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Adaptive Evolution and Hill-Robertson Effects

Rates of adaptive evolution of genomes are affected by numerous processes – variation in mutation rates across the genome, gene density, the recombination landscape (and thus local drift effects), and consequently, the efficacy of natural selection, and differential introgression post divergence, to name a few. Specifically, the reduction of the efficacy of selection in finite populations due to “interference” between selected sites, primarily owing to drift effects at differentially recombining loci, often called “Hill-Robertson Effects”, or interference (HRi) have been often attributed to the evolution of sex, and recombination itself [see Comeron et al. 2008, Keightley and Otto 2006 for reviews, also summarized in this review I wrote for The Molecular Ecologist]. Conversely, reduction in HRi effects as a result of increased recombination is also associated with greater adaptive evolution [see Marais and Charlesworth 2003 for a review]. Observations directly associated with quantifying HRi thus look to regions of reduced recombination exhibiting (1) reduced genomic diversity, (2) reduced codon usage bias, (3) lower dN (number of non-synonymous substitutions on an average) in genes. However, all three of these observations are contentious, with alternate explanations for each observation – reduced genomic diversity could as well be due to differential introgression, and selection against migrant alleles [Peyseur 2010], reduced codon usage bias due to the recombination process itself, or GC-biased gene conversion [eg. Bolivar et al. 2015, Lassalle et al. 2015], and lower dN due to non-recombinant (eg. sex) chromosome linkage effects [Haddrill et al. 2007].

Recently, Harris and Nielsen (2015), and Juric et al. (2015) – also excellently summarized here, have proposed the role of HRi in differentially purging weakly deleterious Neanderthal alleles in early generation hybrids, and hence retention of Neanderthal DNA in some human populations. On the flip-side, reduction in recombination and population size, high mutational load, and hence reduced efficacy of purifying selection would also explain the persistence of some Neanderthal alleles (also particularly depleted around genes, regions which also experience reduced recombination). The same theory can also be invoked in explaining the absence of Y chromosomal/mtDNA remnants of Neanderthal ancestry in humans, and the low frequencies on the X – the apparent dearth of recombination should have allowed for reduced HRi, and hence more effective purging of alleles of low fitness.

In another intriguing find, Castellano et al. (2015) recently reported ~27% reduction in the rate of adaptive evolution in Drosophila melanogaster due to HRi – i.e. higher rates of adaptation in regions of high recombination, and a negative correlation between gene density and rates of adaptation (and positive correlation between mutation rate and adaptation).

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This brings forth a rather complex relationship between mutation rates, recombination rates, the distribution of fitness effects, and gene densities as determinants of HRi, and thus the rate of adaptive evolution. With better recombination maps, more genomes, and methods to analyze data under complex population genetic models, there ought to be more theory and empirical instances of HRi in species. In the words of WG Hill (1974):

Now that it is possible to use starch gel electrophoresis to type the same individual for several different polymorphic loci, some of which may be linked, associations between frequencies of alleles at two or more loci are being studied…In view of the number of these studies being undertaken, whatever their possible contribution to population genetics, it seems worth while to investigate some of the statistical problems of estimation of linkage disequilibrium.



Bolívar, Paulina, et al. “Recombination rate variation modulates gene sequence evolution mainly via GC-biased gene conversion, not Hill-Robertson interference, in an avian system.” Molecular biology and evolution (2015): msv214.

Castellano, David, et al. “Adaptive evolution is substantially impeded by Hill-Robertson interference in Drosophila.” Molecular biology and evolution (2015): msv236.

Comeron, Josep M., A. Williford, and R. M. Kliman. “The Hill-Robertson effect: evolutionary consequences of weak selection and linkage in finite populations.”Heredity 100.1 (2008): 19-31.

Haddrill, Penelope R., et al. “Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over.” Genome biology 8.2 (2007): R18.

Harris K and Nielsen R. The genetic cost of Neanderthal introgression. bioRxiv doi:

Hill, William G., and Alan Robertson. “The effect of linkage on limits to artificial selection.” Genetical research 8.03 (1966): 269-294.

Hill, William G. “Estimation of linkage disequilibrium in randomly mating populations.” Heredity 33.2 (1974): 229-239.

Juric I, Aeschbacher S, Coop G. The strength of selection againt Neanderthal introgression. bioRxiv doi:

Keightley, Peter D., and Sarah P. Otto. “Interference among deleterious mutations favours sex and recombination in finite populations.” Nature 443.7107 (2006): 89-92.

Lassalle, Florent, et al. “GC-content evolution in bacterial genomes: the biased gene conversion hypothesis expands.” PLoS Genet 11.2 (2015): e1004941.

Marais, Gabriel, and Brian Charlesworth. “Genome evolution: recombination speeds up adaptive evolution.” Current biology 13.2 (2003): R68-R70.

Payseur, Bret A. “Using differential introgression in hybrid zones to identify genomic regions involved in speciation.” Molecular Ecology Resources 10.5 (2010): 806-820.

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