Introduction: The Phasianidae family belongs to Galliformes, which is basal to other Neognathae. Despite the availability of chromosome-level genome assemblies for many Phasianidae species, the karyotypes for some species remain poorly investigated. Methods: In this study, we described karyotypes using classical, differential, and molecular cytogenetic (BAC-FISH) methods. To compare chromosome-level genomes of 10 Galliformes species dot-plot analysis was performed. Results: We provide the first comprehensive description of the karyotype of two Tetraonini species: the western capercaillie (Tetrao urogallus, 2n = 78) and the hazel grouse (Tetrastes bonasia, 2n = 80). We mapped chicken BAC clones (CHORI-261) with known coordinates to the chromosomes of the western capercaillie and Japanese quail (Coturnix japonica, 2n = 78) to anchor physical chromosomes to chromosome-level assemblies. Finally, we performed dot-plot comparisons of ten available chromosome-level genome assemblies to identify inter- and intrachromosomal rearrangements in Galliformes. Conclusion: We show that the centromeric fusion of orthologs of GGA6 and GGA8 is shared by all analyzed species in the tetraonid clade: T. urogallus, T. bonasia, and Lagopus muta. We identified linage-specific intrachromosomal rearrangements on chromosomes orthologs to chicken Z (Phasianinae and Tetraoninae), 7 and 12 (Phasianinae and Tetraoninae), 5 and 13 (Perdicinae), 22 (Alectoris). Our study shows that analysis of the genomes of several closely related species allows us to identify chromosomal rearrangements characteristic of individual evolutionary lines.

1.
Delany
ME
,
Krupkin
AB
,
Miller
MM
.
Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening
.
Cytogenet Cell Genet
.
2000
;
90
(
1–2
):
139
45
.
2.
Ellegren
H
.
The evolutionary genomics of birds
.
Annu Rev Ecol Evol Syst
.
2013
;
44
(
1
):
239
59
.
3.
Campagna
L
,
Toews
DP
.
The genomics of adaptation in birds
.
Curr Biol
.
2022
;
32
(
20
):
R1173
86
.
4.
Christidis
L
.
Chordata 3. B. Aves
;
1990
[cited 2024 Dec 28]. Available from: https://www.schweizerbart.de/publications/detail/isbn/9783443260149/L_Christidis_Animal_Cytogenetics_Vol
5.
Griffin
DK
,
Robertson
LBW
,
Tempest
HG
,
Skinner
BM
.
The evolution of the avian genome as revealed by comparative molecular cytogenetics
.
Cytogenet Genome Res
.
2007
;
117
(
1–4
):
64
77
.
6.
Degrandi
TM
,
Barcellos
SA
,
Costa
AL
,
Garnero
AD
,
Hass
I
,
Gunski
RJ
.
Introducing the bird chromosome database: an overview of cytogenetic studies in birds
.
Cytogenet Genome Res
.
2020
;
160
(
4
):
199
205
.
7.
Griffin
DK
,
Robertson
LB
,
Tempest
HG
,
Vignal
A
,
Fillon
V
,
Crooijmans
RPMA
, et al
.
Whole genome comparative studies between chicken and turkey and their implications for avian genome evolution
.
BMC Genomics
.
2008
;
9
:
168
.
8.
Hooper
DM
,
Price
TD
.
Chromosomal inversion differences correlate with range overlap in passerine birds
.
Nat Ecol Evol
.
2017
;
1
(
10
):
1526
34
.
9.
Damas
J
,
Kim
J
,
Farré
M
,
Griffin
DK
,
Larkin
DM
.
Reconstruction of avian ancestral karyotypes reveals differences in the evolutionary history of macro- and microchromosomes
.
Genome Biol
.
2018
;
19
(
1
):
155
.
10.
Damas
J
,
O’Connor
RE
,
Griffin
DK
,
Larkin
DM
.
Avian chromosomal evolution
. In:
Kraus
RHS
, editor.
Avian genomics in ecology and evolution
.
Cham
:
Springer International Publishing
;
2019
. p.
69
92
.
11.
O’Connor
R
,
Kretschmer
R
,
Romanov
MN
,
Griffin
DK
.
A bird’s-eye view of chromosomic evolution in the class aves
.
Cells
.
2024
;
13
(
4
):
310
.
12.
Hooper
DM
,
Griffith
SC
,
Price
TD
.
Sex chromosome inversions enforce reproductive isolation across an avian hybrid zone
.
Mol Ecol
.
2019
;
28
(
6
):
1246
62
.
13.
Knief
U
,
Müller
IA
,
Stryjewski
KF
,
Metzler
D
,
Sorenson
MD
,
Wolf
JB
.
Evolution of chromosomal inversions across an avian radiation
.
Mol Biol Evol
.
2024
;
41
(
6
):
msae092
.
14.
Rutkowska
J
,
Lagisz
M
,
Nakagawa
S
.
The long and the short of avian W chromosomes: no evidence for gradual W shortening
.
Biol Lett
.
2012
;
8
(
4
):
636
8
.
15.
de Oliveira
TD
,
Kretschmer
R
,
Bertocchi
NA
,
Degrandi
TM
,
de Oliveira
EHC
,
Cioffi
MB
, et al
.
Genomic organization of repetitive DNA in woodpeckers (Aves, Piciformes): implications for karyotype and ZW sex chromosome differentiation
.
PLoS One
.
2017
;
12
(
1
):
e0169987
.
16.
Kretschmer
R
,
de Souza
MS
,
Furo
IO
,
Romanov
MN
,
Gunski
RJ
,
Garnero
AV
, et al
.
Interspecies chromosome mapping in Caprimulgiformes, Piciformes, Suliformes, and Trogoniformes (Aves): cytogenomic insight into microchromosome organization and karyotype evolution in birds
.
Cells
.
2021
;
10
(
4
):
826
.
17.
Beklemisheva
VR
,
Tishakova
KV
,
Romanenko
SA
,
Andreushkova
DA
,
Yudkin
VA
,
Interesova
, et al
.
Detailed cytogenetic analysis of three duck species (the northern pintail, mallard, and common goldeneye) and karyotype evolution in the family Anatidae (Anseriformes, Aves)
.
Vavilovskii Zhurnal Genet Selektsii
.
2024
;
28
(
7
):
759
69
.
18.
van Tuinen
M
,
Hedges
SB
.
Calibration of avian molecular clocks
.
Mol Biol Evol
.
2001
;
18
(
2
):
206
13
.
19.
Sun
Z
,
Pan
T
,
Hu
C
,
Sun
L
,
Ding
H
,
Wang
H
, et al
.
Rapid and recent diversification patterns in Anseriformes birds: inferred from molecular phylogeny and diversification analyses
.
PLoS One
.
2017
;
12
(
9
):
e0184529
.
20.
Gill
F
,
Donsker
D
,
Rasmussen
P
.
IOC world bird list (v13. 1)
;
2023
. Available from: https://www.worldbirdnames.org
21.
Shibusawa
M
,
Nishibori
M
,
Nishida-Umehara
C
,
Tsudzuki
M
,
Masabanda
J
,
Griffin
DK
, et al
.
Karyotypic evolution in the Galliformes: an examination of the process of karyotypic evolution by comparison of the molecular cytogenetic findings with the molecular phylogeny
.
Cytogenet Genome Res
.
2004
;
106
(
1
):
111
9
.
22.
Guttenbach
M
,
Nanda
I
,
Feichtinger
W
,
Masabanda
JS
,
Griffin
DK
,
Schmid
M
.
Comparative chromosome painting of chicken autosomal paints 1–9 in nine different bird species
.
Cytogenet Genome Res
.
2003
;
103
(
1–2
):
173
84
.
23.
O’Connor
RE
,
Farré
M
,
Joseph
S
,
Damas
J
,
Kiazim
L
,
Jennings
R
, et al
.
Chromosome-level assembly reveals extensive rearrangement in saker falcon and budgerigar, but not ostrich, genomes
.
Genome Biol
.
2018
;
19
(
1
):
171
.
24.
Shibusawa
M
,
Nishida-Umehara
C
,
Masabanda
J
,
Griffin
DK
,
Isobe
T
,
Matsuda
Y
.
Chromosome rearrangements between chicken and Guinea fowl defined by comparative chromosome painting and FISH mapping of DNA clones
.
Cytogenet Genome Res
.
2002
;
98
(
2–3
):
225
30
.
25.
Shibusawa
M
,
Minai
S
,
Nishida-Umehara
C
,
Suzuki
T
,
Mano
T
,
Yamada
K
, et al
.
A comparative cytogenetic study of chromosome homology between chicken and Japanese quail
.
Cytogenet Cell Genet
.
2001
;
95
(
1–2
):
103
9
.
26.
Shibusawa
M
,
Nishida-Umehara
C
,
Tsudzuki
M
,
Masabanda
J
,
Griffin
DK
,
Matsuda
Y
.
A comparative karyological study of the blue-breasted quail (Coturnix chinensis, Phasianidae) and California quail (Callipepla californica, Odontophoridae)
.
Cytogenet Genome Res
.
2004
;
106
(
1
):
82
90
.
27.
Zimmer
R
,
King
WA
,
Verrinder Gibbins
AM
.
Generation of chicken Z-chromosome painting probes by microdissection for screening large-insert genomic libraries
.
Cytogenet Cell Genet
.
1997
;
78
(
2
):
124
30
.
28.
Coullin
P
,
Bed’Hom
B
,
Candelier
JJ
,
Vettese
D
,
Maucolin
S
,
Moulin
S
, et al
.
Cytogenetic repartition of chicken CR1 sequences evidenced by PRINS in Galliformes and some other birds
.
Chromosome Res
.
2005
;
13
(
7
):
665
73
.
29.
Damas
J
,
O’Connor
R
,
Farré
M
,
Lenis
VPE
,
Martell
HJ
,
Mandawala
A
, et al
.
Upgrading short-read animal genome assemblies to chromosome level using comparative genomics and a universal probe set
.
Genome Res
.
2017
;
27
(
5
):
875
84
.
30.
Kasai
F
,
Garcia
C
,
Arruga
MV
,
Ferguson-Smith
MA
.
Chromosome homology between chicken (Gallus gallus domesticus) and the red-legged partridge (Alectoris rufa); evidence of the occurrence of a neocentromere during evolution
.
Cytogenet Genome Res
.
2003
;
102
(
1–4
):
326
30
.
31.
Kretschmer
R
,
Ferguson-Smith
MA
,
De Oliveira
EHC
.
Karyotype evolution in birds: from conventional staining to chromosome painting
.
Genes
.
2018
;
9
(
4
):
181
.
32.
Sasazaki
S
,
Hinenoya
T
,
Lin
B
,
Fujiwara
A
,
Mannen
H
.
A comparative map of macrochromosomes between chicken and Japanese quail based on orthologous genes
.
Anim Genet
.
2006
;
37
(
4
):
316
20
.
33.
Aslam
ML
,
Bastiaansen
JW
,
Crooijmans
RP
,
Vereijken
A
,
Megens
H-J
,
Groenen
MA
.
A SNP based linkage map of the turkey genome reveals multiple intrachromosomal rearrangements between the turkey and chicken genomes
.
BMC Genomics
.
2010
;
11
(
1
):
647
.
34.
Genome
.
NCBI
[cited 2024 Dec 28]. Available from: https://www.ncbi.nlm.nih.gov/datasets/genome/?taxon=8976
35.
International Chicken Genome Sequencing Consortium
.
Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution
.
Nature
.
2004
;
432
(
7018
):
695
716
.
36.
Dalloul
RA
,
Long
JA
,
Zimin
AV
,
Aslam
L
,
Beal
K
,
Blomberg
LA
, et al
.
Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis
.
PLoS Biol
.
2010
;
8
(
9
):
e1000475
.
37.
Wang
N
,
Hosner
PA
,
Liang
B
,
Braun
EL
,
Kimball
RT
.
Historical relationships of three enigmatic phasianid genera (Aves: Galliformes) inferred using phylogenomic and mitogenomic data
.
Mol Phylogenet Evol
.
2017
;
109
:
217
25
.
38.
Rhie
A
,
McCarthy
SA
,
Fedrigo
O
,
Damas
J
,
Formenti
G
,
Koren
S
, et al
.
Towards complete and error-free genome assemblies of all vertebrate species
.
Nature
.
2021
;
592
(
7856
):
737
46
.
39.
Ball
A
,
Robertson
C
,
Doubleday
M
;
Wellcome Sanger Institute Tree of Life Management, Samples and Laboratory team
;
Wellcome Sanger Institute Scientific Operations: Sequencing Operations
;
Wellcome Sanger Institute Tree of Life Core Informatics team
, et al
.
The genome sequence of the Western Capercaillie Tetrao urogallus Linnaeus, 1758
.
Wellcome Open Res
.
2024
;
9
:
198
.
40.
Morris
KM
,
Hindle
MM
,
Boitard
S
,
Burt
DW
,
Danner
AF
,
Eory
L
, et al
.
The quail genome: insights into social behaviour, seasonal biology and infectious disease response
.
BMC Biol
.
2020
;
18
(
1
):
14
.
41.
Kiazim
LG
,
O’Connor
RE
,
Larkin
DM
,
Romanov
MN
,
Narushin
VG
,
Brazhnik
EA
, et al
.
Comparative mapping of the macrochromosomes of eight avian species provides further insight into their phylogenetic relationships and avian karyotype evolution
.
Cells
.
2021
;
10
(
2
):
362
.
42.
Barros
CP
,
Derks
MF
,
Mohr
J
,
Wood
BJ
,
Crooijmans
RP
,
Megens
H-J
, et al
.
A new haplotype-resolved turkey genome to enable turkey genetics and genomics research
.
GigaScience
.
2022
;
12
:
giad051
.
43.
Zhang
Y
,
Zhang
X
,
O’Hare
TH
,
Payne
WS
,
Dong
JJ
,
Scheuring
CF
, et al
.
A comparative physical map reveals the pattern of chromosomal evolution between the turkey (Meleagris gallopavo) and chicken (Gallus gallus) genomes
.
BMC Genomics
.
2011
;
12
(
1
):
447
.
44.
McPherson
MC
,
Robinson
CM
,
Gehlen
LP
,
Delany
ME
.
Comparative cytogenomics of poultry: mapping of single gene and repeat loci in the Japanese quail (Coturnix japonica)
.
Chromosome Res
.
2014
;
22
(
1
):
71
83
.
45.
Degrandi
TM
,
Gunski
RJ
,
Garnero
AV
,
Oliveira
EHC
,
Kretschmer
R
,
Souza
MS
, et al
.
The distribution of 45S rDNA sites in bird chromosomes suggests multiple evolutionary histories
.
Genet Mol Biol
.
2020
;
43
(
2
):
e20180331
.
46.
Rutkowski
R
,
Jagołkowska
P
,
Zawadzka
D
,
Bogdanowicz
W
.
Impacts of forest fragmentation and post-glacial colonization on the distribution of genetic diversity in the Polish population of the hazel grouse Terastes bonasia
.
Eur J Wildl Res
.
2016
;
62
(
3
):
293
306
.
47.
Wilkinson
NI
,
Doubleday
M
,
Douse
A
,
Ford
A
,
Kelly
LA
,
Kortland
K
, et al
.
Further declines of the Western Capercaillie Tetrao urogallus in Scotland as shown by the 2021–2022 winter survey
.
Bird Study
.
2024
;
71
(
1
):
17
31
.
48.
Yamashina
Y
.
Studies on the chromosomes of three gallinaceous birds
;
1952
[cited 2024 Dec 28]. Available from: https://www.cabidigitallibrary.org/doi/full/10.5555/19560100852
49.
Romanenko
SA
,
Biltueva
LS
,
Serdyukova
NA
,
Kulemzina
AI
,
Beklemisheva
VR
,
Gladkikh
OL
, et al
.
Segmental paleotetraploidy revealed in sterlet (Acipenser ruthenus) genome by chromosome painting
.
Mol Cytogenet
.
2015
;
8
(
1
):
90
.
50.
Kulak
M
,
Komissarov
A
,
Fillon
V
,
Tsukanova
K
,
Saifitdinova
A
,
Galkina
S
.
Genome organization of major tandem repeats and their specificity for heterochromatin of macro- and microchromosomes in Japanese quail
.
Genome
.
2022
;
65
(
7
):
391
403
.
51.
Yang
F
,
Graphodatsky
AS
.
Animal probes and ZOO-FISH
. In:
Liehr
T
, editor.
Fluorescence In Situ Hybridization (FISH): application guide. Springer protocols handbooks
.
Berlin, Heidelberg
:
Springer
;
2009
. p.
323
46
.
52.
Seabright
M
.
A rapid banding technique for human chromosomes
.
Lancet
.
1971
;
2
(
7731
):
971
2
.
53.
Sumner
AT
.
A simple technique for demonstrating centromeric heterochromatin
.
Exp Cell Res
.
1972
;
75
(
1
):
304
6
.
54.
O’Connor
RE
,
Romanov
MN
,
Kiazim
LG
,
Barrett
PM
,
Farré
M
,
Damas
J
, et al
.
Reconstruction of the diapsid ancestral genome permits chromosome evolution tracing in avian and non-avian dinosaurs
.
Nat Commun
.
2018
;
9
(
1
):
1883
.
55.
Ijdo
JW
,
Wells
RA
,
Baldini
A
,
Reeders
ST
.
Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR
.
Nucleic Acids Res
.
1991
;
19
(
17
):
4780
.
56.
Maden
BEH
,
Dent
CL
,
Farrell
TE
,
Garde
J
,
McCallum
FS
,
Wakeman
JA
.
Clones of human ribosomal DNA containing the complete 18 S-rRNA and 28 S-rRNA genes. Characterization, a detailed map of the human ribosomal transcription unit and diversity among clones
.
Biochem J
.
1987
;
246
(
2
):
519
27
.
57.
Graphodatsky
AS
,
Yang
F
,
O’Brien
PCM
,
Serdukova
N
,
Milne
BS
,
Trifonov
V
, et al
.
A comparative chromosome map of the Arctic fox, red fox and dog defined by chromosome painting and high resolution G-banding
.
Chromosome Res
.
2000
;
8
(
3
):
253
63
.
58.
Liehr
T
,
Kreskowski
K
,
Ziegler
M
,
Piaszinski
K
,
Rittscher
K
.
The standard FISH procedure
. In:
Liehr
T
, editor.
Fluorescence In Situ Hybridization (FISH)
.
Berlin, Heidelberg
:
Springer Berlin Heidelberg
;
2017
. p.
109
18
.
59.
Cabanettes
F
,
Klopp
C
.
D-GENIES: dot plot large genomes in an interactive, efficient and simple way
.
PeerJ
.
2018
;
6
:
e4958
.
60.
Geneious|bioinformatics software for sequence data analysis
.
Geneious
[cited 2024 Dec 28]. Available from: https://www.geneious.com/
61.
Kayang
BB
,
Fillon
V
,
Inoue-Murayama
M
,
Miwa
M
,
Leroux
S
,
Fève
K
, et al
.
Integrated maps in quail (Coturnix japonica) confirm the high degree of synteny conservation with chicken (Gallus gallus) despite 35 million years of divergence
.
BMC Genomics
.
2006
;
7
(
1
):
101
.
62.
Chen
D
,
Hosner
PA
,
Dittmann
DL
,
O’Neill
JP
,
Birks
SM
,
Braun
EL
, et al
.
Divergence time estimation of Galliformes based on the best gene shopping scheme of ultraconserved elements
.
BMC Ecol Evo
.
2021
;
21
(
1
):
209
.
63.
Stock
AD
,
Bunch
TD
.
The evolutionary implications of chromosome banding pattern homologies in the bird order Galliformes
.
Cytogenet Cell Genet
.
1982
;
34
(
1–2
):
136
48
.
64.
Larkin
DM
,
Pape
G
,
Donthu
R
,
Auvil
L
,
Welge
M
,
Lewin
HA
.
Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories
.
Genome Res
.
2009
;
19
(
5
):
770
7
.
65.
Bian
X
,
Cai
H
,
Ning
S
,
Li
Q
,
Zhang
H
,
Xong
X
, et al
.
Studies on the karyotypes of birds: XII. 15 species of nonpasserines (Aves)
.
Zool Res
.
1991
;
12
(
4
):
407
12
.
66.
Romanov
MN
,
Farré
M
,
Lithgow
PE
,
Fowler
KE
,
Skinner
BM
,
O’Connor
R
, et al
.
Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor
.
BMC Genomics
.
2014
;
15
(
1
):
1060
.
67.
Zlotina
A
,
Galkina
S
,
Krasikova
A
,
Crooijmans
RPMA
,
Groenen
MAM
,
Gaginskaya
E
, et al
.
Centromere positions in chicken and Japanese quail chromosomes: de novo centromere formation versus pericentric inversions
.
Chromosome Res
.
2012
;
20
(
8
):
1017
32
.
68.
Nanda
I
,
Schrama
D
,
Feichtinger
W
,
Haaf
T
,
Schartl
M
,
Schmid
M
.
Distribution of telomeric (TTAGGG)n sequences in avian chromosomes
.
Chromosoma
.
2002
;
111
(
4
):
215
27
.
69.
Delany
ME
,
Gessaro
TM
,
Rodrigue
KL
,
Daniels
LM
.
Chromosomal mapping of chicken mega-telomere arrays to GGA9, 16, 28 and W using a cytogenomic approach
.
Cytogenet Genome Res
.
2007
;
117
(
1–4
):
54
63
.
70.
Rodrigues
BS
,
de Assis
MDFL
,
O’Brien
PC
,
Ferguson-Smith
MA
,
de Oliveira
EH
.
Chromosomal studies on Coscoroba coscoroba (Aves: Anseriformes) reinforce the Coscoroba–Cereopsis clade
.
Biol J Linn Soc Lond
.
2014
;
111
(
2
):
274
9
.
71.
O’Hare
TH
,
Delany
ME
.
Genetic variation exists for telomeric array organization within and among the genomes of normal, immortalized, and transformed chicken systems
.
Chromosome Res
.
2009
;
17
(
8
):
947
64
.
72.
Swanberg
SE
,
O’Hare
TH
,
Robb
EA
,
Robinson
CM
,
Chang
H
,
Delany
ME
.
Telomere biology of the chicken: a model for aging research
.
Exp Gerontol
.
2010
;
45
(
9
):
647
54
.
73.
Nishida-Umehara
C
,
Tsuda
Y
,
Ishijima
J
,
Ando
J
,
Fujiwara
A
,
Matsuda
Y
, et al
.
The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds
.
Chromosome Res
.
2007
;
15
(
6
):
721
34
.
74.
Delany
ME
,
Robinson
CM
,
Goto
RM
,
Miller
MM
.
Architecture and organization of chicken microchromosome 16: order of the NOR, MHC-Y, and MHC-B subregions
.
J Hered
.
2009
;
100
(
5
):
507
14
.
75.
Chaves
LD
,
Krueth
SB
,
Reed
KM
.
Characterization of the turkey MHC chromosome through genetic and physical mapping
.
Cytogenet Genome Res
.
2007
;
117
(
1–4
):
213
20
.
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