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

Abstract

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.

Figure 1

Percentage of Drosophila melanogaster testis-biased and non-testis-biased expressed genes in two different gene expression datasets. Testis-biased expression profiles for D. melanogaster genes were obtained from Metta and Schlötterer [21]. Segmental dataset corresponds to the 21 movement cases selected by Metta and Schlötterer [21] from the original 46 cases in [23]. Excluded dataset corresponds to the remaining 26 cases. The number of testis-biased genes is significantly higher in the excluded dataset (**Fisher exact test, p = 0.0025), which implies that the filter used by Metta, and Schlötterer [21] disproportionally selected less testis-biased genes in the segmental dataset.

Figure 2

Significant sex-biased gene expression. Adapted from Table 2 in [21]. Dsim: D. simulans; Dyak: D. yakuba; Dana: D. ananassae; Dpse: D. pseudoobscura; Dvir: D. virilis; Dmoj: D. mojavensis. Significant female- and male-biased expression is represented in red and blue, respectively. Female-biased expressed genes located on the X chromosome are shown in grey boxes. Retrogenes and parental genes are shown in “R” and “P”, respectively. Same sex-biased expression can be divided in: no sex-biased expression and female-biased expression for all orthologs analyzed. “-” corresponds to cases where orthologos do not show the same sex-biased expression. “na” refers to no expression data available.