Abstract
BackgroundMany genes involved in the sex determining cascade have indicated signals of positive selection and rapid evolution across different species. Even though fruitless is an important gene involved mostly in several aspects of male courtship behavior, the few studies so far have explained its high rates of evolution by relaxed selective constraints. This would indicate that a large portion of this gene has evolved neutrally, contrary to what has been observed for other genes in the sex cascade.ResultsHere we test whether the fruitless gene has evolved neutrally or under positive selection in species of Anastrepha (Tephritidae: Diptera) using two different approaches, a long-term evolutionary analysis and a populational genetic data analysis. The first analysis was performed by using sequences of three species of Anastrepha and sequences from several species of Drosophila using the ratio of nonsynonymous to synonymous rates of evolution in PAML, which revealed that the fru region here studied has evolved by positive selection. Using Bayes Empirical Bayes we estimated that 16 sites located in the connecting region of the fruitless gene were evolving under positive selection. We also investigated for signs of this positive selection using populational data from 50 specimens from three species of Anastrepha from different localities in Brazil. The use of standard tests of selection and a new test that compares patterns of differential survival between synonymous and nonsynonymous in evolutionary time also provide evidence of positive selection across species and of a selective sweep for one of the species investigated.ConclusionsOur data indicate that the high diversification of fru connecting region in Anastrepha flies is due at least in part to positive selection, not merely as a consequence of relaxed selective constraint. These conclusions are based not only on the comparison of distantly related taxa that show long-term divergence time, but also on recently diverged lineages and suggest that episodes of adaptive evolution in fru may be related to sexual selection and/or conflict related to its involvement in male courtship behavior.
Highlights
Many genes involved in the sex determining cascade have indicated signals of positive selection and rapid evolution across different species
Long-term evolutionary analyses and positive selection in fru For the long-term evolutionary study of the fru connecting region, we amplified a region of 802 bp containing an 81 bp intron (I3 intron) and 721 bp of the first exon from the connecting region (C3 exon) from three closely related Anastrepha species (A. fraterculus, A. sororcula and A. obliqua) (Figure 1B)
The relaxed branch-site test rejected the null model of selective constraint (0 < ω ≤ 1) indicating that the foreground branch (Figure 2) diverged in this region by relaxed selective constraint or by positive selection (Table 2)
Summary
Many genes involved in the sex determining cascade have indicated signals of positive selection and rapid evolution across different species. Even though fruitless is an important gene involved mostly in several aspects of male courtship behavior, the few studies so far have explained its high rates of evolution by relaxed selective constraints This would indicate that a large portion of this gene has evolved neutrally, contrary to what has been observed for other genes in the sex cascade. In Diptera, transformer (tra) and doublesex (dsx) are two of the main genes that control sexual differentiation that have been studied [5,9,10,11] Another important gene in the sex-determination cascade is fruitless (fru), which controls the male courtship behavior by the establishment and development of a male-specific neuronal circuitry [12,13,14] along with dsx [15]. In addition to the sex-specific transcripts, sex-nonspecific products are expressed by three different promoters (P2, P3 and P4) downstream to the exon S, which confers to fru a complex pattern of expression in different tissues and stages of the development [18,19] (Figure 1C)
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