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. 2009 Dec 16:9:291.
doi: 10.1186/1471-2148-9-291.

Molecular evolution of sex-biased genes in the Drosophila ananassae subgroup

Sonja Grath  1 , John F Baines, John Parsch
Affiliations

Molecular evolution of sex-biased genes in the Drosophila ananassae subgroup

Sonja Grath et al. BMC Evol Biol. .

Abstract

Background: Genes with sex-biased expression often show rapid molecular evolution between species. Previous population genetic and comparative genomic studies of Drosophila melanogaster and D. simulans revealed that male-biased genes have especially high rates of adaptive evolution. To test if this is also the case for other lineages within the melanogaster group, we investigated gene expression in D. ananassae, a species that occurs in structured populations in tropical and subtropical regions. We used custom-made microarrays and published microarray data to characterize the sex-biased expression of 129 D. ananassae genes whose D. melanogaster orthologs had been classified previously as male-biased, female-biased, or unbiased in their expression and had been studied extensively at the population-genetic level. For 43 of these genes we surveyed DNA sequence polymorphism in a natural population of D. ananassae and determined divergence to the sister species D. atripex and D. phaeopleura.

Results: Sex-biased expression is generally conserved between D. melanogaster and D. ananassae, with the majority of genes exhibiting the same bias in the two species. However, about one-third of the genes have either gained or lost sex-biased expression in one of the species and a small proportion of genes (approximately 4%) have changed bias from one sex to the other. The male-biased genes of D. ananassae show evidence of positive selection acting at the protein level. However, the signal of adaptive protein evolution for male-biased genes is not as strong in D. ananassae as it is in D. melanogaster and is limited to genes with conserved male-biased expression in both species. Within D. ananassae, a significant signal of adaptive evolution is also detected for female-biased and unbiased genes.

Conclusions: Our findings extend previous observations of widespread adaptive protein evolution to an independent Drosophila lineage, the D. ananassae subgroup. However, the rate of adaptive evolution is not greater for male-biased genes than for female-biased or unbiased genes, which suggests that there are differences in sex-biased gene evolution between the two lineages.

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Figures

Figure 1
Figure 1
Conservation of sex-biased gene expression between D. melanogaster and D. ananassae. Panel A shows the overall conservation of sex-biased expression between the two species. Panel B shows the conservation of the specific sex-bias classes, with the first letter indicating the bias in D. ananassae and the second letter indicating the bias in D. melanogaster. "M" indicates male-biased, "F" indicates female-biased, and "U" indicates unbiased expression. The area of the chart taken up by each category indicates the percentage of genes falling into that category. The number of genes in each category is given in parentheses.
Figure 2
Figure 2
Phylogeny. 50% majority-rule consensus tree generated from concatenated amino acid sequences of 12 genes (3,446 sites) and Bayesian inference analysis (10,000 generations). Identical topologies were recovered in two independent runs of MrBayes [37]. Numbers at the nodes indicate posterior clade probabilities.
Figure 3
Figure 3
Maximum likelihood estimates of the fraction of positively selected amino acid replacements (α). Values of α for genes with male-, female-, and unbiased expression were calculated using a maximum likelihood method [17]. Genes with conserved bias between D. ananassae and D. melanogaster are indicated with solid boxes, genes with bias according to classification in D. ananassae (i.e. including conserved genes and genes with bias private to D. ananassae) are indicated with open boxes. Low frequency polymorphisms (≤ 15%) were excluded. Error bars indicate 95% CI. Asterisks indicate genes with a significant signal of positive selection (*P < 0.05, **P < 0.01).
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