Structure and evolution of the avian W- and Z-sex
chromosomes, especially as this relates to molecular, DNA-based sex identification
of birds.
Most, but not all, birds have differentiated sex chromosomes. Among these
(neognathous) birds males are characterized by the occurrence of two Z
chromosomes whereas in females one of the Z chromosomes is replaced by
a female-specific W chromosome. Whereas the Z chromosome carries many
genes, the W chromosome carries only a few. Current evidence suggests
strongly that the W chromosome has been derived from an ancestral Z chromosome
as a result of loss of a large percentage (>98%) of the Z-chromosomal
genes. It is thought that this loss of genes has been the result of the
cessation of recombination between the two chromosomes early in avian
evolution, approximately 100 - 150 million years ago, which caused the
accumulation of mutations in the W chromosome and the inactivation and
the loss of the affected genes. Since male birds contain two Z chromosomes
this latter chromosome can still recombine and consequently avoid the
accumulation of genetic damage. The loss of identifiable genes on the
W chromosome has however been accompanied by the acquisition of DNA components
of unknown function. Often this DNA component consists of long stretches
of repeated short sequence elements. Such sequence elements are characteristic
for the heterochomatic, dense segments of the chromosomes. This makes
it possible to apply staining procedures which render the W chromosome
uniquely visible by microscopic observation, and consequently allow for
the cytological sex identification of neognathous birds.
Although most of the Z-chromosomal genes therefore lack a counterpart
on the W chromosome, this latter chromosome is not completely genetically
inert. There are still a few genes which occur in an active W-chromosomal
and Z-chromosomal form. These genes include e.g. the CHD gene, an ATP
synthase gene, a protein kinase gene and the spindlin gene. Not all birds
contain the W-chromosomal form of all these genes. Research at Avian Biotech
has shown that in certain parrots, notably the African grey parrot (Psittacus
erythacus) the W-chromosomal form of the ATP synthase gene has also been
lost (1). But where found the W- and Z-chromosomal form of these genes
have a considerable difference in nucleotide sequence as a result of their
long (100 - 150 million years), separate evolution. This sequence difference
is the basis of modern molecular, DNA based sex identification procedures.
In addition to the neognathous birds there exists another group, the palaeognaths
which includes the ratites (ostriches, emus etc.) and the tinamous. Palaeognathous
birds have W and Z chromosomes, which are largely identical and microscopically
indistinguishable. Instead of having lost most of the genes found on the
Z chromosome as in the neognaths, the palaeognath W carries most of these
genes. Contrary to what is found in neognathous birds, recombination between
the palaeognathous W and Z chromosome occurs over their entire length,
which explains the retention of the genes on the W chromosome. Although
not characterized, the paleognath W chromosome must however carry some
genetic activity involved in femaleness, therefore original evidence for
the existence of a palaeognathous W chromosome was initially genetic.
Recent research has identified several DNA sequence elements which are
unique for the palaeognath female, although none of these elements has
any known, identifiable function in female sex differentiation. Most of
these female specific elements are specific for the individual species.
Research at Avian Biotech (2) identified e.g. a DNA sequence element which
is female specific for the emu (Dromaius novaehollandiae), but not female
specific for the ostrich (Struthio camellus), kiwis (Apteryx) or rheas
(Rhea americana), although it is also female specific for the different
cassowaries (Casuarius) which are closely related to the emu.
Tinamous are classified traditionally, based on certain anatomical evidence,
as palaeognathous avian species. Microscopic evidence has shown that the
tinamou W chromosome is structurally intermediate between the highly heterochromatic
W chromosome of the neognathous avian species and the extended, euchromatic
form of the ratites. Such studies have also revealed that the tinamous
W and Z chromosome recombine only over a segment of their length. Further
analysis at Avian Biotech (3, 4) has shown that most of the genes which
occur on the neognathous W and Z chromosome in different forms are identical
in tinamous, except for the spindlin gene, which occurs in a W- and Z-chromosomal
form in these birds. This difference between the W and Z spindlin gene
allows therefore the molecular, DNA based sex identification by procedures
which can also be used for the neognathous species. Since tinamous are
paleognaths, which are an entirely different group of birds than the neognaths,
these results suggest strongly that the cessation of recombination, which
is most likely the underlying reason for the degeneration of the avian
W chromosome, occurred independently in these two avian groups, a finding
in line with what is known about the evolution of sex chromosomes in general,
where such degeneration has occurred numerous times in different animal
families.
References
1) De Kloet, S. R. 2001. Loss of the gene for the alpha subunit of ATP
synthase (ATP5W1) from the W chromosome of the African grey parrot (Psittacus
erithacus). J. Mol. Evol. 53:135-143.
2) De Kloet, S. R. 2001. Development of
a CAPS (cleaved amplified polymorphic sequence) assay for sex identification
of the emu (Dromaius novaehollandiae). Mol. Ecol. Notes 1:273-274.
3) De Kloet, S. R. 2002. Molecular sex
identification of tinamous with PCR using primers derived from the spindlin
gene. Mol. Ecol. Notes 2:465-466.
4) De Kloet, R. S., and S. R. de Kloet.
2003. Evolution of the spindlin gene in birds: independent cessation of
the recombination of sex chromosomes at the spindlin gene in neognathous
birds and tinamous,
a palaeognathous avian family. Genetica 119:333-342.
5) De Kloet, R. S. and de Kloet, S. R.
2005. The evolution of the
spindlin gene in birds: Sequence analysis of an intron of the
spindlin W and Z gene reveals four major divisions of the
Psittaciformes. Mol. Phyl. and Evol. 36: 706-721.
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