REVIEWS

31 Yamamoto, S. (1996) Gap regeneration of major tree species in 41 Busing, R.T. and White, P.S. (1997) Species diversity and small-scale
different forest types of Japan. Vegetatio 127, 203–213
32 Runkle, J.R. (1998) Changes in southern Appalachian canopy tree gaps
sampled thrice. Ecology 79, 1768–1780
33 van der Meer, P.J. et al. (1998) Tree seedling performance in canopy
gaps in a tropical rain forest at Nouragues, French Guiana.
J. Trop. Ecol. 14, 119–137
34 Brokaw, N.V.L. and Scheiner, S.M. (1989) Species composition in gaps
and structure of a tropical forest. Ecology 70, 538–541
35 Zagt, R.J. and Werger, M.J.A. (1998) Community structure and the
demography of primary species in tropical rain forest. In Dynamics
of Tropical Communities (Newbery, D.M. et al., eds), pp. 193–219,
Blackwell Science
36 Lieberman, M. et al. (1995) Canopy closure and the distribution of tropical
forest tree species at La Selva, Costa Rica. J. Trop. Ecol. 11, 161–178
37 Welden, C.W. et al. (1991) Sapling survival, growth, and recruitment:
relationship to canopy height in a neotropical forest. Ecology 72, 35–50
38 Dalling, J.W. et al. (1998) Seed dispersal, seedling establishment and
gap partitioning among tropical pioneer trees. J. Ecol. 86, 674–689
39 Hubbell, S.P. et al. (1999) Light-gap disturbances, recruitment limitation,
and tree diversity in a neotropical forest. Science 283, 554–557
40 Denslow, J.S. (1995) Disturbance and diversity in tropical rain forests:
the density effect. Ecol. Appl. 5, 962–968
disturbance in an old-growth temperate forest: a consideration of gap
partitioning concepts. Oikos 78, 562–568
42 Reader, R.J. et al. (1995) Interspecific variation in tree seedling establish-
ment in canopy gaps in relation to tree density. J. Veg. Sci. 6, 609–614
43 Wright, E.F. et al. (1998) Regeneration from seed of six tree species in
the interior cedar-hemlock forests of British Columbia as affected by
substrate and canopy gap position. Can. J. For. Res. 28, 1352–1364
44 Ribbens, E. et al. (1994) Seedling recruitment in forests: calibrating models
to predict patterns of tree seedling dispersion. Ecology 75, 1794–1806
45 Hurtt, G.C. and Pacala, S.W. (1995) The consequences of recruitment
limitation: reconciling chance, history, and competitive differences
among plants. J. Theor. Biol. 176, 1–12
46 Duncan, R.P. et al. (1998) Small-scale species richness in forest canopy
gaps: the role of niche limitation versus the size of the species pool.
J. Veg. Sci. 9, 455–460
47 Terborgh, J. et al. (1996) Tropical tree communities: a test of the
nonequilibrium hypothesis. Ecology 77, 561–567
48 Yu, D.W. et al. (1998) Can high tree species richness be explained by
Hubbell’s null model? Ecol. Lett. 1, 193–199
49 Grubb, P.J. (1977) The maintenance of species-richness in plant
communities: the importance of the regeneration niche. Biol. Rev.
52, 107–145

Evolution of the avian sex chromosomes

and their role in sex determination
Hans Ellegren

I
t has long been known that the Is it the female-specific W chromosome of to the process of avian sex deter-
Y chromosome is crucial for birds that causes the avian embryo to develop mination. Moreover, these new
development of the male pheno- a female phenotype, analogous to the data give insights into the evo-
type in mammals. Intensive search dominance mode of genic sex differentiation lution of heteromorphic sex chro-
for the testis-determining factor seen in mammals? Or is it the number of Z mosomes in general, and in
culminated in the early 1990s with chromosomes that triggers male development, birds in particular. Here, I will dis-
the identification of the Y-linked similar to the balance mode of differentiation cuss these recent achievements
Sry gene1, present on the Y seen in Drosophila and Caenorhabditis and make comparisons with
chromosome of most mammalian elegans? Although definite answers to these mammals, birds’ closest relatives,
species studied so far. Sry triggers questions cannot be given yet, some recent for which detailed knowledge on
a cascade of proteins involved in data have provided support for the latter sex differentiation processes is
male development that are en- hypothesis. Moreover, despite the potentially available.
coded by autosomal, as well as X- common features of sex determination in
and Y-linked, genes. However, the mammals and birds, comparative mapping The avian sex chromosomes
role of Sry as the key to sex differ- shows that the avian sex chromosomes have The Z and W chromosomes of
entiation does not extend outside a different autosomal origin than the birds share many features with
mammals2. For instance, birds mammalian X and Y chromosomes. mammalian X and Y chromo-
appear to have a different system somes, respectively. Both avian
for sex differentiation, although sex chromosomes are metacen-
the knowledge of how this system Hans Ellegren is at the Dept of Evolutionary Biology, tric. They pair during meiosis and
operates is lagging far behind Evolutionary Biology Centre, Uppsala University, a synaptonemal complex (Box 1)
Norbyvägen 18D, SE-752 36 Uppsala, Sweden
what we know about mammals. (hans.ellegren@evolution.uu.se).
is formed at the end of the short
Importantly, avian sex chromo- arms of the two chromosomes;
somes show a reversed organ- therefore, a small pseudoautos-
ization compared with mammals, omal region (Box 1) exists.
females being heterogametic ZW Typically, the Z chromosome is
and males homogametic ZZ. A long-standing issue in avian comparable in size with the fourth or the fifth chromosome
genetics has been whether the W chromosome is crucial pair, constituting some 7–10% of the total genome size4
for female development or whether it is the number of Z (which in birds is only one-third of that in mammals). In
chromosomes that regulates male development3. The sex most species, the W chromosome is considerably smaller
chromosome aneuploids (Box 1) required to answer this and, without appropriate staining techniques, is some-
question have yet to be identified, but recent molecular times difficult to distinguish from the many microchromo-
analyses and gene mapping data have given the first hints somes. In some species, from taxa as diverse as Piciformes,

188 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(00)01821-8 TREE vol. 15, no. 5 May 2000

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 chromosomes.
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 phenotype
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 phenotype). 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
TREE vol. 15, no. 5 May 2000
REVIEWS
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 chromo-
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
Although all other birds have heteromorphic sex chromosomes, the sex
chromosomes of ratites are either indistinguishable or very similar. Together
with their strong banding homology29, this would indicate that ratite sex chromo-
somes have not yet differentiated. This idea gains further support from the
fact that ZOV3 and IREBP1, which are Z-linked in other birds, are found on
both the Z and the W chromosome in emus30. The observation of homomor-
phic, undifferentiated sex chromosomes in ratites was compatible with the
former assumption of a basal divergence between ratites (Palaeognathae)
and all other extant bird lineages (Neognathae) 70–100 million years ago.
However, recent data from whole mitochondrial DNA sequencing places
passeriform birds basal to Galliformes (e.g. chicken) and ratites31. If this is
correct, avian sex chromosomes might not have started to differentiate at
the time when modern bird lineages diverged. Alternatively, if this process
indeed preceded the split of extant lineages, sex chromosome homogenization
has taken place in ratites.
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,
189
REVIEWS

conclusion is probably premature. Notably, through com-

ATP5A1Z
parative mapping, the chicken Z chromosome has recently
HSA18
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
IFNA1, IFNB1 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
DMRT1 deleted in XY sex reversals, suggesting that one or several
HSA9 genes present within this region are required in two copies
GHR for normal male development in XY individuals [otherwise
VLDLR haploinsufficiency (Box 1) is caused]. If such a gene is
located on the Z chromosome of birds and has similar
BRM functions as those in mammals, one could speculate that it
NTRK2 might play a key role in avian sex determination.

OTC HSAX
CHD1Z HSA5
CHRNB3 HSA8
ACO1
ALDOB
GGTB2
HSA9
IREB1
TMOD
PTCH
GGAZ Human chromosomes
Trends in Ecology & Evolution
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, b polypeptide 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.
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
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 Drosophila and
C. elegans are essentially specific to the respective organ-
ism2. Recently, however, evidence for evolutionary con-
servation of a sex-determining gene has been found. The
mab-3 male sexual regulatory gene of C. elegans contains a
DNA-binding domain (DM-domain) with significant amino
acid homology to the Drosophila sexual 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. elegans mutants12; thus, mab-3 and dsx
are functionally interchangeable.
A gene with a DM-domain similar to mab-3 and dsx has
also been identified in humans, and has been designated
DMRT1 (originally DMT1)12. Interestingly, DMRT1 maps to
the small region on 9p24.3 implicated in sex reversal and is
a strong candidate gene for this trait13. DMRT1 is 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 DMRT1 to the Z chro-
mosome10, suggest that DMRT1 might 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 situ hybridization and
reverse transcriptase PCR (RT-PCR) studies of chicken
embryos14. DMRT1 is 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, DMRT1 expression 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 Sry is not conserved between mammals and
birds, another testis promoter is. In mammals, the gene
product of Sox9 acts downstream of Sry, probably by defin-
ing and maintaining Sertoli cell identity in males17. Appar-
ently triggered by a different mechanism, Sox9 also is
involved in regulating gonadal development in birds. At

190 TREE vol. 15, no. 5 May 2000

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the time when the gonads start to differ-

entiate in the avian embryo, Sox9 is ex- Table 1. Known DNA sequences of avian W chromosomes
pressed exclusively in the testes18. This
indicates further that birds and mammals Type of DNA Locus Homologue on Z Species Refs
might share molecular and physiological sequence chromosome
mechanisms for sex determination.
Genes CHD1W CHD1Z Conserved 19,20
ATP5A1W ATP5A1Z Conserved 9,28,32
Evolution of the avian sex Anonymous unique EE0.6 Yes Conserved 33,34
chromosomes from an ancestral DNAs DQSG10 Yes Goose 35
pair of autosomes RAPD-derived Anonymous No Available in many species, 36–38
So far, only a few genes (or potential cod- fragments but always species-
ing sequences) have been assigned to the specific
avian W chromosome (Table 1). Interest- Minisatellite Anonymous No Kite, wren, parrots and
39–42
ingly, these genes are present as one copy fragments skua
on W and one copy on Z, although they Repetitive DNAs Satellite No Several species, but 5,43,44
are not pseudoautosomal – they are pres- repeats always species- or
genus-specific
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 characterized. This, together with increased efforts to map
nonratite (Neognate) birds studied and sequence data sug- genes onto the sex chromosomes and the use of transgenic
gest that the two genes are evolving independently21. The techniques to study functional properties of candidate genes,
CHD1Z-CHD1W system offers a universal means for molecu- is likely to provide a detailed picture of avian sex deter-
lar sexing of nonratite birds, using straightforward PCR mination in the near future. In particular, the construction of
analysis22. Because some introns differ in size between a ZW bird transgenic for an additional copy of DMRT1 would
CHD1Z and CHD1W, conserved primer pairs that amplify provide interesting information on Z-chromosome dosage
both copies will reveal one PCR fragment in males (CHD1Z) and sex differentiation.
and two fragments in females (CHD1Z and CHD1W)23,24. Recent observations on the evolution of the avian sex
In addition to their use in molecular sexing, the CHD1Z chromosomes have provided answers but also new ques-
and CHD1W genes have allowed investigation of sex- tions. Future research should focus on the molecular evo-
specific mutation rates in birds, thus providing evidence lution of genes on the avian sex chromosomes to reveal
for a male-biased mutation rate (Box 3). what are the functional constraints associated with such
An intriguing issue in the evolution of the avian sex genes. For instance, are nonsynonymous substitution rates
chromosomes is what types of genes have remained on the equal in Z- and W-linked homologues of genes shared
W chromosome. In mammals, we know that many genes between the nonrecombining parts of the Z and W sex
present on the Y chromosome have male-specific func- chromosomes? In the wider perspective, one of the most
tions, so obviously there has been selection for their re- important questions is why some organisms have evolved
tention. Moreover, male-specific genes also have been male heterogamety, while in others females have become
acquired by Y through transposition25 and even retropos- the heterogametic sex? In order to solve this, comparative
ition26 (Box 1) from autosomal origins. If sex determination approaches addressing how sex chromosomes have evolved
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 Box 3. Male-biased avian mutation rate
relates to the fact that dosage compensation (Box 1) of Z- Because the two types of sex chromosomes spend different times in the
linked genes has not yet been found in birds27. If correct, in sexes, any difference in the sex-specific mutation rates should be mani-
cases where the lower amount of gene product produced fested by differing rates of sequence evolution on the two sex chromo-
by females would have an impact on fitness, there should somes (given no selection)45. Specifically, in birds, the rate of neutral
sequence evolution on the W chromosome unique to females should
be selection for retaining a functional homologue on the W directly reflect the female mutation rate. The rate of evolution of neutral
chromosome. This hypothesis is supported by the fact sequences on Z should be governed by a combination of the mutation rate in
that the few pairs of genes shared between Z and W, which males and females; from this, the male mutation rate can be inferred indir-
have been characterized to date, show a high degree of 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
sequence similarity12,21,28. However, overall little is known best approach for analysing sex-specific mutation rates, in the absence of
about how birds deal with the expression of Z-linked genes sequence data from a large number of genes, is to study genes shared
in males and females, respectively. between the sex chromosomes (yet independently evolving). Comparing the
sequences of different bird species, introns, as well as silent sites of CHD1Z,
Prospects 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
Sexual reproduction is one of the most widespread has been estimated. An excess of male mutations also has been revealed
features of life, yet an increasing body of evidence points from studies of the ATP5A1Z/ATP5A1W gene pair28.
to independent solutions to the physiology, genetics and The avian sex chromosome system offers an advantage over the mam-
molecular mechanisms of sexual development in different malian X and Y chromosomes for addressing sex-specific mutation rates. It
lineages. In fact, genes involved in sexual development has been suggested that the mutation rate of the X chromosome might be
seem to be among the most quickly evolving. However, in reduced specifically, owing to the avoidance of exposure of recessive del-
eterious mutations in hemizygote males46. If so, observations of a faster rate
spite of these general differences, parts of the enzymatic of neutral evolution on Y than on X might not necessarily be a result of vary-
cascades underlying sexual development can be con- ing sex-specific rates. However, in birds, estimates of a are conservative
served, as described above for DMRT1. Such common because the effect of a potential reduction in the Z-chromosome mutation
means will be important for dissecting the molecular basis rate would be the opposite of that given by higher male mutation rates.
of sexual development organisms that have not been well

TREE vol. 15, no. 5 May 2000 191

REVIEWS
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.
References
1 Koopman, P.J. et al. (1991) Male development of chromosomally
female mice transgenic for Sry. Nature 351, 117–121
2 Cline, T.W. and Meyer, B.J. (1996) Vive la différence: males vs
females in flies vs worms. Annu. Rev. Genet. 30, 637–702
3 Clinton, M. (1998) Sex determination and gonadal development:
a bird’s eye view. J. Exp. Zool. 281, 457–465
4 Bloom, S.E. et al. (1993) Constant and variable features of avian
chromosomes. In Manipulation of the Avian Genome (Etches, R.J.
and Gibbins, A.M.V., eds), pp. 39–60, CRC Press
5 Tone, M. et al. (1984) Genus specificity and extensive methylation of
the W chromosome-specific repetitive DNA sequences from the
domestic fowl, Gallus gallus domesticus. Chromosoma 89, 228–237
6 Mittwoch, U. (1971) Sex determination in birds and mammals. Nature
231, 432–434
7 Crew, F.A.E. (1954) Sex Determination, John Wiley & Sons
8 Halverson, J.J. and Dvorak, J. (1993) Genetic control of sex
determination in birds and the potential for its manipulation.
Poultry Sci. 72, 890–896
9 Fridolfsson, A-K. et al. (1998) Evolution of the avian sex
chromosomes from an ancestral pair of autosomes, Proc. Natl. Acad.
Sci. U. S. A. 95, 8147–8152
10 Nanda, I. et al. (1999) 300 million years of conserved synteny between
chicken Z and human chromosome 9. Nat. Genet. 21, 258–259
11 Bennet, C.P. et al. (1993) Deletion 9p and sex reversal. J. Med. Genet.
30, 518–520
12 Raymond, C.S. et al. (1998) Evidence for evolutionary conservation of
sex-determining genes. Nature 391, 691–695
13 Raymond, C.S. et al. (1999) A region of human chromosome 9p
required for testis development contains two genes related to known
sexual regulators. Hum. Mol. Genet. 8, 989–996
14 Raymond, C.S. et al. (1999) Expression of Dmrt1 in the genetical ridge
of mouse and chicken embryos suggests a role in vertebrate sexual
development. Dev. Biol. 215, 208–220
15 Smith, C.A. et al. (1999) Conservation of a sex-determining gene.
Nature 402, 601–602
16 Shimada, K. (1998) Gene expression of steroidogenic enzymes in
chicken embryonic gonads. J. Exp. Zool. 281, 450–456
17 Swain, A. and Lovell-Badge, R. (1999) Mammalian sex determination:
a molecular drama. Genes Dev. 13, 755–767
18 Morais da Silva, S. et al. (1996) Sox9 expression during
gonadal development implies a conserved role for the gene
in testis differentiation in mammals and birds. Nat. Genet.
14, 62–68
19 Ellegren, H. (1996) First gene on the avian W chromosome provides a
tag for universal sexing of non-ratite birds. Proc. R. Soc. London Ser. B
263, 1635–1641
20 Griffiths, R. et al. (1996) Sex identification in birds using two CHD
genes. Proc. R. Soc. London Ser. B 263, 1251–1256
21 Ellegren, H. and Fridolfsson, A-K. (1997) Male-driven evolution of
DNA sequences in birds. Nat. Genet. 17, 182–184
22 Ellegren, H. and Sheldon, B.C. (1997) New tools for sex identification
and the study of sex allocation in birds. Trends Ecol. Evol.
12, 255–259
23 Griffiths, R. et al. (1998) A DNA test to sex most birds. Mol. Ecol.
7, 1071–1075
24 Fridolfsson, A-K. and Ellegren, H. (1999) A simple and universal
method for molecular sexing of non-ratite birds. J. Avian Biol.
30, 116–121
25 Lahn, B.T. and Page, D.C. (1997) Functional coherence of the human
Y chromosome. Science 278, 675–680
192
26 Lahn, B.T. and Page, D.C. (1999) Retroposition of autosomal mRNA
yielded testis-specific gene family on human Y chromosome.
Nat. Genet. 21, 429–433
27 Baverstock, P.R. et al. (1982) A sex-linked enzyme in birds – Z
chromosome conservation but no dosage compensation. Nature
296, 763–766
28 Carmichael, A. et al. Male-biased mutation rates revealed from Z- and
W-chromosome linked ATP synthase a-subunit (ATP5A1) sequences
in birds. J. Mol. Evol. (in press)
29 Ansari, H.A. et al. (1988) Morphological differentiation of sex
chromosomes in three species of ratite birds. Cytogenet. Cell Genet.
47, 185–188
30 Ogawa, A. et al. (1998) The location of Z- and W-linked marker genes
and sequence on the homomorphic sex chromosomes of the ostrich
and the emu. Proc. Natl. Acad. Sci. U. S. A. 95, 4415–4418
31 Härlid, A. and Arnason, U. (1999) Analyses of mitochondrial DNA nest
ratite birds within the Neognathae: supporting a neotenous origin of
ratite morphological characters. Proc. R. Soc. London Ser. B
266, 305–309
32 Dvorak, J. et al. (1992) cDNA cloning of a Z- and W-linked gene in
Gallinaceous birds. J. Hered. 83, 22–25
33 Ogawa, A. et al. (1997) Molecular characterization and cytological
mapping of a non-repetitive DNA sequence region from the W
chromosome of chicken and its use as a universal probe for sexing
Carinatae birds. Chromosome Res. 5, 93–101
34 Itoh, Y. et al. (1997) Identification of the sex of Oriental white stork,
Ciconia boyciana, by the polymerase chain reaction based on its sex
chromosome-specific DNA sequences. Genes Genet. Syst. 72, 51–56
35 Quinn, T.W. et al. (1990) Molecular sexing of geese using a cloned
Z chromosomal sequence with homology to the W chromosome.
Auk 107, 199–202
36 Griffiths, R. and Tiwari, B. (1993) The isolation of molecular genetic
markers for the identification of sex. Proc. Natl. Acad. Sci. U. S. A.
90, 8324–8326
37 Sabo, T.J. et al. (1994) PCR-based method for sexing Roseate terns
(Sterna dougallii). Auk 111, 1023–1027
38 Lessells, C.M. and Mateman, A.C. (1998) Sexing birds using random
amplified polymorphic DNA (RAPD) markers. Mol. Ecol. 7, 187–195
39 Rabenold, P.P. et al. (1991) Polymorphic minisatellite amplified on
avian W chromosome. Genome 34, 489–493
40 Miyaki, C.Y. et al. (1992) Sex typing of Aratinga parrots using the
human minisatellite probe 33.15. Nucleic Acids Res. 19, 5235–5236
41 May, C.A. et al. (1993) Polymorphic sex-specific sequences in birds of
prey. Proc. R. Soc. London Ser. B 233, 271–276
42 Millar, C.D. et al. (1992) Sex-specific restriction fragments and sex-
ratios revealed by DNA fingerprinting in the Brown skua. J. Hered.
83, 350–355
43 Griffiths, R. and Holland, P.W.H. (1990) A novel avian W chromosome
DNA repeat sequence in the lesser black-backed gull (Larus fuscus).
Chromosoma 99, 243–250
44 Saitoh, Y. and Mizuno, S. (1992) Distribution of XhoI and EcoRI family
repetitive DNA sequences into separate domains in the chicken
W chromosome. Chromosoma 101, 474–477
45 Hurst, L.D. and Ellegren, H. (1998) Sex biases in the mutation rate.
Trends Genet. 14, 446–452
46 McVean, G.T. and Hurst, L.D. (1997) Evidence for a selectively
favourable reduction in the mutation rate of the X chromosome.
Nature 386, 388–392
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TREE vol. 15, no. 5 May 2000