The correlation between intron length and recombination in drosophila: Dynamic equilibrium between mutational and selective forces

Intron length is negatively correlated with recombination in both Drosphila melanogaster and humans. This correlation is not likely to be the result o f mutational processes alone: evolutionary analysis of intron length polymo rphism in D. melanogaster reveals equivalent ratios of deletion to insertio n in regions of high and low recombination. The polymorphism data do reveal , however, an excess of deletions relative to insertions (i.e., a deletion bias), with an overall deletion-tu-insertion events ratio of 1.35. We propo se two types of selection favoring longer intron lengths. First, the natura l mutational bias toward deletion must be opposed by strong selection in ve ry short introns to maintain the minimum intron length needed for the intro n splicing reaction. Second, selection will favor insertions in introns tha t increase recombination between mutations under die influence of selection in adjacent exons. Mutations that increase recombination, even slightly, w ill be selectively favored because they reduce interference among selected mutations. Interference selection acting on intron length mutations must be very weak, as indicated by frequency spectrum analysis of Drosophila intro n length polymorphism, making the equilibrium for intron length sensitive t o changes in thr recombinational environment and population size. One conse quence of this sensitivity is that the advantage of longer introns is expec ted to decrease inversely with the rate of recombination, thus leading to a negative correlation between intron length and recombination rate. Also in accord with this model, intron length differs between closely related Dros ophila species,with the longest variant present more often in D. melanogast er than in D. simulans. We suggest that the study of the proposed dynamic m odel, taking into account interference among selected sites, might shed lig ht on many aspects of the comparative biology of genome sizes including the C value paradox.