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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.
Aguadé,
Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila.
1999, Pubmed
Aguadé,
Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila.
1999,
Pubmed Aguadé,
Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila.
1992,
Pubmed Altschul,
Basic local alignment search tool.
1990,
Pubmed Andrews,
Gene discovery using computational and microarray analysis of transcription in the Drosophila melanogaster testis.
2000,
Pubmed Bauer DuMont,
Recurrent positive selection at bgcn, a key determinant of germ line differentiation, does not appear to be driven by simple coevolution with its partner protein bam.
2007,
Pubmed Begun,
Molecular population genetics of male accessory gland proteins in Drosophila.
2000,
Pubmed Boul,
Sexual selection drives speciation in an Amazonian frog.
2007,
Pubmed Castillo-Davis,
The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint.
2004,
Pubmed Castillo-Davis,
GeneMerge--post-genomic analysis, data mining, and hypothesis testing.
2003,
Pubmed Chapman,
Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies.
2004,
Pubmed Civetta,
High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species.
1995,
Pubmed Civetta,
Sex-related genes, directional sexual selection, and speciation.
1998,
Pubmed Civetta,
Rapid evolution and gene-specific patterns of selection for three genes of spermatogenesis in Drosophila.
2006,
Pubmed Coulthart,
High level of divergence of male-reproductive-tract proteins, between Drosophila melanogaster and its sibling species, D. simulans.
1988,
Pubmed Dean,
Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus).
2009,
Pubmed Edgar,
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
2004,
Pubmed Good,
Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis.
2005,
Pubmed Haerty,
Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila.
2007,
Pubmed Haerty,
Gene regulation divergence is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila.
2006,
Pubmed Harcourt,
Sexual selection and genital anatomy of male primates.
1994,
Pubmed Hedges,
Molecular evidence for the origin of birds.
1994,
Pubmed Jagadeeshan,
Rapidly evolving genes of Drosophila: differing levels of selective pressure in testis, ovary, and head tissues between sibling species.
2005,
Pubmed Korber,
Immunoinformatics comes of age.
2006,
Pubmed Kulathinal,
The molecular basis of speciation: from patterns to processes, rules to mechanisms.
2008,
Pubmed Kulathinal,
The nature of genetic variation in sex and reproduction-related genes among sibling species of the Drosophila melanogaster complex.
2004,
Pubmed Kulathinal,
CYTOLOGICAL CHARACTERIZATION OF PREMEIOTIC VERSUS POSTMEIOTIC DEFECTS PRODUCING HYBRID MALE STERILITY AMONG SIBLING SPECIES OF THE DROSOPHILA MELANOGASTER COMPLEX.
1998,
Pubmed Lawniczak,
A genome-wide analysis of courting and mating responses in Drosophila melanogaster females.
2004,
Pubmed Lawniczak,
Molecular population genetics of female-expressed mating-induced serine proteases in Drosophila melanogaster.
2007,
Pubmed Lynch,
The evolutionary fate and consequences of duplicate genes.
2000,
Pubmed Lynch,
The probability of duplicate gene preservation by subfunctionalization.
2000,
Pubmed McGraw,
Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster.
2004,
Pubmed Michalak,
Genome-wide patterns of expression in Drosophila pure species and hybrid males.
2003,
Pubmed Mueller,
Cross-species comparison of Drosophila male accessory gland protein genes.
2005,
Pubmed Nei,
Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
1986,
Pubmed Panhuis,
Molecular evolution and population genetic analysis of candidate female reproductive genes in Drosophila.
2006,
Pubmed Parisi,
A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults.
2004,
Pubmed Presgraves,
Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila.
2003,
Pubmed Ram,
Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins.
2007,
Pubmed Reese,
Genome annotation assessment in Drosophila melanogaster.
2000,
Pubmed Roux,
Developmental constraints on vertebrate genome evolution.
2008,
Pubmed Salzburger,
The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics.
2004,
Pubmed Shirangi,
Rapid evolution of sex pheromone-producing enzyme expression in Drosophila.
2009,
Pubmed Singh,
Sex gene pool evolution and speciation: a new paradigm.
2000,
Pubmed Singh,
Male sex drive and the masculinization of the genome.
2005,
Pubmed Swanson,
The rapid evolution of reproductive proteins.
2002,
Pubmed Swanson,
Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila.
2001,
Pubmed Taylor,
Comparative genomics provides evidence for an ancient genome duplication event in fish.
2001,
Pubmed
,
Xenbase Tsaur,
Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism.
1998,
Pubmed Turner,
Comparative analysis of testis protein evolution in rodents.
2008,
Pubmed Wong,
Sexual behavior: a seminal peptide stimulates appetites.
2006,
Pubmed
