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Sex Chromosomes: Evolution of Beneficial to Males but Harmful to Females, and the Other Has the the Weird and Wonderful Opposite Effect

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Sex Chromosomes: Evolution of Beneficial to Males but Harmful to Females, and the Other Has the the Weird and Wonderful Opposite Effect Dispatch R129 microtubule plus ends is coupled to of kinesin-mediated transport of Bik1 1The Scripps Research Institute, microtubule assembly. J. Cell Biol. 144, (CLIP-170) regulates microtubule Department of Cell Biology, 10550 99–112. stability and dynein activation. Dev. Cell 11. Arnal, I., Karsenti, E., and Hyman, A.A. 6, 815–829. North Torrey Pines Road, La Jolla, (2000). Structural transitions at 14. Andersen, S.S., and Karsenti, E. (1997). California 92037, USA. microtubule ends correlate with their XMAP310: a Xenopus rescue-promoting E-mail: [email protected] dynamic properties in Xenopus egg factor localized to the mitotic spindle. J. 2Ludwig Institute for Cancer Research, extracts. J. Cell Biol. 149, 767–774. Cell Biol. 139, 975–983. Department of Cellular and Molecular 12. Busch, K.E., Hayles, J., Nurse, P., and 15. Schroer, T.A. (2004). Dynactin. Annu. Brunner, D. (2004). Tea2p kinesin is Rev. Cell Dev. Biol. 20, 759–779. Medicine, CMM-E Rm 3052, 9500 involved in spatial microtubule 16. Vaughan, P.S., Miura, P., Henderson, M., Gilman Drive, La Jolla, California 92037, organization by transporting tip1p on Byrne, B., and Vaughan, K.T. (2002). A USA. E-mail: [email protected] microtubules. Dev. Cell 6, 831–843. role for regulated binding of p150(Glued) 13. Carvalho, P., Gupta, M.L., Jr., Hoyt, M.A., to microtubule plus ends in organelle and Pellman, D. (2004). Cell cycle control transport. J. Cell Biol. 158, 305–319. DOI: 10.1016/j.cub.2005.02.010 Sex Chromosomes: Evolution of beneficial to males but harmful to females, and the other has the the Weird and Wonderful opposite effect. There is an obvious selective advantage to ensuring that such loci are closely New findings in the platypus and Drosophila pseudoobscura illustrate, linked to the sex-determining yet again, that the sex chromosomes seem never to stop evolving. region [1,6,7]. Degeneration processes lead to a continual loss of genes and gene These ideas apply to genes activity on the Y chromosome, and complete loss of Y-linked genes is that are already on the sex- possible if autosomal genes take over control of male fertility — determining chromosome; though addition of new material to the sex chromosomes may start the linkage between sexually process anew. antagonistic loci on an autosome and the sex-determining region Deborah Charlesworth and non-recombining region of the requires translocations bringing Brian Charlesworth chromosome pair that carries the material from one chromosome sex determining genes forms only onto another [8]. Translocations part of the chromosome, as in between the sex chromosomes I like the duck-billed platypus papaya [4] and the three-spined and autosomes, creating ‘neo- Because it is anomalous. stickleback [5]. sex’ chromosomes, have indeed I like the way it raises its family The initial reason for evolving become established in a variety Partly birdly, partly mammaly. lack of recombination between Y of taxa, most often involving I like its independent attitude. and X (or Z and W) chromosomes Robertsonian fusions between Let no one call it a duck-billed is probably because they sex chromosomes and an platitude. originally carried sex-determining autosome. For example, the Ogden Nash genes, and recombination Drosophila pseudoobscura X is between these genes would have made up of two arms, one produced disadvantageous homologous with the D. Advanced sex chromosomes — sexual phenotypes [2]. It is thus melanogaster 3L chromosome XX/XY with male heterogamety, not surprising that small non- arm and one with its X (Figure 1). ZZ/ZW with female heterogamety recombining regions exist: these The eutherian mammalian Y is — have evolved independently in are presumably the regions also a composite, made up of a many different lineages, and show where the sex-determining genes part that was already X-linked in several striking common features, are located. But why do many marsupials, and a part that including lack of recombination in sex chromosome systems have became X-linked more recently, the heterogametic sex, and much larger non-recombining and which is still autosomal in genetic degeneration of the Y or regions? marsupials [9]. An X-autosome W chromosome [1,2]. Such systems might have been fusion followed by a Y-autosome Degeneration involves the loss or created by chromosome fusion (or vice versa) must have inactivation of most Y- or W- inversions, which when been involved in this case, as linked genes, and this is often heterozygous suppress crossing some genes in both parts are compensated for by sex over across large regions, now present on the X as well as differences in the expression of X potentially including many genes the Y. The DNA sequences of or Z-linked genes [3]. The sex other than those involved in sex those still present in the added chromosomes are frequently determination, and contributing to part have much lower X–Y heteromorphic, with the Y (W) the evolution of chromosome divergence than the others, often smaller than the X (Z), and heteromorphism. The evolutionary consistent with their alleles largely made up of pressure for this wider reduction having stopped recombining heterochromatin. Partially evolved of recombination is thought to more recently. sex chromosomes with only some come from the existence of loci It now appears that the duck- of these features are also known with alleles that are sexually billed platypus, a monotreme, is [1]: in these cases, the antagonistic — one allele is an extreme example of multiple Current Biology Vol 15 No 4 R130 D. subobscura the platypus), out of a D. guanche (obscura subgroup) chromosome complement of 12 pairs plus one unpaired D. affinis chromosome [15]. (affinis subgroup) When another chromosome D. pseudoobscura attaches to the sex chromosome, the resultant neo-Y may start (pseudoobscura subgroup) degenerating, like other Y chromosomes, unless it continues X 1 Y X Y to recombine with its homologue D. miranda X2 X Y [1,2]. In the platypus, the neo-Ys D. melanogaster 3 could presumably recombine over (melanogaster subgroup) 2 part of their length, at least D. hydei initially, so they might not X Y degenerate completely. As with other examples of neo-sex Evolutionary 10 MYA 6 MYA~ 1 MYA~ chromosomes, it is not known divergence times Current Biology what drove the successive exchanges of chromosome arms, Figure 1. Chromosome arrangements in several Drosophila species, showing the but it seems unlikely that such fusions mentioned in the text and rough estimates of the times when they happened. similar events would have The male karyotypes are shown by the branches of the tree, and changed states are repeatedly happened so many shown by the species in which they are found. The time estimates are based on syn- times unless some advantage, onymous site divergence values (Ks) for multiple genes between pairs of species, and such as sexual antagonism, are rough because there is no reliable molecular clock for Drosophila species. The was involved. approximate divergence values from D. pseudoobscura are: D. miranda 3.2%, D. affinis 23%, D. melanogaster 30% [20]. The divergence from either D. melanogaster or The neo-sex chromosomes of D hydei is so large that accurate dating is not possible (the dashed line indicates a long D. pseudoobscura and its time). The D. miranda neo-Y is shown as a broken line to indicate that it is partially relatives have also undergone degenerate. further evolution, but differently from the platypus. At least two reciprocal translocations the ‘X’ chromosome — carries the more transmutations have involving sex chromosomes and DMRT1 gene, located on occurred. In its close relative D. autosomes, with permanent chromosome 9 in humans; miranda, a new translocation has translocation heterozygosity in DMRT1 mutations cause sex joined the autosome homologous males (which had previously been reversal of males. DMRT1 is with the D. melanogaster 2R to known to carry five carried on the Z chromosome of the Y (Figure 1). The new arm is chromosomes absent from birds, and has been proposed as now partially degenerate, after females, out of a chromosome the bird female determining only about one million years in a complement of 52 pairs). To sort factor. Grützner et al. [11] suggest non-recombining state [16,17]. It out their homologies, that the original platypus sex now also seems that the chromosomes from a male were chromosome pair involved the ancestral Y may have separated according to their one carrying DMRT1, not the degenerated completely in an sizes, and DNA fractions homologue of the mammalian sex ancestor of D. pseudoobscura enriched for each particular chromosomes. But the evidence and its relatives as distant as D. chromosome were labelled to for a role of DMRT1 as primary affinis, and that these species’ make ‘chromosome paints’ which sex determiner in birds is weak existing Y may be a remnant of can be used to identify the [12], so this finding could simply the Y2 created by the earlier different chromosomes [10]. Five be coincidental, rather than fusion, rather than the original Y chromosome pairs form a chain implying a ‘partly birdly, partly chromosome as was formerly in meiosis, and the paints mammaly’ sex-determination assumed [18]. establish that they share system for the platypus. The recent availability of homologous arms, indicating that Although these findings seem sequences covering most of the they were formed by reciprocal odd, the platypus is far from D. pseudoobscura genome translocations between different uniquely anomalous [13], and allowed searches for known D. chromosomes (Figure 2). even more extreme examples melanogaster Y-linked genes; One member of the chain is exist. Other well-studied cases these are, as expected, present homologous to the ancestral X of are a termite species with a set of in D.
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