Sex determination in platypus and echidna: autosomal location of SOX3 confirms the absence of SRY from monotremes

Abstract

In eutherian ('placental') mammals, sex is determined by the presence or absence of the Y chromosome-borne gene SRY, which triggers testis determination. Marsupials also have a Y-borne SRY gene, implying that this mechanism is ancestral to therians, the SRY gene having diverged from its X-borne homologue SOX3 at least 180 million years ago. The rare exceptions have clearly lost and replaced the SRY mechanism recently. Other vertebrate classes have a variety of sex-determining mechanisms, but none shares the therian SRY-driven XX female:XY male system. In monotreme mammals (platypus and echidna), which branched from the therian lineage 210 million years ago, no orthologue of SRY has been found. In this study we show that its partner SOX3 is autosomal in platypus and echidna, mapping among human X chromosome orthologues to platypus chromosome 6, and to the homologous chromosome 16 in echidna. The autosomal localization of SOX3 in monotreme mammals, as well as non-mammal vertebrates, implies that SRY is absent in Prototheria and evolved later in the therian lineage 210-180 million years ago. Sex determination in platypus and echidna must therefore depend on another male-determining gene(s) on the Y chromosomes, or on the different dosage of a gene(s) on the X chromosomes.

Did sex chromosome turnover promote divergence of the major mammal groups?

“…Not surprisingly, monotremes lack SRY , and SOX3 is autosomal 58, 59, lying with orthologues of other human X genes on chromosome 6. The bird sex determining gene DMRT1 lies on an X chromosome in monotremes, so is unlikely to promote dosage‐dependent determination in which two copies promote male development.…”

No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution

“…Such appears to be the case in therian mammals where the dominant Y-linked sex-determination gene Sry operates by regulating expression of the autosomal gene Sox 9 [94] and hence controls the entire sex-determination cascade. The absence of Sry from non-mammalian vertebrates and from egg-laying mammals [95] indicates that this mechanism of sex determination, and hence the therian Y chromosome, was acquired relatively recently. A single, Y-linked dominant gene DMY also determines sex in the medaka fish Oryzias latipes [96] but is absent from closely related species [97], indicating recent acquisition of a novel sex-determination system.…”

Identification of mediator complex 26 (Crsp7) gametologs on platypus X1 and Y5 sex chromosomes: a candidate testis-determining gene in monotremes?

“…Monotremes have no Sry gene, but the therian gametolog Sox3 is present on chromosome 6 (Wallis et al 2007). Recently, the crucial step of Sry action has been discovered, where Sry together with Sf-1 binds to a testis-specific enhancer element (TESCO).…”