Segmental dataset and whole body expression data do not support the hypothesis that non-random movement is an intrinsic property of Drosophila retrogenes

BMC Evolutionary Biology, Sep 2012

Background Several studies in Drosophila have shown excessive movement of retrogenes from the X chromosome to autosomes, and that these genes are frequently expressed in the testis. This phenomenon has led to several hypotheses invoking natural selection as the process driving male-biased genes to the autosomes. Metta and Schlötterer (BMC Evol Biol 2010, 10:114) analyzed a set of retrogenes where the parental gene has been subsequently lost. They assumed that this class of retrogenes replaced the ancestral functions of the parental gene, and reported that these retrogenes, although mostly originating from movement out of the X chromosome, showed female-biased or unbiased expression. These observations led the authors to suggest that selective forces (such as meiotic sex chromosome inactivation and sexual antagonism) were not responsible for the observed pattern of retrogene movement out of the X chromosome. Results We reanalyzed the dataset published by Metta and Schlötterer and found several issues that led us to a different conclusion. In particular, Metta and Schlötterer used a dataset combined with expression data in which significant sex-biased expression is not detectable. First, the authors used a segmental dataset where the genes selected for analysis were less testis-biased in expression than those that were excluded from the study. Second, sex-biased expression was defined by comparing male and female whole-body data and not the expression of these genes in gonadal tissues. This approach significantly reduces the probability of detecting sex-biased expressed genes, which explains why the vast majority of the genes analyzed (parental and retrogenes) were equally expressed in both males and females. Third, the female-biased expression observed by Metta and Schlötterer is mostly found for parental genes located on the X chromosome, which is known to be enriched with genes with female-biased expression. Fourth, using additional gonad expression data, we found that autosomal genes analyzed by Metta and Schlötterer are less up regulated in ovaries and have higher chance to be expressed in meiotic cells of spermatogenesis when compared to X-linked genes. Conclusions The criteria used to select retrogenes and the sex-biased expression data based on whole adult flies generated a segmental dataset of female-biased and unbiased expressed genes that was unable to detect the higher propensity of autosomal retrogenes to be expressed in males. Thus, there is no support for the authors’ view that the movement of new retrogenes, which originated from X-linked parental genes, was not driven by selection. Therefore, selection-based genetic models remain the most parsimonious explanations for the observed chromosomal distribution of retrogenes.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

http://www.biomedcentral.com/content/pdf/1471-2148-12-169.pdf

Segmental dataset and whole body expression data do not support the hypothesis that non-random movement is an intrinsic property of Drosophila retrogenes

BMC Evolutionary Biology Segmental dataset and whole body expression data do not support the hypothesis that non-random movement is an intrinsic property of Drosophila retrogenes Maria D Vibranovski 0 1 Yong E Zhang 0 Claus Kemkemer 0 Nicholas W VanKuren 0 Hedibert F Lopes Timothy L Karr Manyuan Long 0 0 Department of Ecology and Evolution, University of Chicago , Chicago, IL 60637 , USA 1 Current address: Departamento de Genetica e Biologia Evolutiva, Instituto de Biociencias Universidade de Sao Paulo , Sao Paulo, SP 05508-090 , Brazil Background: Several studies in Drosophila have shown excessive movement of retrogenes from the X chromosome to autosomes, and that these genes are frequently expressed in the testis. This phenomenon has led to several hypotheses invoking natural selection as the process driving male-biased genes to the autosomes. Metta and Schltterer (BMC Evol Biol 2010, 10:114) analyzed a set of retrogenes where the parental gene has been subsequently lost. They assumed that this class of retrogenes replaced the ancestral functions of the parental gene, and reported that these retrogenes, although mostly originating from movement out of the X chromosome, showed female-biased or unbiased expression. These observations led the authors to suggest that selective forces (such as meiotic sex chromosome inactivation and sexual antagonism) were not responsible for the observed pattern of retrogene movement out of the X chromosome. Results: We reanalyzed the dataset published by Metta and Schltterer and found several issues that led us to a different conclusion. In particular, Metta and Schltterer used a dataset combined with expression data in which significant sex-biased expression is not detectable. First, the authors used a segmental dataset where the genes selected for analysis were less testis-biased in expression than those that were excluded from the study. Second, sex-biased expression was defined by comparing male and female whole-body data and not the expression of these genes in gonadal tissues. This approach significantly reduces the probability of detecting sex-biased expressed genes, which explains why the vast majority of the genes analyzed (parental and retrogenes) were equally expressed in both males and females. Third, the female-biased expression observed by Metta and Schltterer is mostly found for parental genes located on the X chromosome, which is known to be enriched with genes with female-biased expression. Fourth, using additional gonad expression data, we found that autosomal genes analyzed by Metta and Schltterer are less up regulated in ovaries and have higher chance to be expressed in meiotic cells of spermatogenesis when compared to X-linked genes. (Continued on next page) - (Continued from previous page) Conclusions: The criteria used to select retrogenes and the sex-biased expression data based on whole adult flies generated a segmental dataset of female-biased and unbiased expressed genes that was unable to detect the higher propensity of autosomal retrogenes to be expressed in males. Thus, there is no support for the authors view that the movement of new retrogenes, which originated from X-linked parental genes, was not driven by selection. Therefore, selection-based genetic models remain the most parsimonious explanations for the observed chromosomal distribution of retrogenes. Background In Drosophila, there is an excess of retrogenes moving from the X chromosome to autosomal regions [1]. Interestingly, those retrogenes are frequently expressed in testis [1]. Both observations have been reported several times in Drosophila melanogaster [1-3], as well as in other species of mammals [4] and mosquitoes [5,6]. In addition, a comparative study between the genomes of twelve Drosophila species revealed excessive movement out of the X chromosome for both retrogenes and DNA-based duplications in the Drosophila genus [7,8]. Further, older genes that originated before the split of the Drosophila and Sophophora subgenera and for which expression is greater in males than females, are underrepresented on the X chromosome [9-12]. The gene movement off the X chromosome likely contributed, along with other mechanisms, to the paucity of X-linked male-biased genes found in Drosophila [11]. Several hypotheses have been proposed to explain the excessive movement of genes out of the X chromosome and the paucity of male-biased X-linked genes [1,13-19]. These hypotheses include (i) meiotic sex chromosome inactivation (MSCI), (ii) dosage compensation, (iii) meiotic drive, and (iv) sexual antagonism, and they all assume that natural selection has favoured accumulation of male-biased genes on the autosomes [1,13-19]. Two of those hypotheses, MSCI and dosage compensation, have been tested and shown to play a role in the genomic relocation of retrogenes expressed in testis [15,16,20]. MSCI is predicated on the hypothesis that retrogenes located on autosomes continue functioning duri (...truncated)


This is a preview of a remote PDF: http://www.biomedcentral.com/content/pdf/1471-2148-12-169.pdf

Maria D Vibranovski, Yong E Zhang, Claus Kemkemer, Nicholas W VanKuren, Hedibert F Lopes, Timothy L Karr, Manyuan Long. Segmental dataset and whole body expression data do not support the hypothesis that non-random movement is an intrinsic property of Drosophila retrogenes, BMC Evolutionary Biology, 2012, pp. 169, 12, DOI: 10.1186/1471-2148-12-169