Resolution and evolution of the duck-billed platypus karyotype with an X ₁ Y ₁ X ₂ Y ₂ X ₃ Y ₃ X ₄ Y ₄ X ₅ Y ₅ male sex chromosome constitution

Abstract

The platypus (2n ‫؍‬ 52) has a complex karyotype that has been controversial over the last three decades. The presence of unpaired chromosomes and an unknown sex-determining system especially has defied attempts at conventional analysis. This article reports on the preparation of chromosome-specific probes from flow-sorted chromosomes and their application in the identification and classification of all platypus chromosomes. This work reveals that the male karyotype has 21 pairs of chromosomes and 10 unpaired chromosomes (E1-E10), which are linked by short regions of homology to form a multivalent chain in meiosis. The female karyotype differs in that five of these unpaired elements (E1, E3, E5, E7, and E9) are each present in duplicate, whereas the remaining five unpaired elements (E2, E4, E6, E8, and E10) are absent. This finding indicates that sex is determined by the alternate segregation of the chain of 10 during spermatogenesis so that equal numbers of sperm bear either one of the two groups of five elements, i.e., five X and five Y chromosomes. Chromosome painting reveals that these X and Y chromosomes contain pairing (XY shared) and differential (X-or Y-specific) segments. Y differential regions must contain male-determining genes, and X differential regions should be dosage-compensated in the female. Two models for the evolution of the sex-determining system are presented. The resolution of the longstanding debate over the platypus karyotype is an important step toward the understanding of mechanisms of sex determination, dosage compensation, and karyotype evolution.monotremes ͉ multivalent chain ͉ X-inactivation ͉ sex determination

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.…”

Steps in the evolution of heteromorphic sex chromosomes

“…Neo-sex chromosome systems are known in many plants and animals, including XY 1 Y 2 in the plant Rumex acetosa (Rejó n et al, 1994), and multiple sex chromosomes due to translocations in African misteltoes (Barlow and Wiens, 1976), termites (Syren and Luykx, 1977), African pygmy mice (Veyrunes et al, 2004) and monotremes (Rens et al, 2004). As we shall describe below, the sex chromosomes of eutherian mammals represent an ancient case of neo-sex chromosomes, established after the divergence of eutherians and marsupials (Waters et al, 2001).…”

The origin and evolution of vertebrate sex chromosomes and dosage compensation

“…In females, five of these chromosomes are absent and the remaining five are present in duplicate. Thus, the sex chromosomes of males were described as X 1 Y 1 X 2 Y 2 X 3 Y 3 X 4 Y 4 X 5 Y 5 , and in females as X 1 X 1 X 2 X 2 X 3 X 3 X 4 X 4 X 5 X 5 (Grützner et al, 2004;Rens et al, 2004). The echidna has an equally complex sex chromosome system, and it was shown that the sex chromosomes of the platypus and echidna share homology but are not identical; the echidna has five X and four Y chromosomes, sharing seven with the platypus.…”