How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals

Abstract

The duck-billed platypus is an extraordinary mammal. Its chromosome complement is no less extraordinary, for it includes a system in which ten sex chromosomes form an extensive meiotic chain in males. Such meiotic multiples are unprecedented in vertebrates but occur sporadically in plant and invertebrate species. In this paper, we review the evolution and formation of meiotic multiples in plants and invertebrates to try to gain insights into the origin of the platypus meiotic multiple. We describe the meiotic hurdles that translocated mammalian chromosomes face, which make longer chains disadvantageous in mammals, and we discuss how sex chromosomes and dosage compensation might have affected the evolution of sex-linked meiotic multiples. We conclude that the evolutionary conservation of the chain in monotremes, the structural properties of the translocated chromosomes and the highly accurate segregation at meiosis make the platypus system remarkably different from meiotic multiples in other species. We discuss alternative evolutionary models, which fall broadly into two categories: either the chain is the result of a sequence of translocation events from an ancestral pair of sex chromosomes (Model I) or the entire chain came into being at once by hybridization of two populations with different chromosomal rearrangements sharing monobrachial homology (Model II).

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

“…Other gene blocks on the platypus sex chromosomes have homology to other chicken chromosomes, consistent with the derivation of platypus chain by sequential translocations with autosomes 53. Sequence comparisons between X‐Y shared genes revealed that the large X 5 and tiny Y 5 that terminate the chain are the most diverged, and therefore the oldest members of the chain 54, suggesting that they represent the original mammalian sex chromosomes.…”

Evolution of Neo-Sex Chromosomes inSilene diclinis

“…Since F 1 females have 24 chromosomes, we find that the normal autosome is indeed inherited with the X chromosome and acts as a neo-X. Alternate segregation is seen in other species with multiple sex chromosomes that form a chain (Gruetzner et al 2006). For example, in the dioecious species in Rumex section Acetosa having two Y chromosomes and a single X these three chromosomes form a trivalent, Y1-X-Y2, and gametes containing either the X or Y1 and Y2.…”

“…In animals these configurations may include sex chromosomes, resulting in the formation of multiple X and Y chromosomes. For example, the monotreme platypus possesses five X and five Y chromosomes that form a chain of alternating X and Y chromosomes in male meiosis (Bick and Sharman 1975;Gruetzner et al 2006). Such chains are formed due to several interchromosomal translocation events, including sex chromosome-autosome translocations (Gruetzner et al 2006).…”

“…For example, the monotreme platypus possesses five X and five Y chromosomes that form a chain of alternating X and Y chromosomes in male meiosis (Bick and Sharman 1975;Gruetzner et al 2006). Such chains are formed due to several interchromosomal translocation events, including sex chromosome-autosome translocations (Gruetzner et al 2006). Since sex chromosomes are rare in plants, examples of plant sex-linked chromosome multiples have been reported on only a few occasions.…”

Intriguing evidence of translocations in Discus fish (Symphysodon, Cichlidae) and a report of the largest meiotic chromosomal chain observed in vertebrates

“…Meiotic multiples of more than four chromosomes are rare, and most of these cases are confined to plants and invertebrates, having never been described in fish (for review, see Grü tzner et al, 2006). Until this study, the biggest chromosomal chains detected in vertebrates were observed in platypus males (Ornithorhynchus anatinus) that have five X and five Y chromosomes.…”