Abstract
The gene doublesex (dsx) is considered to be under strong selective constraint along its evolutionary history because of its central role in somatic sex differentiation in insects. However, previous studies of dsx used global estimates of evolutionary rates to investigate its molecular evolution, which potentially miss signals of adaptive changes in generally conserved genes. In this work, we investigated the molecular evolution of dsx in the Anastrepha fraterculus species group (Diptera, Tephritidae), and test the hypothesis that this gene evolved solely by purifying selection using divergence-based and population-based methods. In the first approach, we compared sequences from Anastrepha and other Tephritidae with other Muscomorpha species, analyzed variation in nonsynonymous to synonymous rate ratios (dN/dS) in the Tephritidae, and investigated radical and conservative changes in amino acid physicochemical properties. We show a general selective constraint on dsx, but with signs of positive selection mainly in the common region. Such changes were localized in alpha-helices previously reported to be involved in dimer formation in the OD2 domain and near the C-terminal of the OD1 domain. In the population-based approach, we amplified a region of 540 bp that spanned almost all of the region common to both sexes from 32 different sites in Brazil. We investigated patterns of selection using neutrality tests based on the frequency spectrum and locations of synonymous and nonsynonymous mutations in a haplotype network. As in the divergence-based approach, these analyses showed that dsx has evolved under an overall selective constraint, but with some events of positive selection. In contrast to previous studies, our analyses indicate that even though dsx has indeed evolved as a conserved gene, the common region of dsx has also experienced bouts of positive selection, perhaps driven by sexual selection, during its evolution.
Highlights
Even though several genes involved with premeiotic aspects of reproduction are exceptionally conserved throughout evolution [1], many genes related to reproduction in animals and plants are among the most divergent, evolving faster than those not related to sexual traits [2], possibly because of sexual selection and/or sexual conflict [3,4]
The signals of positive selection were evident in sites outside the DM/OD1 and OD2 domains, as indicated by the Bayes Empirical Bayes analyses (Figure 3)
Even though the contrast of model A vs B failed to show significant differences in their substitution rates when we compared the common region to the male-specific exon, models B and C were rejected in the contrasts B vs D and C vs E, respectively (Table 2), which may have been caused by significant
Summary
Even though several genes involved with premeiotic aspects of reproduction are exceptionally conserved throughout evolution [1], many genes related to reproduction in animals and plants are among the most divergent, evolving faster than those not related to sexual traits [2], possibly because of sexual selection and/or sexual conflict [3,4]. Most molecular studies so far have concentrated on genes involved in fertilization or male-female interaction and only a few on genes responsible for sexual differentiation. DSX is a transcription factor that acts by activating or repressing genes downstream in the cascade that are responsible for the development of male or female traits in insects [14]. This gene is functionally conserved among insects and other animals and, differently from other genes involved with sex determination [15,16,17], it occupies a conserved position at the bottom of the cascade [18,19]. Dsx may be subject to sexual selection since it is involved in many aspects of reproduction and sexual behavior [23] and, as a consequence, could show signs of positive selection
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