Original Article
Cytogenet Genome Res 2011;132:165–181
DOI: 10.1159/000322358
Accepted: June 30, 2010
by J. Smith
Published online: November 22, 2010
Synteny Conservation of Chicken
Macrochromosomes 1–10 in Different
Avian Lineages Revealed by Cross-Species
Chromosome Painting
I. Nanda P. Benisch D. Fetting T. Haaf M. Schmid Department of Human Genetics, University of Würzburg, Würzburg, Germany
Key Words
Birds Chicken Chromosome painting Cross-species
hybridization FISH Macrochromosomes Synteny
conservation
Abstract
Cross-species chromosome painting can directly visualize
syntenies between diverged karyotypes and, thus, increase
our knowledge on avian genome evolution. DNA libraries
of chicken (Gallus gallus, GGA) macrochromosomes 1 to 10
were hybridized to metaphase spreads of 9 different species
from 3 different orders (Anseriformes, Gruiformes and Passeriformes). Depending on the analyzed species, GGA1–10
delineated 11 to 13 syntenic chromosome regions, indicating a high degree of synteny conservation. No exchange between the GGA macrochromosome complement and microchromosomes of the analyzed species was observed. GGA1
and GGA4 were distributed on 2 or 3 chromosomes each in
some of the analyzed species, indicating rare evolutionary
rearrangements between macrochromosomes. In all 6 analyzed species of Passeriformes, GGA1 was diverged on 2
macrochromosomes, representing a synapomorphic marker
for this order. GGA4 was split on 2 chromosomes in most
karyotypes, but syntenic to a single chromosome in black-
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cap (Passeriformes). GGA5/10 and also GGA8/9 associations
on chromosomes were found to be important cytogenetic
features of the Eurasian nuthatch (Passeriformes) karyotype.
Fusion of GGA4 and GGA5 segments and of entire GGA6 and
GGA7, respectively, was seen in the 2 analyzed species of
Gruiformes. Consistent with the literature, our inter-species
chromosome painting demonstrates remarkable conservation of macrochromosomal synteny over 100 million years of
avian evolution. The low rate of rearrangements between
macrochromosomes and the absence of detectable macrochromosome-microchromosome exchanges suggests a
predominant role for rearrangements within the genedense microchromosome complement in karyotypic diversification.
Copyright © 2010 S. Karger AG, Basel
Chicken represents the basal lineage (Galloanserae) in
avian phylogeny. It is the most extensively analyzed bird
species with a draft genome sequence. Compared with
other vertebrate models, the chicken genome is organized
in a dichotomous fashion [Bloom et al., 1993]. It consists
of 11 pairs of large macrochromosomes (including the sex
chromosomes) and 28 pairs of microchromosomes which
can not be easily distinguished from each other [Schmid
Michael Schmid
Department of Human Genetics, University of Würzburg, Biocenter, Am Hubland
DE–97074 Würzburg (Germany)
Tel. +49 931 318 4077, Fax +49 931 318 4058
E-Mail m.schmid @ biozentrum.uni-wuerzburg.de
et al., 2000; Masabanda et al., 2004]. The organization
into numerous microchromosomes and relatively few
macrochromosomes is an ancestral feature of avian genomes, including phylogenetically distant paleognathous
species and is even seen in some lower vertebrates [Christidis, 1990]. Synteny mapping between GGA microchromosomes and zebrafish chromosomes confirmed their
ancestral state [Burt, 2002].
Comparative cytogenetic studies on extant birds revealed considerable variation of diploid chromosome
numbers ranging from 42 to 132. However, the majority
(about 65%) of cytogenetically analyzed species from
widely different orders displayed 76 to 82 chromosomes,
including 7 to 8 pairs of macrochromosomes [Christidis,
1990]. Exceptions are some Falconiformes and 1 species
of Charadriiformes whose karyotypes are derived, containing higher numbers of macrochromosomes and relatively few microchromosomes [De Boer, 1976; Bed’Hom
et al., 2003; Nie et al., 2009]. Similar genome organization among birds suggests a low rate of chromosomal
rearrangements during avian radiation, compared to the
rapid chromosome evolution in mammals [Yang et al.,
1997; Wienberg, 2004]. There also may be a high degree
of similarity between different avian genomes at the genetic level. Interspecies hybridization among birds,
which strictly depends on genome and karyotype similarity, is relatively high both in natural and captive avian
populations [Prager and Wilson, 1975; Grant and Grant,
1992].
Early G-banding studies already indicated some homologies between the macrochromosomes of species
from several families [Stock et al., 1974; Takagi and Sasaki, 1974; Ansari et al., 1986]. However, banding similarities provide only indirect (structural) information
and do not necessarily reflect homologies at the molecular level [Stanyon et al., 1995]. Comparative painting
with chromosome-specific DNA libraries allows one to
directly visualize chromosomal homologies among phylogenetically distant species [Scherthan et al., 1994;
Chowdhary et al., 1998; Ferguson-Smith and Trifonov,
2007]. Over the past decade (unidirectional) painting
studies with GGA macrochromosomes revealed extensive syntenies between dozens of avian species [Shetty et
al., 1999; Raudsepp et al., 2002; Guttenbach et al., 2003;
Derjusheva et al., 2004; Shibusawa et al., 2004; Nanda et
al., 2006]. Recently, paints from the highly derived chromosomes of stone curlew (Burhinus oedicnemus), a nongalliform bird were also used for avian genome comparisons [Hansmann et al., 2009; Nie et al., 2009]. Since
chicken has retained the ancestral avian karyotype,
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Cytogenet Genome Res 2011;132:165–181
cross-species hybridization with GGA paints allows reconstruction of evolutionary chromosome rearrangements among modern birds. With the exception of birds
of prey and some parrots [de Oliveira et al., 2005; Nanda
et al., 2006, 2007], GGA macrochromosome painting revealed relatively few rearrangements in bird karyotypes;
even in paleognathous birds the macrochromosomes appear to be well conserved [Shetty et al., 1999; NishidaUmehara et al., 2007]. However, considering the high
number and diversity of bird species among terrestrial
vertebrates, macrochromosome conservation has to be
confirmed in more avian groups. So far, comparative
painting studies have been performed mainly in agriculturally important or domesticated species and rarely in
wild birds.
Here we have used GGA macrochromosome paints
to delineate genomic rearrangements in 9 bird species.
The majority of the analyzed species are Passeriformes,
the largest avian group, showing a wide range of ecological diversification. Enormous efforts have been
made in the last years to develop genetic maps of several Passeriformes which are good models for studying
the genetic basis of ecologically important traits as well
as complex evolutionary processes such as sexual selection, inbreeding, foraging behavior and speciation
[Backström et al., 2008; Hale et al., 2008; Jaari et al.,
2009]. Genetic data from some Passeriformes showed a
high recombination rate in the heterogametic female sex
[Stauss et al., 2003; Hansson et al., 2005; Jaari et al.,
2009], challenging the current view on sex-specific recombination. Cross-species chromosome painting in
representative species of Passeriformes will not only facilitate the generation of genetic maps but also provide
novel insights into avian karyotype evolution. So far,
only a few Passeriformes have been analyzed, revealing
a high degree of synteny conservation of macrochromosomes [Guttenbach et al., 2003; Derjusheva et al., 2004;
Itoh and Arnold, 2005].
Materials and Methods
Analyzed Species and Chromosome Preparation
Nine representative species of modern (neognathous) birds
were included in this study: wood duck (Aix sponsa, ASP; Anatidae, Anseriformes); coot (Fulica atra, FAT; Rallidae, Gruiformes);
common moorhen (Gallinula chloropus, GCH; Rallidae, Gruiformes); common magpie (Pica pica, PPI; Corvidae, Passeriformes), Eurasian jay (Garrulus glandarius, GGL; Corvidae, Passeriformes); Eurasian nuthatch (Sitta europaea, SEU; Sittidae,
Passeriformes); blackcap (Sylvia atricapilla, SAT; Sylviidae, Passeriformes); great tit (Parus major, PMA; Paridae, Passeriformes)
Nanda/Benisch/Fetting/Haaf/Schmid
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GGA-4
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GGA-7
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GGA-10
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1
(For legend see next page.)
Synteny Conservation of Chicken
Chromosomes 1–10 in Avian Lineages
Cytogenet Genome Res 2011;132:165–181
167
and coal tit (Periparus ater, PAT; Paridae, Passeriformes). Mitotic
chromosomes were prepared from fibroblast cultures, following
standard procedures [Schmid et al., 1989]. Individual macrochromosomes were identified by conventional Giemsa and/or DAPI
staining. In some species, constitutive heterochromatin was visualized by C-banding [Sumner, 1972].
Fluorescence in situ Hybridization (FISH)
GGA chromosome-specific DNA libraries (from flow-sorted
chromosomes) were labeled with biotin-16-dUTP or digoxigenin-11-dUTP (Roche Diagnostics, Mannheim, Germany) by
DOP-PCR [Telenius et al., 1992]. Probes were hybridized and
detected, as described earlier [Guttenbach et al., 2003; Nanda et
al., 2007]. FISH images were recorded with a Zeiss Axiophot microscope equipped with a CCD camera and the appropriate filter
sets. FITC and DAPI images were merged using the Applied
Spectral Imaging software (Easyfish 1.0; Neckarhausen, Germany).
ASP1
ASP2
ASP3
ASP5
ASP6
A
Results
Of each species, some high-quality metaphase spreads
were Giemsa-stained to confirm the published diploid
chromosome number and to exclude culture-induced
macrochromosome rearrangements. To establish chromosomal syntenies, paints of GGA macrochromosomes
1–10 were cross-hybridized to representative metaphase
spreads. All painting probes generated distinct hybridization signals, mainly on a single chromosome pair of a
given species. About 10 DAPI-stained metaphases were
examined for each probe and species to identify syntenic
chromosomes. Comparative chromosome painting results are presented in figures 1–10. Synteny data on all 9
analyzed species are summarized in figure 11. An interesting observation from cross-species painting analyses
is the favored location of FISH signals defining the syntenic chromosomes at the nuclear periphery in most interphase nuclei (fig. 12).
Chromosomal Syntenies between Chicken and
A. sponsa (Anseriformes)
The Giemsa-stained karyotype of A. sponsa consists
of 2n = 80 chromosomes. In contrast to an earlier study
[Christidis, 1990], which classified ASP1 as an acrocen-
Fig. 1. FISH of chicken (GGA) macrochromosome paints 1–10 on
DAPI-stained chromosomes of A. sponsa. Left: FITC hybridization signals on the respective GGA chromosomes. Right: crossspecies hybridization to the ASP karyotype.
168
Cytogenet Genome Res 2011;132:165–181
B
C
Fig. 2. A Hybridization of GGA1–3, 5, and 6 to the syntenic A.
sponsa chromosomes. Note the absence of hybridization signals
in heterochromatic pericentromeric regions. B Two-color FISH of
GGA1 (red) and GGA9 (green) to ASP metaphase. Note a small
region syntenic to GGA9 on the proximal long arm of ASP1. C Cbanding of the same ASP metaphase showing large blocks of constitutive heterochromatin at the centromeres of macrochromosomes.
tric chromosome, ASP1 was clearly submetacentric.
With the exception of GGA4, which was distributed on
2 ASP pairs, all GGA macrochromosomes were conserved as entire units in wood duck (fig. 1). The large
C-band positive paracentromeric region on ASP1 and
smaller regions on ASP2 and ASP3 remained unlabeled
(fig. 2A). Because most centromeric satellite DNAs are
species-specific, they do not react with cross-species
painting probes [Yang et al., 1997; Neusser et al., 2001].
Interestingly, GGA9 does not only label the syntenic
ASP macrochromosome 9 but also hybridizes to a small
segment on the proximal long arm of ASP1, close to the
paracentromeric heterochromatin (fig. 2B, C). Most
likely, a small GGA9-syntenic segment has been translocated to ASP1. On the other hand, we cannot rule out
that the GGA9 probe cross-hybridizes with unknown
repetitive sequences in the paracentromeric region of
ASP1.
Nanda/Benisch/Fetting/Haaf/Schmid
Chromosomal Syntenies between Chicken and
Passeriformes (P. pica, G. glandarius, S. europaea,
S. atricapilla, P. major and P. ater)
Passeriformes represent the largest group of extant
birds. Here we performed cross-hybridization experiments in 6 different species from 4 different families. The
diploid chromosome numbers range from 74 to 80, but
the macrochromosome complements appear to be very
similar except for the 2 metacentric chromosomes (6 and
7) in SEU. In most Passeriformes (PPI, GGL, PMA and
PAT) the 10 GGA macrochromosomes delineated 12 syntenic segments (figs. 3, 4, 7 and 8) whereas 11 and 13 syntenic segments were found in SAT and SEU (figs. 5, 6),
respectively. In SEU, GGL, PPI, PMA and PAT, GGA4 is
split on 2 different chromosomes. One corresponds to
chromosome 4; the other one is a smaller macrochromosome. In contrast, GGA4 highlights only a single acrocentric macrochromosome (SAT5) in blackcap (fig. 5).
GGA1 is split on 2 large macrochromosomes in all 6 analyzed Passeriformes. GGA2, 3, and 5–10 are conserved as
whole chromosomes in Passeriformes except in SEU. The
smaller GGA macrochromosomes (8–10), though each
was represented by a single hybridization site, identified
syntenic regions on one arm of the bi-armed chromosomes in S. europaea. Additionally, the syntenic regions
corresponding to GGA5 and 10 and also GGA8 and 9
were associated on SEU6 and 7, respectively (fig. 6). Similar to A. sponsa, no hybridization signals were detected
on microchromosomes.
Chromosomal Syntenies between Chicken and
Gruiformes (F. atra and G. chloropus)
Both F. atra and G. chloropus belong to the family of
Rallidae [Hammar, 1970]. They display a higher number
of bi-armed macrochromosomes (pairs 1–5) than the
other birds in this study. Although coot and common
moorhen differ in their chromosome numbers, macrochromosome structure and number are conserved. All
GGA paints produced identical hybridization patterns in
both species. GGA1–10 are syntenic to 13 FAT and GCH
chromosomes, respectively. GGA4, 5, 6 and 7 labeled different arms of (sub)metacentric chromosomes (figs. 9,
10). Interestingly, GGA4 was distributed on 3 chromosomes in Gruiformes. One large GGA4-syntenic region
corresponds to the short arm of the metacentric FAT4
and GCH4. In addition, GGA4 labeled 2 smaller macrochromosomes (fig. 9). GGA5 was split on 2 chromosomes
in both species, the short arm of a large metacentric chromosome and a smaller macrochromosome. GGA6 and
GGA7 hybridized to different arms of a metacentric
Synteny Conservation of Chicken
Chromosomes 1–10 in Avian Lineages
chromosome (figs. 9, 10). Two-color FISH revealed that
GGA4- and 5-syntenic segments are fused on FAT4
(fig. 10C) and GCH4 (fig. 10A), respectively. The entire
GGA6 and 7 are fused on FAT5 (fig. 10D) and GCH5
(fig. 10B), respectively.
Discussion
Cross-species chromosome painting is a powerful tool
to delineate syntenic chromosome regions among closely
and distantly related species and to reconstruct chromosomal phylogeny. GGA chromosome painting in widely
different species ranging from primitive (paleognathous)
birds such as emu to some highly evolved Passeriformes
showed conservation of macrochromosomal synteny
during avian evolution [Shetty et al., 1999; Raudsepp et
al., 2002; Guttenbach et al., 2003; Derjusheva et al., 2004;
Shibusawa et al., 2004; Itoh and Arnold, 2005; Griffin et
al., 2007]. Our present results on some additional bird
species are in line with earlier studies. Comparative genemapping data even revealed remarkable synteny between
Fig. 3. FISH of GGA1–10 paints on DAPI-stained chromosomes
of P. pica. Left: FITC hybridization signals on the respective GGA
chromosomes. Right: cross-species hybridization to the PPI
karyotype.
Fig. 4. FISH of GGA1–10 paints on DAPI-stained chromosomes
of G. glandarius. Left: FITC hybridization signals on the respective GGA chromosomes. Right: cross-species hybridization to the
GGL karyotype.
Fig. 5. FISH of GGA1–10 paints on DAPI-stained chromosomes
of S. atricapilla. Left: FITC hybridization signals on the respective
GGA chromosomes. Right: cross-species hybridization to the
SAT karyotype.
Fig. 6. FISH of GGA1–10 paints on DAPI-stained chromosomes
of S. europaea. Left: FITC hybridization signals on the respective
GGA chromosomes. Right: cross-species hybridization to the
SEU karyotype.
Fig. 7. FISH of GGA1–10 paints on DAPI-stained chromosomes
of P. major. Left: FITC hybridization signals on the respective
GGA chromosomes. Right: cross-species hybridization to the
PMA karyotype.
Fig. 8. FISH of GGA1–10 paints on DAPI-stained chromosomes
of P. ater. Left: FITC hybridization signals on the respective GGA
chromosomes. Right: cross-species hybridization to the PAT
karyotype.
Fig. 9. FISH of GGA1–10 paints on DAPI-stained chromosomes
of F. atra. Left: FITC hybridization signals on the respective GGA
chromosomes. Right: cross-species hybridization to the FAT
karyotype.
(For figures see next pages.)
Cytogenet Genome Res 2011;132:165–181
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GGA-1
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GGA-6
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Cytogenet Genome Res 2011;132:165–181
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7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
ZW
GGA-8
ZW
GGA-9
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
ZW
GGA-10
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
ZW
4
Synteny Conservation of Chicken
Chromosomes 1–10 in Avian Lineages
Cytogenet Genome Res 2011;132:165–181
171
GGA-1
2
3
4
5
6
7
8
9
10
11
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
12
1
12
ZW
GGA-2
1
2
3
4
5
6
7
8
9
10
11
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
ZW
GGA-3
ZW
GGA-4
ZW
GGA-5
ZW
GGA-6
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
ZW
GGA-7
ZW
GGA-8
ZW
GGA-9
ZW
GGA-10
ZW
5
172
Cytogenet Genome Res 2011;132:165–181
Nanda/Benisch/Fetting/Haaf/Schmid
GGA-1
1
2
3
4
5
6
7
8
9
10
11
12
14
15
16
17
18
19
20
21
22
23
24
25
26
29
30
31
32
33
34
35
36
37
38
39
27
28
13
ZZ
GGA-2
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
29
30
31
32
33
34
35
36
37
38
39
27
28
ZZ
GGA-3
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
29
30
31
32
33
34
35
36
37
38
39
13
ZZ
GGA-4
27
28
ZZ
GGA-5
1
2
3
4
5
6
7
8
9
10
11
12
14
15
16
17
18
19
20
21
22
23
24
25
26
29
30
31
32
33
34
35
36
37
38
39
13
27
28
ZZ
GGA-6
1
2
3
4
5
6
7
8
9
10
11
12
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
16
17
18
19
20
21
22
23
24
25
26
ZZ
GGA-7
14
15
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
ZZ
GGA-8
27
28
16
17
18
19
20
21
22
23
24
25
26
29
30
31
32
33
34
35
36
37
38
39
ZZ
GGA-9
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
29
30
31
32
33
34
35
36
37
38
39
27
28
ZZ
GGA-10
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
29
30
31
32
33
34
35
36
37
38
39
27
28
ZZ
6
Synteny Conservation of Chicken
Chromosomes 1–10 in Avian Lineages
Cytogenet Genome Res 2011;132:165–181
173
GGA-1
1
2
3
14
15
16
27
28
29
5
6
17
18
30
31
4
7
8
19
20
21
32
33
34
9
12
13
10
11
22
23
24
25
26
35
36
37
38
39
ZW
GGA-2
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
ZW
GGA-3
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
ZW
GGA-4
ZW
GGA-5
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
21
22
23
24
25
26
34
35
36
37
38
39
ZW
GGA-6
14
15
16
17
18
19
20
27
28
29
30
31
32
33
ZW
GGA-7
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
ZW
GGA-8
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
ZW
GGA-9
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
38
39
ZW
GGA-10
27
28
29
30
31
32
33
34
35
36
37
ZW
7
174
Cytogenet Genome Res 2011;132:165–181
Nanda/Benisch/Fetting/Haaf/Schmid
GGA-1
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
ZZ
GGA-2
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
ZZ
GGA-3
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
ZZ
GGA-4
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
ZZ
GGA-5
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
ZZ
GGA-6
ZZ
GGA-7
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
ZZ
GGA-8
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
17
18
22
23
24
25
26
ZZ
GGA-9
14
15
16
19
20
21
27
28
29
30
31
32
33
34
35
36
37
38
39
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
ZZ
GGA-10
ZZ
8
Synteny Conservation of Chicken
Chromosomes 1–10 in Avian Lineages
Cytogenet Genome Res 2011;132:165–181
175
GGA-1
1
7
8
9
10
11
12
13
14
15
21
22
23
24
25
26
27
28
29
30
35
36
37
38
39
40
41
42
43
44
45
5
6
7
8
9
10
11
12
13
14
15
2
3
4
5
16
17
18
19
20
31
32
33
34
1
2
3
4
6
ZZ
GGA-2
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
ZZ
GGA-3
ZW
GGA-4
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
ZW
GGA-5
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
ZW
GGA-6
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
ZZ
GGA-7
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
ZW
GGA-8
ZZ
GGA-9
ZW
GGA-10
ZW
9
176
Cytogenet Genome Res 2011;132:165–181
Nanda/Benisch/Fetting/Haaf/Schmid
Fig. 10. 2-color FISH of GGA4/GGA5 and
GGA6/GGA7, respectively, on metaphase
spreads of G. chloropus (A , B) and F. atra
(C , D). A GGA4 (red) and GGA5 (green)
are linked on GCH4. B GGA6 (red) and
GGA7 (green) are linked on GCH5.
C GGA4 (red) and GGA5 (green) are
linked on FAT4. D GGA6 (red) and GGA7
(green) are linked on FAT5.
A
B
C
D
chicken and turtle macrochromosomes [Matsuda et al.,
2005]. Therefore, it is plausible to assume that the chicken
karyotype resembles the ancestral avian genome.
Our study on 9 avian species confirmed that most of
the 10 GGA macrochromosomes are conserved as entire
units. Synteny data on all the species are summarized in
figure 11. GGA paints labeled 11 syntenic segments in
wood duck, suggesting that only 1 evolutionary chromosome break separates chicken (Galliformes) and Anseriformes. Extraordinary conservation of macrochromosomal synteny has also been reported in 2 other species
of Anseriformes, Anser anser and Anas platyrhynchos
[Guttenbach et al., 2003; Schmid et al., 2005]. Galliformes
and Anseriformes are close relatives and together constitute a large phylogenetic group (Galloanserae), representing an early stage of divergence of modern birds [van
Tuinen et al., 2000]. It is, therefore, not surprising to detect a high level of chromosome homology between these
2 phylogenetic groups.
In all 6 analyzed species (4 families) of Passeriformes
and in 4 additional species published previously [Derjusheva et al., 2004; Itoh and Arnold, 2005] GGA1 is split
on 2 large macrochromosomes. This implies fission of the
ancestral GGA1 in a common ancestor of Passeriformes.
This fission is a synapomorphic trait that is shared by all
members of Passeriformes and distinguishes them from
Galliformes. Fission of GGA1 has also been found in the
atypical karyotypes of Accipitridae which are characterized by a reduced number of microchromosomes [de Olivieira et al., 2005; Nanda et al., 2006] as well as in the
karyotypes of Psittaciformes and some species of Strigiformes [Nanda et al., 2007; de Olivieira et al., 2008]. However, in all these species/lineages, other GGA macrochromosomes also produce multiple hybridization signals,
implying additional macrochromosome rearrangements.
The karyotype of S. europaea is strikingly different to
other Passeriformes karyotypes. It not only displays a
high number of syntenic regions (13 chromosomes) but
also reveals association of GGA5/10 and GGA8/9 which
must involve fission and fusion of ancestral macrochromosomes. Since such rearrangements are not marked in
the other species of Passeriformes, it can be assumed that
the exceptional chromosome rearrangements in SEU
may have occurred independently after the divergence of
Passeriformes lineages.
GGA4 is disrupted in most but not all analyzed species
of Passeriformes. In blackcap the GGA4 paint uniformly
labeled 1 acrocentric chromosome pair. Although we
cannot rule out that a second hybridization site on another chromosome pair escaped detection under the conditions used, it is more likely that in contrast to other
Passeriformes the ancestral GGA4 remained intact in
Synteny Conservation of Chicken
Chromosomes 1–10 in Avian Lineages
Cytogenet Genome Res 2011;132:165–181
177
GGA Chromosomes
1
2
3
4
5
6
7
8
9
10
Species
Aix sponsa (2n = 80)
(Wood duck)
Pica pica (2n = 76)
(Magpie)
Garrulus glandarius (2n = 78)
(Eurasian jay)
Sylvia atricapilla (2n = 74)
(Blackcap)
Sitta europaea (2n = 80)
(Eurasian nuthatch)
Parus major (2n = 80)
(Great tit)
Periparus ater (2n = 80)
(Coal tit)
Fulica atra (2n = 92)
(Eurasian coot)
Gallinula chloropus (2n = 78)
(Common moorhen)
Fig. 11. Schematic representation outlining the corresponding homologous regions of individual GGA paints
in 9 different avian lineages. Each chicken chromosome is represented by a specific color.
A
B
Fig. 12. Hybridization of GGA3 and GGA1 to interphase nuclei
of G. glandarius (A) and A. sponsa (B) localizes the syntenic GGL
and ASP chromosomes in the nuclear periphery.
blackcap. In fact, conservation of the entire GGA4 has
been observed in some species of Neoaves [Guttenbach et
al., 2003; Kasai et al., 2003]. Apart from GGA1 and GGA4
all other GGA macrochromosomes are conserved as
whole chromosomes (or chromosome arms) in Passeriformes. Comparative cytogenetic studies are consistent
with recent molecular data, showing a high degree of synteny conservation between chicken and several species of
Passeriformes [Backström et al., 2008; Hale et al., 2008;
Jaari et al., 2009]. Although the phylogenetic split of Gal178
Cytogenet Genome Res 2011;132:165–181
liformes and Passeriformes occurred approximately 100
million years ago, only 2 major macrochromosome rearrangements were detected by cross-species painting in 5
out of 6 species analyzed. It must be noted that some additional macrochromosome rearrangements (inversions)
can be inferred by comparing the morphology of some
GGA macrochromosomes with that of the corresponding
homologous chromosomes in other karyotypes, but this
has not disrupted synteny. Compared with the rate of
chromosome rearrangements in mammals (on average 1
change per 10 million years) [O’Brien and Stanyon, 1999],
karyotype evolution, thus, appears to be slow in birds
[Burt et al., 1999]. Consistent with earlier reports [Raikow, 1982; Irestedt et al., 2001], the conservation of macrochromosomal synteny and the synapomorphic split of
GGA1 argue in favor of monophyly of Passeriformes.
In 2 species (coot and common moorhen) of Gruiformes, the 10 GGA macrochromosomes are syntenic to
13 conserved segments, implying a higher number of rearrangements than in Anseriformes as well as in many
Passeriformes. Most notable are associations of GGA4/
GGA5 and GGA6/GGA7. Since both GGA4 and GGA5
delineated multiple syntenic segments in coot and common moorhen, we conclude that fission of the ancestral
GGA chromosomes was followed by fusion events in
Gruiformes. With the notable exception of 1 species of
Nanda/Benisch/Fetting/Haaf/Schmid
Strigiformes [de Oliveira et al., 2008], associations of
GGA4/GGA5 and GGA6/GGA7 are not known in other
lineages. Because most Neoaves lack these associations,
it is plausible to assume that GGA4/GGA5 and GGG6/
GGA7 originated independently in Gruiformes and Strigiformes. In most avian lineages, GGA4 diverged on 2
chromosomes. In Gruiformes, GGA4 is syntenic to 3
chromosomes, indicating additional fission events. The
radiation of Rallidae within Neoaves occurred only 20
million years ago [Ericsson et al., 2006]. This suggests a
higher rate of karyotype diversification among the recently evolved avian species, compared with older lineages such as Galliformes and Passeriformes.
It is interesting to speculate which selective pressure
has conserved macrochromosomal synteny during avian
evolution, including paleognathous and neognathous
birds. The avian macrochromosomes are relatively genepoor compared to the gene-dense microchromosomes. In
chicken cells the microchromosomes are clustered in the
nuclear center whereas macrochromosomes are preferentially located in the nuclear periphery [Habermann et al.,
2001]. In fact, screening of interphase cells in 2 species
demonstrated localization of macrochromosomes (delineated by GGA paints) at the nuclear periphery (fig. 12).
This radial nuclear compartmentalization may be crucial
to avoid exchange between macrochromosomes and microchromosomes [Grandy et al., 2002]. Although evolutionary and radiation-induced chromosome rearrangements occur between different macrochromosomes and
between different microchromosomes, there is little, if
any, evidence for macrochromosome-microchromosome
rearrangements. Macrochromosomal and microchromosomal complements evolve largely independently
from each other. Since in none of the species analyzed
here the microchromosome complement contained detectable segments syntenic to GGA macrochromosomes,
it is plausible to assume a similar nuclear organization as
in chicken cells. This promotes the idea that synteny conservation of macrochromosomes is interrelated with
functional nuclear organization of avian genomes.
The diploid chromosome numbers of the analyzed
species are similar to that of chicken (2n = 78), only coot
has a somewhat higher number (2n = 92). Although in
birds the diploid number can vary dramatically from 42
to 132, the majority of species have 76 to 82 chromosomes. Considering the high degree of macrochromosomal synteny conservation and the lacking evidence for
microchromosome-macrochromosome rearrangements,
these changes in chromosome number must be largely
due to rearrangements within the microchromosome
complement. Although in some atypical avian karyotypes with low diploid chromosome numbers some ancestral microchromosomes were fused to larger chromosomes, in most instances the large ancestral macrochromosomes have been conserved [Nie et al., 2009]. Since the
number of ancestral segments syntenic to GGA macrochromosomes does not vary dramatically among species,
avian karyotype diversification may mainly involve the
gene-dense microchromosomes, which are enriched with
CpG islands. Comparison of orthologous sequences of
GGA11 and GGA28 showed a clear correlation between
CpG-rich DNA segments and evolutionary breakpoint
regions [Gordon et al., 2007]. Studying the nucleotide
substitution rate in orthologous chicken and turkey sequences revealed that microchromosomal genes are under greater evolutionary constraints than macrochromosomal genes [Axelsson et al., 2005].
Synteny Conservation of Chicken
Chromosomes 1–10 in Avian Lineages
Cytogenet Genome Res 2011;132:165–181
Conclusion
GGA chromosome painting in 9 widely different species confirmed the dichotomous nature of avian genomes
and conservation of macrochromosomal synteny. There
has been little or no cross-talk between the macrochromosomal and microchromosomal complements during
avian evolution. Indirect evidence suggests that the genepoor macrochromosomes and the gene-dense microchromosomes are important for a preferred functional
nuclear organization and that the microchromosomal
complement may be more susceptible to evolutionary rearrangements.
Acknowledgement
We thank Prof. Darren K. Griffin (University of Kent, UK) for
providing chicken DNA libraries.
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