Directory UMM :Data Elmu:jurnal:P:PlantScience:ecology:21-40:

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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 deterY chromosome is crucial for birds that causes the avian embryo to develop mination. Moreover, these new
development of the male phenoa female phenotype, analogous to the
data give insights into the evotype in mammals. Intensive search
dominance mode of genic sex differentiation
lution of heteromorphic sex chrofor 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 disthe 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
mammals, birds’ closest relatives,
elegans? Although definite answers to these
questions cannot be given yet, some recent
species studied so far. Sry triggers
for which detailed knowledge on
data have provided support for the latter
a cascade of proteins involved in
sex differentiation processes is
hypothesis. Moreover, despite the potentially
male development that are enavailable.
common features of sex determination in

coded by autosomal, as well as Xmammals and birds, comparative mapping
The avian sex chromosomes
and Y-linked, genes. However, the
shows that the avian sex chromosomes have
The Z and W chromosomes of
role of Sry as the key to sex differa different autosomal origin than the
birds share many features with
entiation does not extend outside
mammalian X and Y chromosomes.
mammalian X and Y chromomammals2. For instance, birds
somes, respectively. Both avian
appear to have a different system
sex chromosomes are metacenfor sex differentiation, although
the knowledge of how this system Hans Ellegren is at the Dept of Evolutionary Biology, tric. They pair during meiosis and
Evolutionary Biology Centre, Uppsala University,
a synaptonemal complex (Box 1)
operates is lagging far behind
Norbyvägen 18D, SE-752 36 Uppsala, Sweden
is formed at the end of the short
what we know about mammals.

(hans.ellegren@evolution.uu.se).
arms of the two chromosomes;
Importantly, avian sex chromotherefore, a small pseudoautossomes show a reversed organomal region (Box 1) exists.
ization compared with mammals,
Typically, the Z chromosome is
females being heterogametic ZW
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 somequestion have yet to be identified, but recent molecular times difficult to distinguish from the many microchromoanalyses 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

REVIEWS
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 chromosome expansion operating on the two sex chromosomes.
Another exception to the general pattern of avian sex chromosome 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 constitutive heterochromatin (Box 1), which is otherwise only
found in high densities at the centromeres of microchromosomes and at one of the ends of the Z chromosome, at least
in chickens. The heterochromatic region of the W chromosome 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 determination 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 balance between X chromosomes and autosomes determining femaleness (the latter is the case in Drosophila and
C. elegans). However, in birds the corresponding aneuploids are extremely rare, if they exist at all. If a male phenotype 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 phenotype 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 single (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 phenotype 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 different taxa. This approach is one of the most important in
genome projects, allowing map information to be transferred 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

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 chromosomes try to balance the expression of genes on one of the sex chromosomes 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 recombine. 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 chromosomes 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 homomorphic, 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 vertebrate, this would be suggestive of the two taxa sharing molecular 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, mapping places genes from the chicken Z chromosome on several different human autosomes9. So far, only one Z-linked
gene (OTC) has been found on the human X chromosome,

189

REVIEWS

ATP5A1Z

HSA18

IFNA1, IFNB1

DMRT1
GHR

HSA9

VLDLR
BRM
NTRK2
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 associated, actin-dependent regulator of chromatin, subfamily A, member 2;
NTRK2, neurotrophic tyrosine kinase receptor 2; OTC, ornithine transcarbamylase; 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 determination 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

190

conclusion is probably premature. Notably, through comparative 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 dysgenesis 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 Drosophila and
C. elegans are essentially specific to the respective organism2. Recently, however, evidence for evolutionary conservation 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 differentiation 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 proteins 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 chromosome10, suggest that DMRT1 might also be involved in
regulating sexual differentiation in birds, through Z chromosome 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 antiMüllerian 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 defining and maintaining Sertoli cell identity in males17. Apparently triggered by a different mechanism, Sox9 also is
involved in regulating gonadal development in birds. At
TREE vol. 15, no. 5 May 2000

REVIEWS
the time when the gonads start to differentiate in the avian embryo, Sox9 is expressed exclusively in the testes18. This
indicates further that birds and mammals
might share molecular and physiological
mechanisms for sex determination.

Table 1. Known DNA sequences of avian W chromosomes
Type of DNA
sequence

Locus

Homologue on Z Species
chromosome

Refs

Genes

CHD1W
ATP5A1W
EE0.6
DQSG10
Anonymous

CHD1Z
ATP5A1Z
Yes
Yes
No

19,20
9,28,32
33,34
35
36–38

Conserved
Conserved
Conserved
Goose
Available in many species,
but always speciesspecific
Kite, wren, parrots and
skua
Several species, but
always species- or
genus-specific

Evolution of the avian sex
Anonymous unique
chromosomes from an ancestral
DNAs
pair of autosomes
RAPD-derived
So far, only a few genes (or potential codfragments
ing sequences) have been assigned to the
Minisatellite
Anonymous
No
39–42
avian W chromosome (Table 1). Interestfragments
ingly, these genes are present as one copy
Repetitive DNAs
Satellite
No
5,43,44
on W and one copy on Z, although they
repeats
are not pseudoautosomal – they are present 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 deterlar 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.
Recent observations on the evolution of the avian sex
and two fragments in females (CHD1Z and CHD1W)23,24.
In addition to their use in molecular sexing, the CHD1Z chromosomes have provided answers but also new quesand CHD1W genes have allowed investigation of sex- tions. Future research should focus on the molecular evospecific mutation rates in birds, thus providing evidence lution of genes on the avian sex chromosomes to reveal
what are the functional constraints associated with such
for a male-biased mutation rate (Box 3).
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 chromosomes, it becomes less straightforward to invoke sex-speBox 3. Male-biased avian mutation rate
cific roles for genes retained on W. Perhaps the answer
relates to the fact that dosage compensation (Box 1) of ZBecause 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 manifested by differing rates of sequence evolution on the two sex chromocases where the lower amount of gene product produced
somes (given no selection)45. Specifically, in birds, the rate of neutral
by females would have an impact on fitness, there should
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
males and females; from this, the male mutation rate can be inferred indirthat the few pairs of genes shared between Z and W, which
ectly given that a Z chromosome spends exactly two-thirds of its time in the
have been characterized to date, show a high degree of
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
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 conserved, 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
TREE vol. 15, no. 5 May 2000

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 mammalian 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 deleterious 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 varying sex-specific rates. However, in birds, estimates of a are 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.

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.
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TREE vol. 15, no. 5 May 2000