Abstract
BackgroundGene duplicates often exhibit asymmetric rates of molecular evolution in their early evolutionary existence. This asymmetry in rates is thought to signify the maintenance of the ancestral function by one copy and the removal of functional constraint on the other copy, enabling it to embark on a novel evolutionary trajectory. Here I focused on a large population of evolutionarily young gene duplicates (KS ≤ 0.14) in the Caenorhabditis elegans genome in order to conduct the first combined analysis of four predictors (evolutionary age, chromosomal location, structural resemblance between duplicates, and duplication span) which may be implicated in the asymmetric sequence divergence of paralogs at the nucleotide and amino acid level. In addition, I investigate if either paralog is equally likely to embark on a trajectory of accelerated sequence evolution or whether the derived paralog is more likely to exhibit faster sequence evolution.ResultsThree predictors (evolutionary age of duplicates, chromosomal location and duplication span) serve as major determinants of sequence asymmetry between C. elegans paralogs. Paralogs diverge asymmetrically in sequence with increasing evolutionary age, the relocation of one copy to a different chromosome and attenuated duplication spans that likely fail to capture the entire ancestral repertoire of coding sequence and regulatory elements. Furthermore, for paralogs residing on the same chromosome, opposite transcriptional orientation and increased genomic distance do not increase sequence asymmetry between paralogs. For a subset of duplicate pairs wherein the ancestral versus derived paralog could be distinguished, the derived paralogs are more likely to evolve at accelerated rates.ConclusionsThis genome-wide study of evolutionarily young duplicates stemming primarily from DNA-mediated small-scale duplication events demonstrates that genomic relocation to a new chromosome has important consequences for asymmetric divergence of paralogs, akin to paralogs arising from RNA-mediated duplication events. Additionally, the duplication span is negatively correlated with sequence rate asymmetry among paralogs, suggesting that attenuated duplication spans stemming from incomplete duplication of the ORF and/or ancestral regulatory elements further accelerate sequence divergence between paralogs. Cumulatively, derived copies exhibit accelerated rates of sequence evolution suggesting that they are primed for a divergent evolutionary trajectory by changes in structure and genomic context at inception.
Highlights
Gene duplicates often exhibit asymmetric rates of molecular evolution in their early evolutionary existence
Of the initial 290 gene duplicate pairs with low synonymous site divergence (KS ≤ 0.10) within the C. elegans genomic data set of Katju and Lynch [35,36], 63 of the initial 290 pairs were no longer consider valid paralogs in Wormbase WS214 owing to one of the following conditions: (i) alterations to the ORF(s) of one or both paralogs such that they no longer appeared homologous in their coding regions, or (ii) one or both paralogs retired/killed/superseded
These results suggest that sequence asymmetry at the DNA sequence level is positively correlated with increasing evolutionary age
Summary
Gene duplicates often exhibit asymmetric rates of molecular evolution in their early evolutionary existence. This asymmetry in rates is thought to signify the maintenance of the ancestral function by one copy and the removal of functional constraint on the other copy, enabling it to embark on a novel evolutionary trajectory. Recent whole-genome sequencing of Saccharomyces cerevisiae [12] and comparative genome hybridization of Caenorhabditis elegans [13] experimental lines maintained under strict bottlenecking conditions to permit the accumulation of mutations under relaxed selective constraints have provided the most robust direct estimates of the spontaneous gene duplication rate. The contribution of CNVs and other structural variants to intraspecific polymorphism is thought to vastly exceed that of SNPs [5]
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