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I
t has long been known that the Y chromosome is crucial for development of the male pheno-type in mammals. Intensive search for the testis-determining factor culminated in the early 1990s with the identification of the Y-linkedSry gene1, present on the Y chromosome of most mammalian species studied so far. Srytriggers a cascade of proteins involved in male development that are en-coded by autosomal, as well as X-and Y-linked, genes. However, the role of Sryas the key to sex differ-entiation does not extend outside mammals2. For instance, birds appear to have a different system for sex differentiation, although the knowledge of how this system operates is lagging far behind what we know about mammals. Importantly, avian sex chromo-somes show a reversed organ-ization compared with mammals, females being heterogametic ZW
and males homogametic ZZ. A long-standing issue in avian genetics has been whether the W chromosome is crucial for female development or whether it is the number of Z chromosomes that regulates male development3. The sex chromosome aneuploids (Box 1) required to answer this question have yet to be identified, but recent molecular analyses and gene mapping data have given the first hints
to the process of avian sex deter-mination. Moreover, these new data give insights into the evo-lution of heteromorphic sex chro-mosomes in general, and in birds in particular. Here, I will dis-cuss these recent achievements and make comparisons with mammals, birds’ closest relatives, for which detailed knowledge on sex differentiation processes is available.
The avian sex chromosomes
The Z and W chromosomes of birds share many features with mammalian X and Y chromo-somes, respectively. Both avian sex chromosomes are metacen-tric. They pair during meiosis and a synaptonemal complex (Box 1) is formed at the end of the short arms of the two chromosomes; therefore, a small pseudoautos-omal region (Box 1) exists. Typically, the Z chromosome is comparable in size with the fourth or the fifth chromosome pair, constituting some 7–10% of the total genome size4 (which in birds is only one-third of that in mammals). In most species, the W chromosome is considerably smaller and, without appropriate staining techniques, is some-times difficult to distinguish from the many microchromo-somes. In some species, from taxa as diverse as Piciformes,
Evolution of the avian sex chromosomes
and their role in sex determination
Hans Ellegren
Is it the female-specific W chromosome of birds that causes the avian embryo to develop
a female phenotype, analogous to the dominance mode of genic sex differentiation
seen in mammals? Or is it the number of Z chromosomes that triggers male development,
similar to the balance mode of differentiation seen in Drosophila and Caenorhabditis elegans? Although definite answers to these
questions cannot be given yet, some recent data have provided support for the latter hypothesis. Moreover, despite the potentially
common features of sex determination in mammals and birds, comparative mapping shows that the avian sex chromosomes have
a different autosomal origin than the mammalian X and Y chromosomes.
Hans Ellegren is at the Dept of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University,
Falconiformes and Gruiformes, enlarged sex chromosomes can be seen. In these cases, the Z chromosome is the largest in the karyotype, and the W chromosome is also unusually large. This suggests a coordinated mechanism for chromo-some expansion operating on the two sex chromochromo-somes. Another exception to the general pattern of avian sex chromo-some characteristics is found in ratites, where Z and W are similar in size (Box 2).
The W chromosome contains few genes. The staining technique C-banding indicates that W is rich in constitut-ive heterochromatin (Box 1), which is otherwise only found in high densities at the centromeres of microchromo-somes and at one of the ends of the Z chromosome, at least in chickens. The heterochromatic region of the W chromo-some consists mainly of late-replicating repetitive satellite DNA, which has been cloned and characterized in a few species5. Generally, one or a few repeat types prevail within each species and the repeats appear to be poorly conserved across species.
Avian sex determination: is it the Z or the W that matters?
It has been tempting to assign a similar dominance role for the avian W chromosome as found in the mammalian Y chromosome – that it is a chromosome unique to one sex, the presence of which triggers a sex differentiation process (to females in birds)6. This type of sex determin-ation traditionally has been demonstrated by studying sex chromosome aneuploids. Thus, in mammals, the fact that 2A:X0 individuals develop a female phenotype, but 2A:XXY individuals show male characteristics, illustrates that the presence of Y determines maleness, rather than the bal-ance between X chromosomes and autosomes determin-ing femaleness (the latter is the case in Drosophila and
C. elegans). However, in birds the corresponding aneu-ploids are extremely rare, if they exist at all. If a male pheno-type develops from 2A:ZZW birds or a female phenopheno-type from 2A:Z0 individuals, it would be the balance between the number of Z chromosomes relative to the number of autosomal complements that matters. But, if a female pheno-type develops from 2A:ZZW birds, it would be the mere presence of a dominant W chromosome that drives the ZW embryo towards female development.
Given that mass screenings for these aneuploids have been made without great success in poultry breeding, they might be lethal or at least severely deleterious. There is a sin-gle (and somewhat uncertain) report of a ZZW male chicken from 1954 (Refs 3,7), but nothing else. However, there is some circumstantial evidence supporting the Z-autosome balance view from gynandromorphic birds (which are lateral sex chimeras, where one side of the bird has a male pheno-type and the other a female phenopheno-type). In at least a few such cases, ZZ/Z0 constitutions have been identified, the male half of the bird being ZZ and the female half Z0 (Refs 3,8). Although this provides some information, firmly establishing the role of the avian sex chromosome in sex determination will require techniques other than aneuploids.
Clues from comparative mapping
Comparative mapping reveals the chromosomal location of orthologous DNA fragments, commonly genes, in differ-ent taxa. This approach is one of the most important in genome projects, allowing map information to be trans-ferred from map-rich species (typically human or mice) to map-poor species (less well characterized genomes). For instance, once a trait locus has been mapped by linkage analysis to a particular chromosomal region, candidate
genes (Box 1) can be searched for within the corresponding region in a species with more extensive map information. Comparative mapping can also be of great importance for addressing the evolution of chromosomes, genomes or, as in this case, patterns of sex determination.
First, we can ask whether avian and mammalian sex chromosomes share a common ancestry. If they evolved from the same pair of autosomes in an ancestral verte-brate, this would be suggestive of the two taxa sharing mol-ecular or chromosomal principles for sex determination. One suitable way to address this is to find out whether genes on the avian Z chromosome are similarly sex-linked in mammals (or vice versa) – comparative mapping shows that they are not (Fig. 1). Genetic, as well as physical, map-ping places genes from the chicken Z chromosome on sev-eral different human autosomes9. So far, only one Z-linked gene (OTC) has been found on the human X chromosome,
Box 1. Glossary
Aneuploidy: an abnormal chromosomal condition where one or more chromosome from a haploid set is either absent or present more than once.
Candidate gene:a gene that potentially could be responsible for a particular trait, but where functional or mutant studies have not yet provided a causal relationship. Often, researchers search for candidate genes among those known to reside within a chromosomal region to which a trait locus has been mapped by linkage analysis or association studies.
Dosage compensation:many organisms with heteromorphic sex somes try to balance the expression of genes on one of the sex chromo-somes so that the expression does not differ between sexes. In organisms with XY/XX sex chromosomes, this can take place by more or less completely inactivating gene expression on one of a female’s two X chromosomes (as in mammals) or by upregulating gene expression on a male’s single X chromosome (as in Drosophila).
Haploinsufficiency: the loss of function when a protein is expressed from only one copy of the gene. Haploinsufficiency can arise from a deletion of one of the two gene copies.
Heterochromatin:chromosomal region with a compact structure (heavily folded) during most parts of the cell cycle. Generally, heterochromatic regions contain few genes (which require less compact structures for their regulation and expression).
Pseudoautosomal region: the part of the sex chromosomes that recom-bine. A marker from the pseudoautosomal region will show no sex linkage.
Retroposition:a mobile genetic element that results in a copy of a certain RNA sequence being inserted elsewhere in the genome. The inserted sequence might differ from the original DNA sequence because the mobile element is an RNA molecule, which generally lacks introns and contains post-transcriptional modifications (e.g. polyadenylation).
Synaptonemal complex: the structure of proteins joining homologous chromosomal regions at meiosis before recombination.
Transposition:a mobile genetic element that results in a copy of a certain DNA sequence being inserted elsewhere in the genome. The mobile element is in the form of DNA.
Box 2. The undifferentiated sex chromosomes of ratites
1 9 0 TREE vol. 15, no. 5 May 2000 but given the size of X this could be expected by chance.
The few genes mapped to the chicken W chromosome are not sex-linked in mammals either9. Thus, in spite of the sex chromosomes being a common means for sex determin-ation among vertebrates, it appears that sex chromosomes have evolved independently in different lineages.
The absence of significant homologies between Z/W and X/Y might suggest that there are no links between sex determination in birds and mammals. However, this
conclusion is probably premature. Notably, through com-parative mapping, the chicken Z chromosome has recently been found to be homologous to a large part of human chromosome 9, including 9p (Refs 9,10). At first glance, the significance of this observation is obscure, but it becomes clearer when it is noted that 9p is one of the chromosomal regions implicated in female sex reversal and gonadal dys-genesis among XY humans11. Specifically, a small region at 9p24.3 (close to the telomere) has been found to be deleted in XY sex reversals, suggesting that one or several genes present within this region are required in two copies for normal male development in XY individuals [otherwise haploinsufficiency (Box 1) is caused]. If such a gene is located on the Z chromosome of birds and has similar functions as those in mammals, one could speculate that it might play a key role in avian sex determination.
What is the role of DMRT1?
Most genes involved in vertebrate sex determination seem not to be conserved across taxa. For instance, the genes involved in sex differentiation processes in Drosophilaand
C. elegansare essentially specific to the respective organ-ism2. Recently, however, evidence for evolutionary con-servation of a sex-determining gene has been found. The
mab-3male sexual regulatory gene of C. elegans contains a DNA-binding domain (DM-domain) with significant amino acid homology to the Drosophilasexual regulatory gene
doublesex(dsx)12. A common feature of the two proteins is that they control sex-specific neuroblast differentiation and regulate transcription of yolk proteins. Transgenic studies reveal that the DSX protein can restore male differ-entiation in mab-3 C. elegansmutants12; thus, mab-3 and dsx are functionally interchangeable.
A gene with a DM-domain similar to mab-3and dsxhas also been identified in humans, and has been designated
DMRT1(originally DMT1)12. Interestingly, DMRT1maps to the small region on 9p24.3 implicated in sex reversal and is a strong candidate gene for this trait13. DMRT1is expressed exclusively in the genetical ridge before sex differentiation (the only other gene which shows this pattern is Sry) and soon after is expressed only in the testes14; thus, DMRT1 seems to be involved in mammalian sexual development. Moreover, the conserved function of DMRT1-related pro-teins in downstream sexual development in divergent phyla, the probable requirement of two expressed copies of DMRT1 for an XY human to develop male phenotype, and the recent mapping of chicken DMRT1to the Z chro-mosome10, suggest that DMRT1might also be involved in regulating sexual differentiation in birds, through Z chro-mosome dosage. Recently, support for this has been obtained through whole-mount in situhybridization and reverse transcriptase PCR (RT-PCR) studies of chicken embryos14. DMRT1is expressed in the genetical ridge from the time it starts to form, as well as in the Wolffian ducts, which become the male-specific internal reproductive structures. Moreover, DMRT1expression is higher in male embryos than in female embryos. The expression of
DMRT1 might occur before the expression of the anti-Müllerian hormone (AMH), which is an early marker of testis differentiation3,15,16, thus inhibiting the development of female reproductive structures.
Although Sryis not conserved between mammals and birds, another testis promoter is. In mammals, the gene product of Sox9acts downstream of Sry, probably by defin-ing and maintaindefin-ing Sertoli cell identity in males17. Appar-ently triggered by a different mechanism, Sox9 also is involved in regulating gonadal development in birds. At
Fig. 1. Genes mapped to the chicken Z chromosome (GGAZ) and their chromosomal location in humans (HSA1chromosome number). Vertical bars depict physical assignments to GGAZ. Genes not associated with a horizontal bar have been mapped only by linkage analysis to GGAZ. Note that the order of genes along GGAZ might, in some cases, not be precisely as indicated in the figure. Locus designations are as follows: ATP5A1Z, ATP synthase a-subunit; IFNA1/IFNB1, interferon a1/b1; DMRT1, doublesex and mab-3 related in testis 1; GHR, growth hormone receptor; VLDLR, very low density lipoprotein receptor; BRM, SWI/SNF-related, matrix associ-ated, actin-dependent regulator of chromatin, subfamily A, member 2; NTRK2, neurotrophic tyrosine kinase receptor 2; OTC, ornithine transcar-bamylase; CHD1Z, chromodomain helicase DNA binding protein 1; CHRNB3, cholinergic receptor, neuronal nicotinic, bpolypeptide 3; ACO1, aconitase 1; ALDOB, aldolase B; GGTB2, b-1,4-galactosyltransferase, polypeptide 1; IREB1, iron-responsive element-binding protein 1; TMOD, tropomodulin; PTCH, homologue of Drosophila patched.
HSA18
HSA9
HSAX
HSA5
HSA8
HSA9
GGAZ Human chromosomes IFNA1, IFNB1
DMRT1
VLDLR
BRM
NTRK2
GGTB2 ACO1
TMOD ALDOB
PTCH ATP5A1Z
GHR
OTC
CHD1Z
CHRNB3
IREB1
the time when the gonads start to differ-entiate in the avian embryo, Sox9is ex-pressed exclusively in the testes18. This indicates further that birds and mammals might share molecular and physiological mechanisms for sex determination.
Evolution of the avian sex chromosomes from an ancestral pair of autosomes
So far, only a few genes (or potential cod-ing sequences) have been assigned to the avian W chromosome (Table 1). Interest-ingly, these genes are present as one copy on W and one copy on Z, although they are not pseudoautosomal – they are pres-ent on the nonrecombining parts of the two types of sex chromosomes. The best characterized pair are the CHD1Z-CHD1W
genes19,20. They are Z- and W-linked, respectively, in all nonratite (Neognate) birds studied and sequence data sug-gest that the two genes are evolving independently21. The
CHD1Z-CHD1Wsystem offers a universal means for molecu-lar sexing of nonratite birds, using straightforward PCR analysis22. Because some introns differ in size between
CHD1Zand CHD1W, conserved primer pairs that amplify both copies will reveal one PCR fragment in males (CHD1Z) and two fragments in females (CHD1Z and CHD1W)23,24. In addition to their use in molecular sexing, the CHD1Z
and CHD1W genes have allowed investigation of sex-specific mutation rates in birds, thus providing evidence for a male-biased mutation rate (Box 3).
An intriguing issue in the evolution of the avian sex chromosomes is what types of genes have remained on the W chromosome. In mammals, we know that many genes present on the Y chromosome have male-specific func-tions, so obviously there has been selection for their re-tention. Moreover, male-specific genes also have been acquired by Y through transposition25and even retropos-ition26(Box 1) from autosomal origins. If sex determination in birds is principally a matter of the number of Z chromo-somes, it becomes less straightforward to invoke sex-spe-cific roles for genes retained on W. Perhaps the answer relates to the fact that dosage compensation (Box 1) of Z-linked genes has not yet been found in birds27. If correct, in cases where the lower amount of gene product produced by females would have an impact on fitness, there should be selection for retaining a functional homologue on the W chromosome. This hypothesis is supported by the fact that the few pairs of genes shared between Z and W, which have been characterized to date, show a high degree of sequence similarity12,21,28. However, overall little is known about how birds deal with the expression of Z-linked genes in males and females, respectively.
Prospects
Sexual reproduction is one of the most widespread features of life, yet an increasing body of evidence points to independent solutions to the physiology, genetics and molecular mechanisms of sexual development in different lineages. In fact, genes involved in sexual development seem to be among the most quickly evolving. However, in spite of these general differences, parts of the enzymatic cascades underlying sexual development can be con-served, as described above for DMRT1. Such common means will be important for dissecting the molecular basis of sexual development organisms that have not been well
characterized. This, together with increased efforts to map genes onto the sex chromosomes and the use of transgenic techniques to study functional properties of candidate genes, is likely to provide a detailed picture of avian sex deter-mination in the near future. In particular, the construction of a ZW bird transgenic for an additional copy of DMRT1would provide interesting information on Z-chromosome dosage and sex differentiation.
Recent observations on the evolution of the avian sex chromosomes have provided answers but also new ques-tions. Future research should focus on the molecular evo-lution of genes on the avian sex chromosomes to reveal what are the functional constraints associated with such genes. For instance, are nonsynonymous substitution rates equal in Z- and W-linked homologues of genes shared between the nonrecombining parts of the Z and W sex chromosomes? In the wider perspective, one of the most important questions is why some organisms have evolved male heterogamety, while in others females have become the heterogametic sex? In order to solve this, comparative approaches addressing how sex chromosomes have evolved
Box 3. Male-biased avian mutation rate
Because the two types of sex chromosomes spend different times in the sexes, any difference in the sex-specific mutation rates should be mani-fested by differing rates of sequence evolution on the two sex chromo-somes (given no selection)45. Specifically, in birds, the rate of neutral sequence evolution on the W chromosome unique to females should directly reflect the female mutation rate. The rate of evolution of neutral sequences on Z should be governed by a combination of the mutation rate in males and females; from this, the male mutation rate can be inferred indir-ectly given that a Z chromosome spends exactly two-thirds of its time in the male germline. Because the mutation rate might differ between genes, the best approach for analysing sex-specific mutation rates, in the absence of sequence data from a large number of genes, is to study genes shared between the sex chromosomes (yet independently evolving). Comparing the sequences of different bird species, introns, as well as silent sites of CHD1Z, are found to evolve faster than paralogous sequences of CHD1W (Ref. 21). From this, a male-to-female mutation rate ratio (a) of between three and six has been estimated. An excess of male mutations also has been revealed from studies of the ATP5A1Z/ATP5A1W gene pair28.
The avian sex chromosome system offers an advantage over the mam-malian X and Y chromosomes for addressing sex-specific mutation rates. It has been suggested that the mutation rate of the X chromosome might be reduced specifically, owing to the avoidance of exposure of recessive del-eterious mutations in hemizygote males46. If so, observations of a faster rate of neutral evolution on Y than on X might not necessarily be a result of vary-ing sex-specific rates. However, in birds, estimates of aare conservative because the effect of a potential reduction in the Z-chromosome mutation rate would be the opposite of that given by higher male mutation rates.
Table 1. Known DNA sequences of avian W chromosomes
Type of DNA Locus Homologue on Z Species Refs sequence chromosome
Genes CHD1W CHD1Z Conserved 19,20 ATP5A1W ATP5A1Z Conserved 9,28,32 Anonymous unique EE0.6 Yes Conserved 33,34
DNAs DQSG10 Yes Goose 35 RAPD-derived Anonymous No Available in many species, 36–38
fragments but always species-specific
Minisatellite Anonymous No Kite, wren, parrots and 39–42 fragments skua
Repetitive DNAs Satellite No Several species, but 5,43,44 repeats always species- or
1 9 2 TREE vol. 15, no. 5 May 2000 in a variety of lineages are needed, along with knowledge
of the mechanisms of sex determination in these lineages. Evolutionary biologists, geneticists and developmental biologists should join forces to accomplish this task.
Acknowledgements
I thank Ben Sheldon for comments on this article and members of my group for discussions. Financial support has been obtained from the Swedish Natural Sciences Research Council.
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