Is Genome Complexity a Consequence of Inefficient Selection? Evidence from Intron Creation in Nonrecombining Regions

Genomes show remarkable variation in architecture and complexity across organisms, with large differences in genome size and in numbers of genes, gene duplicates, introns and transposable elements. These differences have important implications for transcriptome and regulatory complexity and ultimately for organismal complexity. Numbers of spliceosomal introns show particularly striking differences, ranging across organisms from zero to hundreds of thousands of introns per genome. The causes of these differences remain poorly understood. According to one influential perspective, differences across species reflect the differential ability of selection in different populations to eliminate allegedly deleterious intron-containing alleles. Direct tests of this theory have been elusive. Here, I study evolution of intron-exon structures in genomic regions of recombination suppression (RRSs), which experience drastically reduced selective efficiency due to hitchhiking and background selection. I studied intron creation in eight independently evolved RRSs, spanning substantial diversity phylogenetically (plants, animals, fungi and brown algae) and biologically (sex chromosomes, mating type chromosomes, genomic regions flanking self-incompatibility loci, and the Drosophila "dot" chromosome). To identify newly created introns in RRSs, I compared intron positions in RRS genes with those in homologous genes. I found very few intron gains: no intron gains were observed in 7/8 studied data sets, and only three intron gains were observed overall (on the Drosophila dot chromosome). These results suggest that efficiency of selection may not be a major cause of differences in intron-exon structures across organisms. Instead, rates of spontaneous intron-creating and intron-deleting mutations may play the central role in shaping intron-exon structures.