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Homeobox genes encode transcription factors that play important roles in various developmental processes and are usually evolutionarily conserved. Here we report a case of rapid evolution of a homeobox gene in humans and non-human primates.ESX1is an X-linked homeobox gene primarily expressed in the placenta and testis, with physiological functions in placenta/fetus development and spermatogenesis.ESX1is paternally imprinted in mice, but is not imprinted in humans. We provide evidence for a significantly higher non-synonymous substitution rate than synonymous rate inESX1between humans and chimps as well as among a total of 15 primate species. Population genetic data also show signals of recent selective sweeps within humans. Positive selection appears to be concentrated in the C-terminal non-homeodomain region, which has been implicated in regulating human male germ cell division by prohibiting the degradation of cyclins. In contrast, mouseEsx1has a substantively different C-terminal region subject to strong purifying selection. These and other results suggest that even the fundamental process of spermatogenesis has been targeted by positive selection in primate and human evolution and that mouse may not be a suitable model for studying human reproduction.

Rapid evolution of primate ESX1 , an X-linked placenta- and testis-expressed homeobox gene