The Hill–Robertson effect: evolutionary consequences of weak selection and linkage in finite populations

Abstract

The 'Hill-Robertson (HR) effect' describes that linkage between sites under selection will reduce the overall effectiveness of selection in finite populations. Here we discuss the major concepts associated with the HR effect and present results of computer simulations focusing on the linkage effects generated by multiple sites under weak selection. Most models of linkage and selection forecast differences in effectiveness of selection between chromosomes or chromosomal regions involving a number of genes. The abundance and physical clustering of weakly selected mutations across genomes, however, justify the investigation of HR effects at a very local level and we pay particular attention to linkage effects among selected sites of the same gene. Overall, HR effects caused by weakly selected mutations predict differences in effectiveness of selection between genes that differ in exon-intron structures and across genes. Under this scenario, introns might play an advantageous role reducing intragenic HR effects. Finally, we summarize observations that are consistent with local HR effects in Drosophila, discuss potential consequences on population genetic studies and suggest future lines of research.