No Accelerated Rate of Protein Evolution in Male-Biased <i>Drosophila pseudoobscura</i> Genes

Metta, Muralidhar; Gudavalli, Rambabu; Gibert, Jean‐Michel; Schlötterer, Christian

doi:10.1534/genetics.106.057414

Cited by 33 publications

(43 citation statements)

References 58 publications

(65 reference statements)

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“…Non-sex-biased genes show intermediate average K a /K s ratios that are significantly higher than those of female-biased genes (P ¼ 2.16 3 10 À4 ). These observations are not consistent with previous findings for a small set of genes that are only male biased in D. pseudoobscura but not in D. melanogaster (Metta et al 2006).…”

Section: Resultscontrasting

confidence: 99%

Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Jiang

Machado

2009

Genetics

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Sexual dimorphism in morphological, physiological, and behavioral traits is pervasive in animals, as is the observation of strong sexual dimorphism in genomewide patterns of gene expression in the few species where this has been studied. Studies of transcriptome divergence show that most interspecific transcriptional divergence is highly sex dependent, an observation consistent with the action of sexdependent natural selection during species divergence. However, few transcriptome evolution studies have been conducted between recently diverged species (,1 MY). Here, we present analyses of sex-biased transcriptome divergence in sexually mature adults of three recently diverged species of Drosophila: Drosophila pseudoobscura, D. persimilis, and D. pseudoobscura bogotana. Data were collected using a custom designed Agilent oligonucleotide. Expression was detected in 12,507 genes. About 80% of the expressed genes show sex-biased expression in each species. Across species, 21% of the transcriptome shows switches between nonsex bias and sex bias, and just 0.9% of the transcriptome shows reversals of sex-biased expression. Over 80% of the expression divergence between species is due to changes in one sex only. About 15% of the expression divergence between species is due to changes in the same direction in both sexes and just 2% is due to changes in both sexes but in opposite directions. In agreement with previous studies, we observe a high level of sex-dependent transcriptome divergence and strong demasculinization of the two arms of the X chromosome in all species. However, in contrast to previous studies we find that male-biased genes do not have higher levels of expression divergence than non-sex-biased genes, and sexbiased genes show higher levels of expression divergence in the alternate sex, suggesting that sex-biased genes endure stronger selection when expressed in the alternate sex.

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Section: Resultscontrasting

confidence: 99%

Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Jiang

Machado

2009

Genetics

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“…This failure to reject selective neutrality at the DNA sequence level of the 5 prime regions raises the interesting question how selection appears to be so obvious a factor driving population differentiation at the level of gene expression (c.f. also Fay and Wittkopp (2008), Hahn (2007), Holloway et al (2007), Lemos et al (2005), Meiklejohn et al (2003), Metta et al (2006), Ranz and Machado (2006), Townsend et al (2003), Whitehead and Crawford (2006a;2006b), Wray (2003), Wray et al (2003)), as it has been for other complex traits in other studies, yet so elusive at the sequence level. A few studies that were able to document the role of 5 prime sequences in governing expression and phenotypes were able to document selection at the sequence level, however, suggesting both selection and drift can promote the differentiation among natural populations in expression and sequence (Edwards et al, 2006;Fang et al, 2002;Weber et al, 2007).…”

Section: Resultsmentioning

confidence: 93%

Decoupled differentiation of gene expression and coding sequence among Drosophila populations

Kohn

Shapiro

2008

Genes Genet. Syst.

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Owing to the relevance to evolutionary theories of genotypic and phenotypic evolution, the correspondence of differentiation among natural populations in complex phenotypic traits and genetic markers has been studied extensively, and generally found to be poor. In contrast, the correspondence of differentiation among natural populations in gene expression, now often considered a genomic era proxy for the phenotype, and genetic markers, remains largely unexplored. Here, an analysis of expression and nucleotide sequence polymorphism of 106 genes in Drosophila melanogaster strains of the Cosmopolitan (M) and Zimbabwe, Africa (Z) mating races showed that differentiation of gene expression and of coding sequences, measured as Q ST and G ST , respectively, were uncorrelated and, generally, Q ST > G ST . However, an exploratory analysis showed that G ST of the 5 prime sequences of genes was correlated with Q ST calculated from expression data, while G ST of the coding sequences remained uncorrelated with Q ST . This scenario is consistent with the population differentiation at cis-regulatory regions that is decoupled from differentiation of the coding regions. However, despite evidence for selection on global levels of gene expression (deduced from Q ST > G ST ), 5 prime sequence polymorphisms generally were compatible with selective neutrality, suggesting differentiation in cis-regulated gene expression for these genes has been promoted by drift or selection too weak or too long ago to be detected, or higher organizational levels underlying the genetic architecture of expression are targets of selection. In all, this raises the question how selection on the expression changes (i.e. the phenotype) can be so obvious yet elusive at the level of the nucleotide sequence. Our contrasts between genetic differentiation of populations in expression and sequences revealed that even when genotype and phenotype can be connected the sources of variation that are the target of selection remain to be identified.

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“…The greater proportion of male D. melanogaster reproductive genes lacking detectable orthologs in distantly related Drosophila species suggests a higher rate of gain/loss. This may be due to lineage-specific duplications or faster rates of new genes being co-opted into reproductive functions, leading to loss of orthology due to various selective pressures (True and Carroll 2002;Ranz et al 2003;Metta et al 2006). Alternatively, lost orthology may be a result of faster sequence divergence of male reproductive genes as previously observed between D. melanogaster and D. pseudoobscura (Mueller et al 2005;Musters et al 2006).…”

Section: Discussionmentioning

confidence: 92%

Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila

et al. 2007

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A large portion of the annotated genes in Drosophila melanogaster show sex-biased expression, indicating that sex and reproduction-related genes (SRR genes) represent an appreciable component of the genome. Previous studies, in which subsets of genes were compared among few Drosophila species, have found that SRR genes exhibit unusual evolutionary patterns. Here, we have used the newly released genome sequences from 12 Drosophila species, coupled to a larger set of SRR genes, to comprehensively test the generality of these patterns. Among 2505 SRR genes examined, including ESTs with biased expression in reproductive tissues and genes characterized as involved in gametogenesis, we find that a relatively high proportion of SRR genes have experienced accelerated divergence throughout the genus Drosophila. Several testis-specific genes, male seminal fluid proteins (SFPs), and spermatogenesis genes show lineage-specific bursts of accelerated evolution and positive selection. SFP genes also show evidence of lineage-specific gene loss and/ or gain. These results bring us closer to understanding the details of the evolutionary dynamics of SRR genes with respect to species divergence.

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No Accelerated Rate of Protein Evolution in Male-Biased Drosophila pseudoobscura Genes

Cited by 33 publications

References 58 publications

Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Decoupled differentiation of gene expression and coding sequence among Drosophila populations

Evolution in the Fast Lane: Rapidly Evolving Sex-Related Genes in Drosophila

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