Are homologies in vertebrate sex determination due to shared ancestry or to limited options?

Abstract

The same candidate genes and the same autosomes are repeatedly used as sex chromosomes in vertebrates. Are these systems identical by descent, or are some genes or chromosomes intrinsically better at triggering the first steps of sex determination?

Figure 1

Phylogeny and sex-determination systems in vertebrates. (a) Tetrapods; (b) teleost fishes. The different sex-determination systems found in the different lineages are indicated on the right of the figure. For the fish lineages (b), homologies of identified sex chromosomes to the ancestral teleost karyotype (TEL) are shown [67]. See Table 2 for details.

Figure 2

The antagonistic relationship between the pathways determining testis or ovary development in mammals. The male-determining pathway is shown on the left and the female pathway on the right. In males, SRY on the Y chromosome is activated by various upstream factors (small green arrows), including SF1, and upregulates the autosomal gene SOX9, which then maintains its own activity with the help of several other factors (small green arrows), including FGF9, whose expression is in turn upregulated by SOX9. FGF9 induces a cascade of downstream steps that is controlled by several genes, including DMRT1. These steps culminate in the differentiation of Sertoli cells, which are crucial to the development of the gonad as a testis. SOX9 and FGF9 repress RSPO1 and WNT4, which promote the development of the gonad as an ovary. In females, RSPO1 upregulates WNT4, which is accompanied by the stabilization of β-catenin, which is probably the mediator by which RSPO1 and WNT4 repress SOX9 and FGF9. Activation steps are represented by green arrows and inhibition by red bars.

Figure 3

Orthology of sex chromosomes and autosomes in amniotes. Four conserved regions, containing orthologous genes, are represented as green, dark blue, red and yellow regions in a variety of amniotes, lying on sex chromosomes (background shaded in yellow, pink or blue) or autosomes (numbered where known). The human (eutherian) XY pair consists of the blue and green ancestral regions that are separate in reptiles and birds and in monotremes and marsupials; the blue represents the ancestral therian XY (XCR) and the green blocks an addition in eutherians (XAR or YAR). SOX3 in the dark-blue block evolved into the mammalian sex-determining gene SRY. The dark-blue and the green blocks are autosomal in birds, reptiles and monotreme mammals. In birds, a different ancestral block (red), containing the sex-determining gene DMRT1, forms the ZW sex-chromosome pair; this gene block is also present in the ZW sex-chromosome pair in a gekko lizard (not shown), and on the sex-chromosome complex of platypus. In eutherians and marsupials, this block is autosomal. The red block is also autosomal in snakes, in which a different chromosome (yellow) has taken on a sex-determining role; the snake ZW is autosomal in all other lineages. All these genome regions are autosomal in a turtle that has temperature sex determination (TSD).