Adaptive Evolution Is Substantially Impeded by Hill–Robertson Interference inDrosophila

Abstract

Hill–Robertson interference (HRi) is expected to reduce the efficiency of natural selection when two or more linked selected sites do not segregate freely, but no attempt has been done so far to quantify the overall impact of HRi on the rate of adaptive evolution for any given genome. In this work, we estimate how much HRi impedes the rate of adaptive evolution in the coding genome of Drosophila melanogaster. We compiled a data set of 6,141 autosomal protein-coding genes from Drosophila, from which polymorphism levels in D. melanogaster and divergence out to D. yakuba were estimated. The rate of adaptive evolution was calculated using a derivative of the McDonald–Kreitman test that controls for slightly deleterious mutations. We find that the rate of adaptive amino acid substitution at a given position of the genome is positively correlated to both the rate of recombination and the mutation rate, and negatively correlated to the gene density of the region. These correlations are robust to controlling for each other, for synonymous codon bias and for gene functions related to immune response and testes. We show that HRi diminishes the rate of adaptive evolution by approximately 27%. Interestingly, genes with low mutation rates embedded in gene poor regions lose approximately 17% of their adaptive substitutions whereas genes with high mutation rates embedded in gene rich regions lose approximately 60%. We conclude that HRi hampers the rate of adaptive evolution in Drosophila and that the variation in recombination, mutation, and gene density along the genome affects the HRi effect.

Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila

“…Among the 807 TEs located in regions with high recombination rates, 215 were fixed and 177 were present at low frequencies (LowFreq), defined here as being present at ≤ 10% frequency in each of the analyzed samples (Fig 2). Note that the percentage of fixed TEs in high recombination regions is significantly lower than the percentage in low recombination regions (27% vs 79% respectively, Chi-squared p-value = 2.2 e-16 ), as expected if the efficiency of selection is lower in low recombination regions, and slightly deleterious TEs reached fixation neutrally [37, 38]. Finally, 300 of the 807 TEs located in high recombination regions were present at high frequencies (HighFreq), defined here as being present at < 95% frequency overall and at >10% frequency in at least three samples (Fig 2, S1 Fig).…”

“…In addition, among all the TEs present at high frequencies, TEs located in regions with high recombination rates are less likely to have increased in frequency neutrally compared with TEs located in low recombination regions. This is so because the efficiency of selection in genomic regions with low recombination rates tends to be lower due to the increase in noise generated by linked selection such as background selection and recurrent selective sweeps [37, 38]. Moreover, TEs located in low recombination regions are more likely to be linked to an adaptive mutation rather than being the causal mutation [33-35].…”

“…In this work, we identified 300 TEs present at high frequencies in natural populations, and located in genomic regions with high recombination, where the efficiency of selection is high [37, 38]. Most of these TEs are young insertions suggesting that they have increased in frequency relatively fast (Fig 3).…”

A novel method for quantifying the rate of embryogenesis uncovers considerable genetic variation for the duration of embryonic development in Drosophila melanogaster

“…Genes that are involved in highly conserved functions, such as developmental patterning and morphogenesis, are expected to be highly constrained [ 61 ]. Instead, altering the expression of crucial developmental genes through chromatin modifications or changes in transcription factor binding activity is a safer, yet effective way to control phenotypes.…”

Detecting positive selection in the genome

“…Since N e for a genomic region is positively related to the rate of recombination [ 20 ], increased rates of fixation of advantageous mutations and decreased rates of fixation of deleterious mutations are expected in high recombination regions. Campos et al also observed that the rate of recombination is positively correlated with ω a , the estimated rate of advantageous substitution relative to the rate of neutral substitution (Box 1), suggesting that beneficial substitutions increase with increasing recombination rate, perhaps due to decreasing interference between selected loci [ 21 ].…”