Erratic evolution of SRY in higher primates.

Abstract

SRY, a Y-chromosomal gene that is pivotal in initiating the development of testis and a determinant of male sex in mammals (Goodfellow and Lovell-Badge 1993), has been subject to intense evolutionary study in the past decade (Foster et al. 1992; Tucker and Lundrigan 1993; Whitfield, Lovell-Badge, and Goodfellow 1993; Pamilo and O’Neill 1997; Nagai 2001). SRY protein is a transcription factor containing the conserved DNA-binding HMG domain (;78 amino acids) in the middle of the sequence and highly variable Nand Cterminal sequences (Whitfield, Lovell-Badge, and Goodfellow 1993). A higher rate of nonsynonymous nucleotide substitution than that of synonymous substitution in the terminal regions of SRY has been reported in primates and rodents, with suggestions that these regions may be subject to positive Darwinian selection (Tucker and Lundrigan 1993; Whitfield, Lovell-Badge, and Goodfellow 1993). Here, we sequence the SRY genes of nine Old World (OW) monkeys and show that the evolution of the SRY has been significantly decelerated in these species. Thus, the SRY shows a complex pattern of erratic evolution among different groups of primates, raising an intriguing possibility of varied selective pressures on this fundamentally important gene in evolution. Using PCR and DNA sequencing, we determined the SRY gene sequences of nine OW monkeys (see fig. 1). The SRY sequences of six hominoids, one OW monkey, and one New World (NW) monkey were available in the GenBank at the time of this study. Thus, a total of 17 sequences are analyzed here (fig. 1). Because the HMG domain of SRY is conserved throughout mammalian evolution, we only analyze the Nand C-terminal regions, which have 120 codons after the indels are removed. We first computed the numbers of synonymous (dS) and nonsynonymous (dN) nucleotide substitutions between pairs of the six hominoid sequences, using the modified Nei-Gojobori method (Zhang, Rosenberg, and Nei 1998). We found that dN is greater than dS for 13 of the 15 pairwise comparisons (fig. 2), suggesting possible actions of positive selection. We then