Evolutionary Genomics of Colias Phosphoglucose Isomerase (PGI) Introns
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Little is known of intron sequences’ variation in cases where eukaryotic gene coding regions undergo strong balancing selection. Phosphoglucose isomerase, PGI, of Colias butterflies offers such a case. Its 11 introns include many point mutations, insertions, and deletions. This variation changes with intron position and length, and may leave little evidence of homology within introns except for their first and last few basepairs. Intron position is conserved between PGIs of Colias and the silkmoth, but no intron sequence homology remains. % GC content and length are functional properties of introns which can affect whole-gene transcription; we find a relationship between these properties which may indicate selection on transcription speed. Intragenic recombination is active in these introns, as in coding sequences. The small extent of linkage disequilibrium (LD) in the introns decays over a few hundred basepairs. Subsequences of Colias introns match subsequences of other introns, untranslated regions of cDNAs, and insect-related transposons and pathogens, showing that a diverse pool of sequence fragments is the source of intron contents via turnover due to deletion, recombination, and transposition. Like Colias PGI’s coding sequences, the introns evolve reticulately with little phylogenetic signal. Exceptions are coding-region allele clades defined by multiple amino acid variants in strong LD, whose introns are closely related but less so than their exons. Similarity of GC content between introns and flanking exons, lack of small introns despite mutational bias toward deletion, and findings already mentioned suggest constraining selection on introns, possibly balancing transcription performance against advantages of higher recombination rate conferred by intron length.
KeywordsMolecular polymorphism Complex haplotypes Natural variation Intron evolution Glycolysis Linkage disequilibrium Intragenic recombination Transposable elements
We thank Carol Boggs, Mike Bramson, Jason Hill, Jen Johnson, Martin Kreitman, Mark Longo, Dmitri Petrov, Steve Palumbi, and Chris Wheat for comments on the paper or other helpful discussions. We also thank Chris Aakre, Will Bassett, Nina Duong, Daniel Herrador, Alejandro Perez, and Eddie Wang for technical assistance. This work was supported by US National Science Foundation grants DEB 05-20315 and MCB 08-46870 to WBW. Our results do not represent official policy of any agency or corporate entity.
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