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. 2008 Jul;179(3):1479–1495. doi: 10.1534/genetics.108.088195

A Gene-Based Genetic Linkage Map of the Collared Flycatcher (Ficedula albicollis) Reveals Extensive Synteny and Gene-Order Conservation During 100 Million Years of Avian Evolution

Niclas Backström *, Nikoletta Karaiskou †,1, Erica H Leder , Lars Gustafsson , Craig R Primmer , Anna Qvarnström , Hans Ellegren *,2
PMCID: PMC2475748  PMID: 18562642

Abstract

By taking advantage of a recently developed reference marker set for avian genome analysis we have constructed a gene-based genetic map of the collared flycatcher, an important “ecological model” for studies of life-history evolution, sexual selection, speciation, and quantitative genetics. A pedigree of 322 birds from a natural population was genotyped for 384 single nucleotide polymorphisms (SNPs) from 170 protein-coding genes and 71 microsatellites. Altogether, 147 gene markers and 64 microsatellites form 33 linkage groups with a total genetic distance of 1787 cM. Male recombination rates are, on average, 22% higher than female rates (total distance 1982 vs. 1627 cM). The ability to anchor the collared flycatcher map with the chicken genome via the gene-based SNPs revealed an extraordinary degree of both synteny and gene-order conservation during avian evolution. The great majority of chicken chromosomes correspond to a single linkage group in collared flycatchers, with only a few cases of inter- and intrachromosomal rearrangements. The rate of chromosomal diversification, fissions/fusions, and inversions combined is thus considerably lower in birds (0.05/MY) than in mammals (0.6–2.0/MY). A dearth of repeat elements, known to promote chromosomal breakage, in avian genomes may contribute to their stability. The degree of genome stability is likely to have important consequences for general evolutionary patterns and may explain, for example, the comparatively slow rate by which genetic incompatibility among lineages of birds evolves.


GENOMICS is in a phase where new technology allows genome characterization beyond that of traditional model organisms and species of medical or agricultural interest. For example, genomic analyses of nonmodel species holds great promise for dissecting the genetic background to fitness traits in natural populations, to adaptive population divergence, to speciation, and to other key aspects of evolutionary biology (Ellegren and Sheldon 2008). Genomic characterization of new and phylogenetically divergent lineages has the additional benefit that it provides the necessary comparative perspective for addressing the evolution of genome organization. Specifically, with genetic maps or genome sequence information available across taxa, the broad-scale pattern of genome and chromosomal evolution can be investigated. This, in turn, opens the possibility of investigating to what extent evolution at the chromosomal level sets the stage for the evolutionary processes, which occur on the level of the phenotype.

Reshuffling of chromosomal segments, through translocations and inversions, is an integral part of genome evolution. However, it is clear that the rate of rearrangement differs radically among lineages as well as on a temporal scale (Kohn et al. 2006; Ferguson-Smith and Trifonov 2007). From comparative mapping of chicken and different mammals it was suggested that the rate of chromosomal rearrangement in the avian lineage is very low (Burt et al. 1999). This has subsequently been confirmed through analyses of vertebrate genome sequence data, including chicken (Bourque et al. 2005), the only bird that has had its genome sequenced to date (International Chicken Genome Sequencing Consortium 2004). Moreover, evidence for an unusually stable avian karyotype with few interchromosomal rearrangements has been obtained by cross-species chromosome painting or the use of other types of in situ hybridization probes (Shetty et al. 1999; Shibusawa et al. 2001, 2004a,b; Raudsepp et al. 2002; Guttenbach et al. 2003; Kasai et al. 2003; Derjusheva et al. 2004; Schmid et al. 2005; Itoh et al. 2006; Fillon et al. 2007; Griffin et al. 2007; Nishida-Umehara et al. 2007). However, these experiments rarely have the resolution for detecting intrachromosomal or small-scale interchromosomal rearrangements.

Genetic maps are available for turkey (Reed et al. 2005) and quail (Kayang et al. 2006), two agricultural species that are closely related to chicken as members of the order Galliformes. However, a lack of genetic markers, in particular those informative for comparative mapping, has been a major obstacle to linkage analyses of bird species belonging to other orders. As a consequence, linkage mapping in natural bird populations is still in its infancy. Hansson et al. (2005) developed a partial microsatellite-based linkage map (58 markers) in the great reed warbler (Acrocephalus arundinaceus), a species from the order Passeriformes, the largest and ecologically most well-studied group of birds. This study also made the unexpected observation that the recombination rate was twice as high in females as in males, which is in contrast to the prevailing trend of recombination usually being lower in the heterogametic sex (in birds, males are ZZ and females ZW). Backström et al. (2006) reported on a gene-based linkage map of the Z chromosome of another passerine species, the collared flycatcher (Ficedula albicollis). The Z chromosome was found to be completely syntenic between collared flycatcher and chicken. Subsequently, Dawson et al. (2007) developed an extended great reed warbler map and found a high degree of chromosomal conservation when compared to chicken (see also Åkesson et al. 2007).

We have recently adopted the comparative anchor-tagged sequences approach (Lyons et al. 1997) to develop a genomewide, gene-based marker resource for avian comparative mapping (Backström et al. 2008). This set of 200+ markers target conserved exonic sequences in genes spread over all chromosomes currently covered in the chicken genome assembly, with a mean marker interval of 4 Mb. The uniform distribution of these markers across the chicken genome means that, if they are used for comparative mapping in other birds, the degree of synteny and gene-order conservation across a significant part of the avian genome can be revealed. Here we present a genetic linkage map of the collared flycatcher based on the new marker set. This species has long been in focus for studies of sexual selection, life-history evolution, and speciation (Gustafsson and Sutherland 1988; Gustafsson and Pärt 1990; Gustafsson et al. 1995; Ellegren et al. 1996; Qvarnström et al. 2000, 2006; Veen et al. 2001; Saether et al. 2007) and hence is a well-established “ecological model organism.” Importantly, songbirds (passeriforms) and galliforms diverged at the time of the major radiation of avian lineages ≈100 million years (MY) ago (Van Tuinen et al. 2000). With genetic map data for the collared flycatcher we can thus address genome evolution at the level of gene order across two highly divergent lineages of the avian phylogenetic tree.

MATERIALS AND METHODS

Species samples and DNA extraction:

Blood samples were collected from collared flycatcher (F. albicollis) families breeding on the Baltic islands Öland and Gotland and DNA was extracted by a standard proteinase K digestion/phenol–chlorophorm purification protocol. The mapping pedigree consisted of 24 half-sib families with a few interconnections and 11 F2's, in total 322 birds (supplemental Table 1) after excluding all recognized extra-pair offspring (see below).

Marker genotyping:

In a previous resequencing effort, we surveyed 200 collared flycatcher genes for intronic diversity among 10 unrelated individuals from the same population as the mapping pedigree, which uncovered 904 segregating sites (Backström et al. 2008). From this, 341 single nucleotide polymorphisms (SNPs) with a minor allele frequency of >0.1 and representing the majority of all genes screened were selected for genotyping in the pedigree; for many genes, more than one SNP from the same intron were included. An additional 43 SNPs were obtained from 21 different genes previously screened for variability in collared flycatchers (Borge et al. 2005) (Table 1). The total of 384 SNPs were genotyped using the Golden Gate Assay (Fan et al. 2003) from Illumina (San Diego) at the SNP Technology Platform, Uppsala University (http://www.medsci.uu.se/molmed/snpgenotyping/index.htm). The overall genotype call rate was 95.7% and the reproducibility was 100% according to duplicate analysis of 5.4% (7218/132,848) of the genotypes. The quality of the genotype data was further assessed by testing for Hardy–Weinberg equilibrium (HWE) using the chi-square distribution for each assay. All SNPs conformed to HWE.

TABLE 1.

Markers included in the collared flycatcher linkage map

Marker Linkage group Gene descriptiona Ensembl IDb Chicken chromosome Chicken genome start position (bp)
Gene-based SNPs
00548 Unlinked Hypothetical protein 00548 22 1,221,445
02079 Unlinked Hypothetical protein 02079 10 1,854,152
02419 Fal9 No longer in the Ensembl database, not mapped to new identifiers
04550 Fal27 No longer in the Ensembl database, not mapped to new identifiers
05087 Fal13 Hypothetical protein 05087 19 5,590,343
07726 Fal16 Hypothetical protein 07726 11 10,700,742
08235 Fal6 Hypothetical protein 08235 Un 42,824,332
08544 Fal10 No description 08544 6 17,299,861
12630 Fal28 Magmas-like protein 12630 14 13,386,833
15691 Fal6 Uncharacterized protein C15orf24 precursor 15691 5 32,353,219
15738 Fal5 Similar to CG1218-PA 15738 4 26,412,511
17140 Fal5 No longer in the Ensembl database, not mapped to new identifiers
18798 Fal6 Kinesin light chain 18798 5 52,944,389
20352 Fal1 No description 20352 2 56,437,562
20904 Fal1 Hypothetical protein 20904 2 67,141,279
21277 Fal1 No description 21277 2 80,448,704
22644 Fal2 No description 22644 3 58,129,917
25613 Fal8 Hypothetical protein 25613 1 108,461,452
25924 Unlinked Hypothetical protein 25924 4 93,260,081
27425 Fal4 Hypothetical protein 27425 1 171,909,504
27623 Fal4 No longer in the Ensembl database, not mapped to new identifiers
ABHD10 Fal8 Abhydrolase domain-containing mitochondrial precursor 24813 1 91,842,859
ACADL Fal7 Acyl-coenzyme A dehydrogenase, long chain 04557 7 2,734,809
ACADSB Fal10 Acyl-coenzyme A dehydrogenase, short/branched chain 15724 6 33,024,247
ACHA9 Fal5 Neuronal acetylcholine receptor subunit α-9 precursor 23080 4 70,872,474
ACLYc Fal1 ATP citrate lyase 05502 27 4,344,212
ACOT8 Fal15 Acyl-coenzyme A thioesterase 8 11074 20 10,473,488
ACTBc Fal32 Actin, cytoplasmic type 5 39969 10 1,891,946
ADAL Fal23 Adenosine deaminase-like 06419 10 7,196,900
ADH5 Fal5 Alcohol dehydrogenase 5 (class III), χ polypeptide 19994 4 61,539,229
ADIPOR1 Fal27 Adiponectin receptor 1 00132 26 1,090,425
ALAS1c Fal21 5-Aminolevulinate synthase, nonspecific, mitochondrial precursor 06295 12 2,762,886
AN32B Fal26 Acidic leucine-rich nuclear phosphoprotein 32 family member B 02401 28 1,324,041
ANAPC5 Fal9 Anaphase-promoting complex subunit 5 06640 15 5,498,421
ANKRD49 Fal4 Ankyrin repeat domain-containing protein 49 27818 1 189,909,241
ARF1 Unlinked ADP-ribosylation factor 1 08661 2 2,259,733
ARHGEF9 Unlinked Rho guanine nucleotide exchange factor 9 12303 4 11,866,519
ARHL2 Unlinked Poly(ADP-ribose) glycohydrolase ARH3 03624 23 4,457,042
ARP6 Fal3 Actin-related protein 6 18851 1 49,106,063
ASB6 Fal25 Ankyrin repeat and SOCS box-containing 6 06983 17 6,201,193
ATG4B Fal14 Cysteine protease ATG4B 10179 9 5,828,498
ATP6AP2 Fal4 ATPase, H+ transporting, lysosomal accessory protein 2 26187 1 115,861,428
ATP6V1E1 Unlinked Vacuolar H+ ATPase E1 21281 1 63,935,883
BZW1 Fal7 Basic leucine zipper and W2 domain-containing protein 1 13380 7 12,346,390
C12orf29 Fal3 Hypothetical protein 18208 1 44,668,513
C7orf27 Fal32 HEAT repeat domain-containing protein C7orf27 precursor 06938 14 3,350,565
C8orf53 Fal1 Uncharacterized protein C8orf53 25969 2 140,964,418
CACYBP Fal19 Calcyclin-binding protein 07248 8 7,413,974
CATB Fal2 Cathepsin B precursor 26896 3 110,173,920
CBPZ Fal5 Carboxypeptidase Z precursor 25149 4 84,149,787
CCDC104 Unlinked Coiled-coil domain-containing protein 104 13093 3 129,733
CCDC132 Fal1 Coiled-coil domain containing 132 15463 2 22,899,725
CCDC137 Unlinked MGC16597 protein 07177 18 9,164,974
CCNG1 Fal12 Cyclin-G1 02636 13 6,483,608
CCT2 Fal3 Chaperonin-containing TCP1, subunit 2 16215 1 37,378,125
CDH9 Fal1 Cadherin-9 precursor 21079 2 72,557,369
CEPU1c Fal24 Protein CEPU-1 precursor 29072 24 1,827,157
CGI-62 Fal1 UPF0418 protein C8orf70 25374 2 125,087,485
CHCc Fal13 Clathrin heavy chain 39267 19 7,239,507
CHD1L Fal8 Chromodomain helicase DNA-binding protein 1-like 24254 1 83,862,026
CHM1B Fal18 Charged multivesicular body protein 1b 06500 4 1,509,856
CHMP5 Fal1 Charged multivesicular body protein 5 21491 2 87,941,041
CNTN1 Fal3 Contactin-1 precursor 15506 1 30,637,524
COEA1 Fal1 Collagen α-1(XIV) chain precursor 26472 2 142,375,665
CRIPT Fal2 Postsynaptic protein CRIPT 16264 3 27,956,254
CT030 Unlinked UPF0414 transmembrane protein C20orf30 00227 22 346,000
DC1L1 Fal1 Cytoplasmic dynein 1 light intermediate chain 1 18728 2 40,471,155
DDAH1 Fal11 Dimethylarginine dimethylaminohydrolase 1 14108 8 16,977,584
DECR1 Fal1 2,4-dienoyl-CoA reductase, mitochondrial precursor 25647 2 129,135,915
DLD Fal3 Dihydrolipoamide dehydrogenase 12884 1 15,844,353
DPYSL3 Unlinked Dihydropyrimidinase-like 3 12260 13 18,592,762
DST Fal2 Bullous pemphigoid antigen 1 26267 3 89,753,995
EDF1 Unlinked Endothelial differentiation-related factor 1 homolog 14657 17 932,044
EF1A1 Fal2 Elongation factor 1-α 1 25653 3 84,252,820
EF1A Fal15 Elongation factor 1-α 09385 20 8,992,662
EIF3S1 Unlinked Eukaryotic translation initiation factor 3, subunit 1-α 13336 10 21,935,894
ENO1c Fal20 α-Enolase 03745 21 3,197,152
ETNK1 Fal3 Ethanolamine kinase 1 21571 1 68,619,958
FAK1 Fal1 Focal adhesion kinase 1 26060 2 151,344,071
FNc Fal7 Fibronectin 05663 7 4,362,118
FTHc Fal6 Ferritin H-subunit 11687 5 8,042,629
GAS7 Unlinked Growth-arrest-specific protein 7 00500 18 181,941
GH1c Fal8 Growth hormone factor 1 24989 1 96,197,113
GNB1 Fal20 Guanine nucleotide-binding protein (G protein) β polypeptide 1 02040 21 1,907,993
GTF2B Fal11 Transcription initiation factor IIB 10015 8 15,855,345
HARS Fal12 Histidyl-tRNA synthetase 01152 13 825,160
HEPACAM Fal24 Hepatocyte cell adhesion molecule 00574 24 244,611
HMGB2 Fal5 High-mobility group protein B2 17483 4 44,739,576
HMGN2 Fal29 Nonhistone chromosomal protein HMG-17 00504 23 132,497
IGF2R Fal2 Insulin-like growth factor 2 receptor 18986 3 47,356,791
IGFBP7 Fal5 Insulin-like growth factor-binding protein 7 precursor 18503 4 50,637,829
KCNIP4 Unlinked Kv channel-interacting protein 4 23272 4 77,264,411
KCRBc Fal6 Creatine kinase B-type 18765 5 52,833,368
KIAA1706 Fal1 CDNA FLJ14480 fis, clone MAMMA1002215 19789 2 46,847,660
LARP1 Fal12 La-related protein 1 06374 13 12,129,582
LDHA Fal6 L-lactate dehydrogenase A chain 10181 5 13,644,404
LHCGRc Fal22 Luteinizing hormone/choriogonadotropin receptor 14806 3 7,517,756
MAGOH Fal11 Mago-nashi homolog, proliferation-associated 17388 8 25,398,748
MBP Fal1 Myelin basic protein 22187 2 92,901,749
METRNL Unlinked Meteorin-like protein precursor 02154 18 3,058,036
MIC1 Fal1 Colon cancer-associated protein Mic1 24206 2 106,186,277
MITD1 Fal4 MIT domain-containing protein 1 27060 1 136,635,855
MMAA Fal5 Methylmalonic aciduria type A protein, mitochondrial precursor 16214 4 32,303,140
MOSPD2 Fal4 Motile sperm domain-containing protein 2 26743 1 125,737,284
MPP1c Fal18 Myelin proteolipid protein NA NA NA
MPP6 Fal1 MAGUK p55 subfamily member 6 17898 2 31,506,073
MRPS18A Fal2 28S ribosomal protein S18a, mitochondrial precursor 16751 3 32,021,644
NAT5 Fal33 N-acetyltransferase 5 20554 7 38,349,143
NDST3 Fal12 Bifunctional heparan sulfate N-deacetylase/N-sulfotransferase 3 19599 4 56,617,452
NDUFA7 Fal33 NADH dehydrogenase 1 α subcomplex subunit 7 00895 28 871,010
NSMAF Fal1 Protein FAN (factor associated with N-SMase activation) 24908 2 115,869,042
NY-SAR-48 Fal26 Sarcoma antigen NY-SAR-48 isoform a 05915 28 3,757,065
OAZ Fal26 Ornithine decarboxylase antizyme 01183 28 1,446,253
ODC11c Fal2 Ornithine decarboxylase 26527 3 99,660,031
PARK7 Fal20 Protein DJ-1 Parkinson disease protein 7 homolog 00742 21 235,467
PDCD11 Fal10 RRP5 protein homolog programmed cell death protein 11 13446 6 25,047,124
PDHL1 Fal4 Phosphoglycerate dehydrogenase-like 1 27270 1 148,754,342
PES1 Fal9 Pescadillo homolog 1 12619 15 11,118,356
PKHB2 Fal14 Pleckstrin homology domain-containing family B member 2 03399 9 3,184,527
PNN Fal6 Pinin 16532 5 40,003,168
POLR2C Fal16 DNA-directed RNA polymerase II subunit RPB3 01768 11 552,555
POLR2H Fal14 DNA-directed RNA polymerases I, II, and III subunit RPABC3 13907 9 17,035,879
PPIL4 Fal2 Peptidyl-prolyl cis-trans isomerase-like 4 20195 3 50,008,973
PRS4 Fal6 26S protease regulatory subunit 4 17367 5 46,255,522
PSMB1 Fal2 Proteasome (prosome, macropain) subunit, β-type, 1 18217 3 42,604,002
PSMC2 Fal3 Proteasome (prosome, macropain) 26S subunit, ATPase, 2 13403 1 13,964,547
PSMC3 Fal6 Proteasome 26S ATPase subunit 3 13163 5 25,021,822
PSMC5 Fal17 26S protease regulatory subunit 8 00469 27 1,607,679
PSMD14 Fal7 Proteasome (prosome, macropain) 26S subunit, non-ATPase, 14 18142 7 22,963,970
PSMD6 Fal21 26S proteasome non-ATPase regulatory subunit 6 11836 12 13,910,990
PTMS Fal8 Parathymosin 23363 1 80,288,088
RAB12 Fal1 Gallus gallus similar to Rab12 protein 22528 2 101,592,940
RAB3GAP1 Fal7 Rab3 GTPase-activating protein catalytic subunit 19948 7 32,114,339
RABL4 Fal3 Putative GTP-binding protein RAY-like 20454 1 53,623,713
RASGEF1A Fal10 RasGEF domain family, member 1A 03978 6 5,681,912
RBBP7 Fal4 Histone-binding protein RBBP7 26698 1 124,845,745
RBM18 Unlinked Probable RNA-binding protein 18 02045 17 9,445,180
RBM26 Fal4 RNA-binding protein 26 27331 1 157,186,094
RHOc Fal31 Rhodopsin (opsin-2) 33236 12 20,163,795
RL13 Fal30 60S ribosomal protein L13 09974 11 20,692,991
RNASEH1 Fal2 Ribonuclease H1 26438 3 96,571,133
ROBO1 Fal9 Roundabout1 protein 25008 1 99,689,366
RPL5c Fal11 60S ribosomal protein L5 09525 8 14,745,903
RPL7Ac Fal25 60S ribosomal protein L7a 21881 17 7,532,190
RPL11 Fal29 Ribosomal protein L11 06305 23 5,837,007
RPL23 Fal17 60S ribosomal protein L23 02496 27 3,957,106
RPL30c Fal1 60S ribosomal protein L30 36621 2 132,392,442
RPL37Ac Fal7 60S ribosomal protein L37a 18702 7 24,873,612
SBDS Fal13 Shwachman–Bodian–Diamond syndrome 01658 19 782,450
SERINC1 Fal2 Tumor differentially expressed 2 23989 3 63,939,040
SPCS1 Fal21 Signal peptidase complex subunit 1 02526 12 749,082
STYX Unlinked Serine/threonine/tyrosine-interacting protein 20280 5 60,813,050
TGFB2c Fal2 Transforming growth factor β-2 precursor 15664 3 20,477,096
THUMPD3 Fal31 THUMP domain-containing protein 3 13674 12 20,067,036
TIMM17A Fal27 Translocase of inner mitochondrial membrane 17 homolog A 00123 26 1,096,567
TMc Fal23 Tropomyosin α-1 chain 05572 10 5,107,950
TMEM32 Fal18 Transmembrane protein 32 precursor 09949 4 4,186,140
TUBGCP3 Fal4 Gamma-tubulin complex component 3 27189 1 142,174,289
TXNDC14 Unlinked Thioredoxin domain containing 14 11887 5 18,159,850
UBE2J1 Fal2 Ubiquitin-conjugating enzyme E2, J1 25442 3 78,396,237
UCHL3 Fal4 Ubiquitin carboxyl-terminal esterase L3 27356 1 159,089,890
UCHL5 Fal11 Ubiquitin carboxyl-terminal hydrolase L5 03977 8 3,533,310
UQCRC1 Fal21 Ubiquinol-cytochrome-c reductase complex core protein 1 09300 12 9,301,215
VIPR2 Fal1 Vasoactive intestinal peptide receptor 2 10623 2 9,569,988
VISL1 Unlinked Visinin-like protein 1 26565 3 102,957,139
VPS26A Unlinked Vacuolar protein sorting-associated protein 26A 06635 6 11,919,165
WDR24 Fal28 WD repeat protein 24 03862 14 13,908,481
YME1L1 Fal1 YME1-like 1 12112 2 15,827,680
YPEL5 Unlinked Yippee-like 5 14726 3 8,031,083
Microsatellites
EST9 Fal10 6 24,700,943
EST10 Fal10 6 24,725,801
EST16 Fal1 Adenylate cyclase-activating polypeptide 1 2 104,980,406
EST31 Fal19 Peroxiredoxin-6 8 4,336,642
EST46 Fal30 α-Fetoprotein enhancer-binding protein 11 21,546,200
Fhy215 Fal1
Fhy216 Fal3
Fhy217 Fal3
Fhy220 Fal4
Fhy221 Fal16
Fhy223 Fal4 NW_001471545.1 Gga1 WGA43_2 1 140,906,192
Fhy224 Fal9 NW_001471459.1 Gga15 WGA207_2 15 1,723,096
Fhy225 Fal2
Fhy226 Fal2
Fhy227 Fal8
Fhy228 Fal22
Fhy230 Fal1 NW_001471633.1 Gga2 WGA60_2 2 49,531,823
Fhy231 Unlinked
Fhy234 Fal1
Fhy235 Fal22 NW_001471676.1 Gga3 WGA95_2 3 5,902,333
Fhy236 Fal15 NW_001471568.1 Gga20 WGA258_2 20 12,551,523
Fhy237 Fal6
Fhy301 Fal16 NW_001471434.1 Gga11 WGA182_2 11 4,504,384
Fhy304 Fal5
Fhy306 Fal5
Fhy310 Fal17
Fhy321 Fal10
Fhy326 Fal6 NW_001471698.1 Gga5 WGA124_2 5 16,318,616
Fhy328 Fal5
Fhy329 Fal2 NW_001471669.1 Gga3 WGA102_2 3 48,212,536
Fhy336 Fal1
Fhy339 Fal8
Fhy341 Fal3
Fhy342 Unlinked
Fhy344 Fal5 NW_001471687.1 Gga4 WGA113_2 4 84,661,433
Fhy350 Fal9 NW_001471461.1 Gga15 WGA209_2 15 9,498,662
Fhy356 Fal3 NW_001471552.1 Gga1 WGA4_2 1 7,812,491
Fhy361 Fal1 NW_001471633 Gga2 WGA60_2 2 45,075,848
Fhy370 Fal8 NW_001471529.1 Gga1 WGA29_2 1 92,668,432
Fhy401 Fal5
Fhy403 Fal1
Fhy404 Unlinked
Fhy405 Fal9
Fhy407 Fal4 NW_001471554.1 Gga1 WGA51_2 1 177,252,431
Fhy408 Fal3
Fhy413 Fal1
Fhy415 Fal1 NW_001471639.1 Gga2 WGA66_2 2 79,942,990
Fhy427 Fal3 NW_001471510.1 Gga1 WGA11_2 1 21,414,296
Fhy428 Fal1
Fhy429 Unlinked
Fhy431 Fal10
Fhy432 Unlinked
Fhy444 Fal4
Fhy448 Fal2
Fhy450 Fal7
Fhy452 Fal4
Fhy453 Fal10 NW_001471713.1 Gga6 WGA139_2 6 3,534,436
Fhy454 Unlinked
Fhy458 Fal1 NW_001471651.1 Gga2 WGA78_2 2 129,424,241
Fhy464 Fal2
Fhy465 Fal4 NW_001471554.1 Gga1 WGA51_2 1 176,719,296
Fhy466 Fal7 NW_001471729.1 Gga7 WGA155_2 7 13,437,385
Fhy467 Fal1
FhU3 Fal1
FhU4 Fal3
FhU5 Fal1
GG-C25 Fal6 5 31,720,224
SS12 Fal3
ZF-C59 Fal1 Adenylate cyclase-activating polypeptide 1 2 104,980,320
ZF-S8 Unlinked Hypothetical protein 18 4,041,446
ZF-S9 Fal12 13 8,811,918
a

The contig number from the chicken genome sequence build 2.1 is described for microsatellites.

b

ENSEMBL ID for the orthologous chicken gene (ENSGALG000000xxxxx).

c

Loci from Borge et al. (2005).

Seventy microsatellites were isolated from the closely related pied flycatcher (Ficedula hypoleuca: Leder et al. 2008). Sixty-three of these markers, as well as five EST-linked microsatellites and nine microsatellites from other passerines (Karaiskou et al. 2008), were PCR multiplexed in sets of six to nine loci using 30 ng of DNA per reaction. Each PCR multiplex could be analyzed on a single run of an ABI3130xl (Applied Biosystems). Detailed PCR multiplex protocols and electrophoresis details can be found in Karaiskou and Primmer (2007).

Data analysis:

Microsatellites were scored using the GeneMapper software (Applied Biosystems). SNPs from the same intron were combined into haplotypes using the available pedigree information. For both types of markers, missing data points of parents were inferred from the haplotypes of offspring and mates when possible. Offspring showing deviations from the expected parental genotypes/haplotypes were not included in further analysis. These are likely to represent extra-pair offspring since previous work in this population has revealed that ∼15% of all offspring result from extra-pair copulations (Sheldon et al. 1997; Sheldon and Ellegren 1999).

Linkage analyses were performed with CRI-MAP (Green et al. 1990). Initially, all markers were tested against each other with the two-point option and markers that clustered together with significant lod score support (>3.0) were treated as linkage groups. Framework maps were constructed with the build option and the best position of all markers within an ordered linkage group was then estimated with recurrent runs of the option flips4 until no better order could be found (best order map).

Microsatellite clone sequences were used in cross-species MEGABLAST searches against the chicken genome sequence (http://www.ncbi.nlm.nih.gov/genome/seq/BlastGen/BlastGen.cgi?taxid=9031), first with default settings and then with relaxed settings according to Dawson et al. (2006). Both search methods generated the same set of significant (arbitrarily set at <E−5) hits, although the relaxed settings generated somewhat lower E-values. Because of this procedure 20 of the microsatellites could be anchored to a single location in the chicken genome and therefore be used for comparative studies. Chicken genomic locations were taken from Build 2.1 of the chicken genome, obtained from http://www.ncbi.nlm.nih.gov/mapview/maps.cgi?taxid=9031. Data on chicken recombination rates were from the same source. The particular markers that we used for collared flycatcher mapping were not always included in the chicken genetic map. To obtain recombination rate estimates for orthologous regions of the collared flycatcher and chicken genomes, we therefore used data from genetic markers located preferably within 1 Mb of our markers in the chicken genome. Graphical presentations of genetic maps were created in MapChart (Voorrips 2002).

RESULTS

Marker analysis:

We genotyped 384 previously identified SNPs in a pedigree of 322 collared flycatchers. After excluding SNPs found to be monomorphic in the pedigree (36 sites) or with a sample call rate <60% (23), segregation data for 321 SNPs from 170 genes became available. These genes are from 26 of the 28 chromosomes contained within the most recent (May 2006) version of the chicken genome assembly; it was not possible to develop conserved markers for Gga16 and Gga25 due to a lack of assigned genes to these small microchromosomes. SNPs from the same intron were combined into haplotypes to increase the informativeness of each gene in pedigree analysis. In addition, 71 polymorphic microsatellites were scored in the pedigree. We thereby had a total of 241 loci (“markers”) available for mapping. The average number of informative meioses for SNP haplotypes and microsatellites was 184 and 240, respectively (supplemental Table 2).

Linkage mapping:

Linkage analysis detected significant two-point linkage (lod score >3.0) to at least one other marker for 211 of the 241 loci. These 211 markers form a best-order genetic map consisting of 33 linkage groups (Figure 1), ranging in size from a genetic length of 325 cM (with 37 markers) to 0 cM (two groups with two markers showing no recombination). We refer to these linkage groups as Fal1-33 (F. albicollis linkage groups 1–33). The mean genetic distance between adjacent markers in the map is 10.0 cM (±6.7 SD). A framework map based on markers showing a multi-point lod score >3 is presented in supplemental Figure 1; generally, the framework map differs from the best-order map only by the inability to confidently place some markers on either side of adjacent loci.

Figure 1.—

Figure 1.—

Figure 1.—

Figure 1.—

A genetic linkage map of the collared flycatcher genome. Cumulative genetic distances in centimorgans are given to the right of each chromosome. Gene markers (genotyped by SNPs) are in regular text while anonymous microsatellites are in italics.

The total sex-average length of the best-order map is 1787 cM, with significantly more recombination in males (P = 0.01, Wilcoxon's test for paired data). Overall, recombination is 22% higher in males than in females (total distance 1982 vs. 1627 cM), although for individual intervals the female point estimate is sometimes higher than the male estimate. Sex-specific linkage maps are presented in supplemental Figure 2.

Figure 2.—

Figure 2.—

Figure 2.—

Figure 2.—

Figure 2.—

Figure 2.—

Genome conservation revealed by the alignment of orthologous collared flycatcher linkage groups and chicken chromosomes. Chromosomes/linkage groups are drawn proportional to their genetic length (the same for both species) with the full length of chicken chromosomes displayed.

Thirty markers (22 genes and eight microsatellites) remain unlinked. It is clear that this is at least in part due to a lack of power to detect linkage, since unlinked markers are highly overrepresented among markers with a low number of informative meioses (supplemental Table 2). However, nine unlinked genic SNP haplotypes and six unlinked microsatellites appear as singletons despite >70 informative meioses. Because the microsatellites were isolated by random library screening (Leder et al. 2008), it is possible that they correspond to regions of the chicken genome, which is not yet contained within the chicken genome assembly. For the gene-based SNPs, a possible explanation of the absence of linkage is that they are located in regions of high recombination within conserved linkage groups. Given the observation that recombination rates tend to be elevated toward telomeric ends of avian chromosomes (International Chicken Genome Sequencing Consortium 2004; Schmid et al. 2005; Wahlberg et al. 2007), this explanation is supported by the fact that 6 of 9 unlinked genes are the most distal marker on chicken chromosomes in our marker set (at 2p, 3p, 4q, 5q, 10p, and 10q, respectively). Alternatively, they may indicate chromosomal rearrangements (see supplemental data).

Comparative mapping:

A major advantage of this map is that genic markers allow the identification of homologous regions in the genomes of other species; this is particularly important for the ability to transfer genomic information from model organisms to nonmodel ones. The 33 collared flycatcher linkage groups correspond to 24 different chromosomes in chicken, with the 2 remaining chicken chromosomes from which we had markers (Gga18 and Gga22) each being represented by two to three unlinked singletons. By comparing the location of gene sequences in the chicken and collared flycatcher genomes (as well as of 20 flycatcher microsatellites for which a homologous sequence could be identified in chicken), we find a remarkable degree of chromosomal conservation, both at the level of shared synteny and at the level of conserved gene order (Figure 2). No fewer than 18 chicken chromosomes correspond to a single linkage group in the collared flycatcher, indicating completely conserved synteny.

Seven chicken chromosomes are orthologous to two to three collared flycatcher linkage groups, suggestive of fusion/fission events. However, as discussed in detail in the supplemental data, several of these cases are likely to represent a lack of power to connect linkage groups that originate from the same collared flycatcher chromosome. The interval between SNP-based gene markers is generally <10 Mb in the chicken genome. As recombination rates are known to vary across the genome, particularly due to the presence of recombination hot spots, physical intervals of this size may correspond to genetic distances longer than that possible for detecting linkage. Of course, length expansions in the collared flycatcher genome would accentuate such problems. In the end, only two rearrangements that distinguish the karyotypes of the chicken and the collared flycatcher are strongly supported by our data (supplemental data) and are also independently confirmed in other species. These include a fission of the ancestral chromosome 1 in Passeriformes to yield the collared flycatcher linkage groups Fal3 and Fal8 (supported by data in Guttenbach et al. 2003; Derjusheva et al. 2004; Itoh and Arnold 2005) and the fusion of ancestral chromosomes 4 (corresponding to Fal5) and 10 (Fal18) in the chicken lineage to yield Gga4 (supported by Reed et al. 2005). One or a few more rearrangements could be indicated by our data but would need a denser map for confirmation.

Generally, gene order within syntenic groups is completely conserved in the chicken–collared flycatcher comparison. There are 18 cases of intrachromosomal rearrangements in the best-order map. However, only 7 of these remain in the framework map [corresponding to Gga1-Fal4 (two cases), Gga1-Fal8, Gga3-Fal2, Gga4-Fal5, Gga15-Fal9, and Gga20-Fal15; supplemental Figure 1]; the other 11 cases are in the form of inversed order of markers that is not statistically supported (multi-point lod score <3). Six of the 7 well-supported cases are consistent with rather short inversions of ∼1.5–6 Mb according to the chicken genome sequence, while the seventh represents a large proportion of Gga4-Fal5 that spans at least 38 Mb.

DISCUSSION

This work reveals an evolutionary stasis of gene order and chromosome organization in a comparison of two highly diverged avian lineages, estimated to have separated 100 million years ago (MYA) ago. Our results confirm the stability of avian genomes previously indicated by results from comparative mapping in chicken and mammals (Burt et al. 1999; Bourque et al. 2005) and from cytogenetic (e.g., Griffin et al. 2007) and genetic (e.g., Dawson et al. 2007) analyses within birds. However, as previous work has been largely insensitive to intrachromosomal structures, and to fine-scale interchromosomal organization, our findings extend the observation of the genomic stability of birds to be valid also at the level of gene order and organization and across distantly related taxa.

Stasis of avian genome organization:

The karyotype of the collared flycatcher has not been characterized, but the great majority of passerine birds so far analyzed have a chromosome number between 78 and 80, i.e., quite similar to the 2n = 78 of chicken (Gregory et al. 2006). The structure of the karyotype is also well conserved with a few large macrochromosomes and a large number of very small microchromosomes. Moreover, available data from measurements of DNA content indicate that genome size is more or less identical in chicken and birds from the order Passeriformes, at just ≈1 Gb (Gregory et al. 2006). Assembled genome sequence has been assigned to 28 of the 36 chicken autosomes (Gga29-36 are not covered in the assembly and represent microchromosomes with <5–10 Mb DNA). Most of these chromosomes correspond to a single linkage group in the collared flycatcher map. We find strong support for two interchromosomal rearrangements that have occurred since the divergence of the lineages leading to the chicken and the collared flycatcher, rearrangements which are also supported by previous observations (International Chicken Genome Sequencing Consortium 2004; Griffin et al. 2007). There are other gaps in the collared flycatcher linkage map aligned to chicken that might indicate the presence of one to three additional fissions or fusions (corresponding to Gga1, Gga3, and Gga12). However, it is possible that we lack the power to detect linkage in these cases because markers flanking the gaps might be too far apart, contain too little information, or are separated by a region of high recombination rate (see supplemental data).

There is also evidence for at least seven intrachromosomal rearrangements in the chicken–collared flycatcher comparison. Four of these have occurred in the vicinity of the sites for interchromosomal rearrangement, indicating that there are regions of avian chromosomes that are particularly fragile and prone to different types of rearrangement. The number of observed intrachromosomal rearrangements in the collared flycatcher–chicken comparison is roughly two to three times the number of interchromosomal rearrangements. A similar ratio is also found in mammals (Pevzner and Tesler 2003; Pontius et al. 2007). This indicates that it is not just the inter- or the intrachromosomal rate of rearrangement that is low in birds; rather, it is the overall rate of rearrangements that is uniformly low.

The incidence of inter- and intrachromosomal rearrangements seen in this study can be used to roughly estimate the minimum rate of chromosomal rearrangement in birds. We have to take into account that our map does not cover the entire genome and that the resolution may be insufficient for detecting small rearrangements within mapped regions. With this caveat in mind and assuming a 66% genomic coverage of the map (see below) and 100 MY since the most recent common ancestor of Galliformes and Passeriformes (200 MY of evolution in total), there is an overall minimum rate of chromosomal exchange during avian evolution of approximately one event/15 (200/9 × 0.66) MY (0.045/MY). Separate estimates for inter- and intrachromosomal rearrangement give one fission/fusion event/66 MY (0.015/MY) and one large-scale inversion event/19 MY (0.05/MY). This is considerably lower than what has been estimated for mammalian lineages (≈0.6–2.0; Pontius et al. 2007) and gives a quantitative idea of the relative stability of avian genomes.

The genomic integrity shown by the comparison of two distantly related avian lineages provides insight into vertebrate karyotype evolution. It has been shown that the rate of chromosomal diversification varies considerably on a temporal scale (Ferguson-Smith and Trifonov 2007). For example, while the rate of chromosomal diversification is thought to have been comparatively high in the lineage leading from an early vertebrate ancestor to the eutherian ancestor, by contrast it was considered to be low in the lineage from the eutherian ancestor to the primate ancestor (and continued to be so in the human lineage) (Kohn et al. 2006). However, no such temporal heterogeneity is indicated in either the chicken or the collared flycatcher lineage. In fact, the ancestral vertebrate karyotype is highly conserved in the chicken so genomic stability must have been prevalent all along the lineage leading to modern birds since the split of synapsids and diapsids 310 MYA. The only clear exception is provided by birds of prey that have an atypical bird karyotype that lacks distinct macrochromosomes and microchromosomes (Deoliveira et al. 2005).

Why does the degree of genomic integrity differ extensively between birds and mammals? One possible explanation relates to the role of repeat elements in governing chromosome fragility and the dearth of active families of interspersed repeat elements in avian genomes (International Chicken Genome Sequencing Consortium 2004). Breakpoints for chromosome rearrangements tend to be enriched with interspersed repetitive elements, low-copy repeats, and segmental duplications (Bailey et al. 2004; Freudenreich 2007; Kehrer-Sawatzki and Cooper 2007), including in chicken (Gordon et al. 2007). Mechanistically, unequal crossing over between repeated sequences within or between chromosomes is likely to contribute to this pattern (Lupski and Stankiewicz 2005). The bird genome has remained compact and repeat poor during avian evolution (Organ et al. 2007); there is only one abundant class of interspersed repeats in the chicken genome: the long interspersed CR1 element, with a vanishingly small proportion representing anything other than short and heavily truncated copies (International Chicken Genome Sequencing Consortium 2004). In light of the potential link between a low-repeat content and chromosomal integrity, it is tempting to invoke a nonadaptive explanation to genomic stability of birds.

One interesting aspect of genomic stability of birds is the role of chromosomal rearrangements in speciation (Noor et al. 2001; Rieseberg 2001; Navarro and Barton 2003). It is known that crosses between chromosomal variants can result in hybrid inviability or impaired fitness (Capanna and Castiglia 2004). Speciation rates differ considerably between birds and mammals with the evolution of post-zygotic incompatibility being ∼10 times slower in birds than in mammals (Price and Bouvier 2002; Fitzpatrick 2004). It is possible that the formation of post-zygotic barriers in birds is delayed due to the slow rate of chromosomal rearrangement.

A partial genetic map, based mainly on microsatellites and AFLP markers, has been developed for another passerine bird, the great reed warbler (Hansson et al. 2005; Åkesson et al. 2007; Dawson et al. 2007). The seven collard flycatcher–chicken gene-order differences that we detected in this study are not evident in the comparison between the great reed warbler and the chicken (Dawson et al. 2007). This could suggest that these inversions arose in the collared flycatcher lineage subsequent to the split of Muscicapoidea–Sylvoidea. However, the physical marker density and chromosomal coverage in the great reed warbler map is relatively low, especially for markers informative in comparative mapping, so it may be that the resolution is not sufficient for detection of some intrachromosomal rearrangements. Neither of these inversions is seen in the fairly dense map of the turkey genome (Reed et al. 2005) so they may have arisen either early in the evolution of Galliformes or somewhere along the passerine lineage leading to the collared flycatcher. The great reed warbler map revealed two clear cases of inversions when compared to chicken chromosomes 1 and 2, respectively (Dawson et al. 2007). However, they are not seen in the collared flycatcher–chicken comparison despite dense marker coverage in these regions. They are therefore likely to have arisen in the lineage leading to the great reed warbler subsequent to the split of Muscicapoidea–Sylvoidea.

Sex-specific recombination rates:

There is evidence for heterochiasmy in collared flycatchers and the direction (22% more recombination in males) is in agreement with the Haldane–Huxley rule, which states that, in species where the autosomal recombination rate differs quantitatively between sexes, it is usually the heterogametic sex that has a reduced recombination rate. However, as in several galliform birds (Groenen et al. 2000; Kayang et al. 2004; Reed et al. 2005), the difference is not as pronounced as that seen in most mammals [in humans, for example, the female rate is ∼1.6 times higher than the male rate (Broman et al. 1998)]. The great reed warbler shows a quite contrasting pattern, with a more than twofold excess of recombination in females (Hansson et al. 2005; Dawson et al. 2007), i.e., against the expectations of the Haldane–Huxley rule. This difference between two passerine birds is unexpected and not easily conceived in light of alternative hypotheses for the evolution of heterochiasmy (Lenormand 2003). For example, there is some support for the idea that haploid selection plays a role (Lenormand and Dutheil 2005). According to this model, and assuming epistasis, the sex experiencing the largest variance in reproductive success should recombine less to keep favorable gene combinations together. However, both collared flycatchers (Sheldon et al. 1997; Sheldon and Ellegren 1999) and great reed warblers (Hasselquist et al. 1998) are polygynous species and there is no obvious reason to believe that the intensity of gametic selection would differ between them. As it stands now, further work in additional bird species is needed to obtain a more broad-scale picture of avian recombination rates.

Genome coverage:

How large a proportion of the collared flycatcher genome is covered by this map? One way to approach this question is to make use of physical information from the chicken genome. The amount of chicken sequence contained within linkage groups shared between the chicken and the collared flycatcher is 663 Mb, or 66% of the total ≈1-Gb autosomal genome (the sequence assigned to chromosomes in the chicken genome assembly covers ∼90% of the genome). Obviously, additional sequence is covered in the flycatcher map if the 15 highly polymorphic unlinked singletons are included and when considering the fact that each end marker in all linkage groups covers some flanking distance. Assuming a similar genome size as in chicken (Gregory et al. 2006), it may be estimated that our map covers 75–80% of the collared flycatcher genome. It is more difficult to assess the proportion of the total genetic length of the flycatcher genome covered by the map. First, we probably lack markers from a number of microchromosomes to which assembled sequence has not yet been assigned in the chicken. However small a microchromosome is, it contributes 50 cM to the total map length since there is an obligate crossing over per chromosome (Jones and Franklin 2006). Second, recombination rates tend to increase toward telomeres, so it can therefore be difficult to assess the amount of recombination outside linkage groups by extrapolation. When it comes to genetic coverage, we thus conclude that it must be less than the physical coverage estimated above.

Genomics of natural populations:

There is a slow but steady progress in applying genetic maps for quantitative trait locus (QTL) mapping in natural animal populations (Slate 2005), either directly in the wild or by using wild-caught individuals raised in the laboratory. Notable examples from ecologically important animal models include the analysis of the genetic basis of body armour in the stickleback Gasterosteus aculeatus (Peichel et al. 2001; Colosimo et al. 2005) and of body weight and morphology in the free-living Soay sheep Ovis aries (Beraldi et al. 2007) and the red deer Cervus elaphus (Slate et al. 2002). In the two latter systems, microsatellite markers developed in closely related domestic animals could be used across species. In sticklebacks, anonymous, species-specific microsatellites were used and random approaches for map development have also included the use of microsatellites, RAPD, or AFLP markers in a number of other species (Reid et al. 2007; Troggio et al. 2007).The development of the collared flycatcher map represents an application of a new approach to genetic mapping in natural populations. For several reasons, it benefited from an earlier systematic effort to develop a set of conserved reference markers evenly spread across the avian genome (Backström et al. 2008).

First, through identification of particularly conserved sites for primer design, these markers had a high amplification success rate in collared flycatchers. Second, the design of intronic amplicons 500–1000 bp in size uncovered >900 polymorphic sites with just a moderate amount of screening (10 unrelated individuals; Backström et al. 2008), from which we could choose the most informative polymorphisms for genotyping. SNP-based mapping is particularly attractive since large-scale analysis can be conducted using automatic procedures; this study generated 150,000 genotypes. Third, and importantly, since the reference set of markers was developed to represent a uniform coverage of all assembled chicken chromosomes, the markers also covered a significant part of the collared flycatcher genome. Clearly, using the same number of randomly selected markers would not have given the same degree of genome coverage. Indeed, the high degree of synteny and gene-order conservation in birds added to this benefit, although, in principle, the use of markers evenly distributed in a related species should always give better coverage than using random markers. Fourth, as the first map of a natural population based on protein-coding gene markers, it is straightforward to transfer genetic information from model species by means of anchoring of orthologous loci. These features should apply equally to any bird species and we therefore envision that the marker set will become important for future studies of the genetics of natural bird populations. The use of the same set of markers should also aid comparison of maps across many different species. More generally, the approach of designing evenly distributed, conserved gene markers from one or more model species could potentially be applied to many groups of organisms.

While SNPs offer a nearly inexhaustible source of genetic markers that are amenable to large-scale analysis, they come with the price of typically showing lower levels of polymorphism compared to microsatellites. For this reason, we also included a set of microsatellites in this study, as this was expected to facilitate anchoring of linkage groups. However, the difference in average information content between microsatellites and SNPs was not very large (mean number of informative meioses of 240 and 184, respectively). Moreover, we could not detect any significant difference in the percentage of unlinked markers from the different categories (8 of 71 for microsatellites vs. 22 of 170 for SNP haplotypes). This is likely due to the fact that for most genes we combined SNPs into haplotypes, thereby increasing their informativeness.

To conclude, we report here a gene-based genetic map of the collared flycatcher that, when compared to the chicken map, demonstrates extensive synteny and gene-order conservation during 100 MY of evolution. This high degree of genome stability of birds is likely to have important consequences for their general evolutionary patterns, including processes of speciation.

Acknowledgments

Financial support was obtained from the Swedish Research Council. SNP genotyping was performed at the SNP Technology Platform at Uppsala University, which is gratefully acknowledged.

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