genomic patterns of variation is that regions with lower recombination rates tend to have lower levels of intraspecific diversity but not of interspecies divergence. This uncoupling of variation within and between species has been widely interpreted as evidence that natural selection shapes patterns of genetic variability genomewide. We revisited the relationship between diversity, divergence, and recombination in humans, using data from closely related species and better estimates of recombination rates than previously available. We show that regions that experience less recombination have reduced divergence to chimpanzee and to baboon, as well as lower levels of diversity. This observation suggests that mutation and recombination are associated processes in humans, so that the positive correlation between diversity and recombination may have a purely neutral explanation. Consistent with this hypothesis, diversity levels no longer increase significantly with recombination rates after correction for divergence to chimpanzee.

Figure 1

A, Human diversity levels (π) increase with human recombination rates. B, Human-chimpanzee divergence levels increase with human recombination rates. Note that the lines are for illustrative purposes only; the regression analyses used transformed values (see “Materials and Methods” section).

Figure 2

Human-baboon divergence levels increase with human recombination rates. Note that the line is for illustrative purposes only; the regression analyses used transformed values of divergence (see “Materials and Methods” section).

Figure 3

A, Human diversity levels (π) versus human-chimpanzee divergence (d) for the 76 loci in the SeattleSNPs survey. B, π/d versus human recombination rate estimates for the 76 loci in the SeattleSNPs survey. Note that the lines are for illustrative purposes only (see “Materials and Methods” section).