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Int J Evol Biol
2011 Jan 01;2011:274975. doi: 10.4061/2011/274975.
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Elevated Evolutionary Rates among Functionally Diverged Reproductive Genes across Deep Vertebrate Lineages.
Grassa CJ
,
Kulathinal RJ
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Among closely related taxa, proteins involved in reproduction generally evolve more rapidly than other proteins. Here, we apply a functional and comparative genomics approach to compare functional divergence across a deep phylogenetic array of egg-laying and live-bearing vertebrate taxa. We aligned and annotated a set of 4,986 1 : 1 : 1 : 1 : 1 orthologs in Anolis carolinensis (green lizard), Danio rerio (zebrafish), Xenopus tropicalis (frog), Gallus gallus (chicken), and Mus musculus (mouse) according to function using ESTs from available reproductive (including testis and ovary) and non-reproductive tissues as well as Gene Ontology. For each species lineage, genes were further classified as tissue-specific (found in a single tissue) or tissue-expressed (found in multiple tissues). Within independent vertebrate lineages, we generally find that gonadal-specific genes evolve at a faster rate than gonadal-expressed genes and significantly faster than non-reproductive genes. Among the gonadal set, testis genes are generally more diverged than ovary genes. Surprisingly, an opposite but nonsignificant pattern is found among the subset of orthologs that remained functionally conserved across all five lineages. These contrasting evolutionary patterns found between functionally diverged and functionally conserved reproductive orthologs provide evidence for pervasive and potentially cryptic lineage-specific selective processes on ancestral reproductive systems in vertebrates.
Figure 1. Protein divergence versus functional class across vertebrate lineages. Boxplots show the distribution of dN, nonsynonymous substitutions per nonsynonymous site in seven functional classes for each of the five species, A. carolinensis, D. rerio, G. gallus, M. musculus, and X. tropicalis. The three tissue-specific classes are found on the top (nonshaded), tissue-expressed classes are below in grey, and the non-reproductive functional class is indicated on the bottom, in black. Asterisks on the right-hand side of a boxplot signifies a highly significant (P < 0.001) difference in mean, as given by the Wilcoxon rank sum test, when compared to the non-reproductive class. No ovary-specific genes were identified in M. musculus.
Figure 2. Venn diagrams of common functionally conserved genes across all five vertebrate species. For each of the seven functional classes, the number of genes found in all combination of species intersections and exclusions are listed. (a) testis-specific, (b) ovary-specific, (c) gonadal-specific, (d) testis-expressed, (e) ovary-expressed, (f) gonadal-expressed, (g) non-reproductive.
Figure 3. dN among functionally conserved classes across all five vertebrate species. Only four of the seven functional classes contained genes that were found in the same functional class across zebrafish, Anolis, Xenopus, chicken, and mouse. Functional classes were not significantly different from each other.
Figure 4. Word-size frequency distribution of Gene Ontology (GO) terms for the most diverged orthologs in A. carolinensis. Associated GO terms for the top 10% diverged ortholog subset are displayed according to size, based on the frequency of that term. GO terms from Biological Process (BP) and Cellular Component (CC) were used. Similar GO-based word-size frequencies based on 10% most diverged orthologs from M. musculus, G. gallus, and D. rerio are found in Supplementary Figure 2.
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