Abstract
BackgroundThe mechanism by which duplicate genes originate – whether by duplication of a whole genome or of a genomic segment – influences their genetic fates. To study events that trigger duplicate gene persistence after whole genome duplication in vertebrates, we have analyzed molecular evolution and expression of hundreds of persistent duplicate gene pairs in allopolyploid clawed frogs (Xenopus and Silurana). We collected comparative data that allowed us to tease apart the molecular events that occurred soon after duplication from those that occurred later on. We also quantified expression profile divergence of hundreds of paralogs during development and in different tissues.ResultsOur analyses indicate that persistent duplicates generated by allopolyploidization are subjected to strong purifying selection soon after duplication. The level of purifying selection is relaxed compared to a singleton ortholog, but not significantly variable over a period spanning about 40 million years. Despite persistent functional constraints, however, analysis of paralogous expression profiles indicates that quantitative aspects of their expression diverged substantially during this period.ConclusionThese results offer clues into how vertebrate transcriptomes are sculpted in the wake of whole genome duplication (WGD), such as those that occurred in our early ancestors. That functional constraints were relaxed relative to a singleton ortholog but not significantly different in the early compared to the later stage of duplicate gene evolution suggests that the timescale for a return to pre-duplication levels is drawn out over tens of millions of years – beyond the age of these tetraploid species. Quantitative expression divergence can occur soon after WGD and with a magnitude that is not correlated with the rate of protein sequence divergence. On a coarse scale, quantitative expression divergence appears to be more prevalent than spatial and temporal expression divergence, and also faster or more frequent than other processes that operate at the protein level, such as some types of neofunctionalization.
Highlights
The mechanism by which duplicate genes originate – whether by duplication of a whole genome or of a genomic segment – influences their genetic fates
The likelihood of sequence data can be quantified under a model with no change in the rate ratio of nonsynonymous to synonymous substitution (Ka/Ks ratio) before versus after tetraploid speciation, and it can be compared to the likelihood of an alternative model in which there is a different Ka/Ks ratio during these two stages of duplicate gene evolution
In Xenopus, a concatenated analysis of 80,856 base pairs of expressed paralogs indicates that synonymous substitutions per synonymous site (Ks) between X. laevis paralogs (XLα and XLβ in Fig. 1B) is 0.2111, and Ks between the alpha paralogs of X. laevis and X. borealis (XLα and XBα in Fig. 1B) is 0.1393
Summary
The mechanism by which duplicate genes originate – whether by duplication of a whole genome or of a genomic segment – influences their genetic fates. To study events that trigger duplicate gene persistence after whole genome duplication in vertebrates, we have analyzed molecular evolution and expression of hundreds of persistent duplicate gene pairs in allopolyploid clawed frogs (Xenopus and Silurana). It appears that mechanisms that promote duplicate gene persistence in polyploid genomes are either different from or more effective than those that operate on duplicated genes generated by segmental duplication. This is probably because mechanisms specific to polyploid genomes, such as stoichiometric requirements/genic balance, increase their longevity [6,7,8,9], whereas characteristics specific to segmental duplicates, such as incomplete coding regions and regulatory elements decrease theirs [10]. Segmental duplicates begin as polymorphisms whose probability of fixation and time to fixation depend on genetic drift and natural selection [14]
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