The Chromosomal Basis of Sex-Differentiation in Marsupials

Abstract

Data on ten intersexual marsupials, eight of which were of known karyotype, are presented and reviewed. Three of the intersexes were known or suspected XO/XX or XO/XX/XXX, two were XXY, one was XXY/XY/XX and two were XY in sex chromosome constitution. In all three intersexes which had an XO cell line, but in which no Y chromosome was found in any cell, a small empty scrotum was found to one side of the midline or in the midline. Those which had a non-midline scrotum had mammary tissue on the opposite side and a partial or complete pouch. The intersex with the midline scrotum had no pouch or mammary glands. Unilateral or bilateral putative spermatic cords, not containing a ductus deferens, descended to the scrotum, but in all other respects the internal reproductive systems were like those of normal XX female marsupials. Intersexes with no Y chromosome were of female body size when adult. The XXY and XXY/XY/XX intersexes all had complete pouches and mammary glands and none had a scrotum. All had well developed male internal reproductive systems and undescended testis-like gonads, and were of intermediate body size. Both XY intersexes also had complete pouches and mammary glands, no scrotum, and male-type internal reproductive systems with undescended testes which were normal except for absence of post- primary spermatocyte stages of spermatogenesis. One XY intersex was fully adult and it did not differ from normal XY males of the same species in body measurements, body weight and secondary sex coloration. One of the intersexes of unknown karyotype, but of suspected XX chromosome constitution, was morphologically like the XO/XX/XXX mosaic with a centrally placed scrotum. The other, of suspected XY chromosome constitution, was essentially comparable to the XY intersexes. The data are interpreted, at the whole chromosome level, as follows. In the presence of a single active X chromosome scrotal and spermatic cord development were initiated, whereas they were inhibited in the presence of two X chromosomes. Complete scrotal development completely inhibited, and unilateral scrotal development partly inhibited, pouch and mammary gland development. The Y chromosome was responsible for primary gonadal sex and, apparently through production of MIS, eliminated the Miillerian (i.e. female) sex ducts. Development of a male type of reproductive system was dependent on presence of a Y chromosome and, apparently, androgen production from testes or testis-like gonads. At the gene level the data may be interpreted in terms of a hypothetical S or 'switch' locus, carried on the X chromosome, which induced scrotal development in single dose and a pouch and mammary glands in double dose. If this hypothesis is correct, it would explain the occurrence of incomplete X-chromosome inactivation in marsupials; complete X-inactivation is impossible in marsupials because it would leave each female with a scrotum, not a pouch.