In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes

Abstract

Two centuries after the duck-billed platypus was discovered, monotreme chromosome systems remain deeply puzzling. Karyotypes of males, or of both sexes, were claimed to contain several unpaired chromosomes (including the X chromosome) that form a multi-chromosomal chain at meiosis. Such meiotic chains exist in plants and insects but are rare in vertebrates. How the platypus chromosome system works to determine sex and produce balanced gametes has been controversial for decades. Here we demonstrate that platypus have five male-specific chromosomes (Y chromosomes) and five chromosomes present in one copy in males and two copies in females (X chromosomes). These ten chromosomes form a multivalent chain at male meiosis, adopting an alternating pattern to segregate into XXXXX-bearing and YYYYY-bearing sperm. Which, if any, of these sex chromosomes bears one or more sex-determining genes remains unknown. The largest X chromosome, with homology to the human X chromosome, lies at one end of the chain, and a chromosome with homology to the bird Z chromosome lies near the other end. This suggests an evolutionary link between mammal and bird sex chromosome systems, which were previously thought to have evolved independently.

Genome analysis of the platypus reveals unique signatures of evolution

“…Platypuses have multiple sex chromosomes with some homology to the bird Z chromosome 16 . Males have five X and five Y chromosomes, which form a chain at meiosis and segregate into 5X and 5Y sperm 17,18 . Sex determination and sex chromosome dosage compensation remain unclear.…”

The genetic contribution to sex determination and number of sex chromosomes vary among populations of common frogs (Rana temporaria)

“…Co-segregation of multiple sex chromosomes has notably been documented in some populations of Rana tagoi, where male heteromorphy for C-banding patterns suggests that both chromosome pairs 8 and 9 co-segregate as sex chromosomes (Ryuzaki et al, 1999). In some cases multiple translocations are involved, resulting in a multivalent chain of chromosomes during male meiosis (see, for example, Barlow and Wiens, 1976;Syren and Luykx, 1977;Grützner et al, 2004;Gazoni et al, 2012).…”

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

“…These form a chain at male meiosis which is held together by crossing over within nine pseudoautosomal regions. The five Xs segregate to one pole and the five Ys to the other 50.…”