An unexpectedly large number of human autosomal genes are subject to monoallelic 
expression (MAE). Our analysis of 4,227 such genes uncovers surprisingly high 
genetic variation across human populations. This increased diversity is unlikely 
to reflect relaxed purifying selection. Remarkably, MAE genes exhibit an 
elevated recombination rate and an increased density of hypermutable sequence 
contexts. However, these factors do not fully account for the increased 
diversity. We find that the elevated nucleotide diversity of MAE genes is also 
associated with greater allelic age: variants in these genes tend to be older 
and are enriched in polymorphisms shared by Neanderthals and chimpanzees. Both 
synonymous and nonsynonymous alleles of MAE genes have elevated average 
population frequencies. We also observed strong enrichment of the MAE signature 
among genes reported to evolve under balancing selection. We propose that an 
important biological function of widespread MAE might be the generation of 
cell-to-cell heterogeneity; the increased genetic variation contributes to this 
heterogeneity.