A first-generation microsatellite-based genetic linkage map of the Siberian jay (Perisoreus infaustus) : insights into avian genome evolution

BioMed Central Page 1 of 17 (page number not for citation purposes) BMC Genomics Open Access Research article A first-generation microsatellite-based genetic linkage map of the Siberian jay (Perisoreus infaustus): insights into avian genome evolution Sonja Jaari, Meng-Hua Li* and Juha Merilä Address: Ecological Genetics Research Unit, Department of Biological and Environmental Sciences, PO Box 65, FIN-00014 University of Helsinki, Finland Email: Sonja Jaari - [email protected]; Meng-Hua Li* - [email protected]; Juha Merilä - juha.meril[email protected] * Corresponding author Abstract Background: Genomic resources for the majority of free-living vertebrates of ecological and evolutionary importance are scarce. Therefore, linkage maps with high-density genome coverage are needed for progress in genomics of wild species. The Siberian jay (Perisoreus infaustus; Corvidae) is a passerine bird which has been subject to lots of research in the areas of ecology and evolutionary biology. Knowledge of its genome structure and organization is required to advance our understanding of the genetic basis of ecologically important traits in this species, as well as to provide insights into avian genome evolution. Results: We describe the first genetic linkage map of Siberian jay constructed using 117 microsatellites and a mapping pedigree of 349 animals representing five families from a natural population breeding in western Finland from the years 1975 to 2006. Markers were resolved into nine autosomal and a Z-chromosome-specific linkage group, 10 markers remaining unlinked. The best-position map with the most likely positions of all significantly linked loci had a total sex-average size of 862.8 cM, with an average interval distance of 9.69 cM. The female map covered 988.4 cM, whereas the male map covered only 774 cM. The Z-chromosome linkage group comprised six markers, three pseudoautosomal and three sex-specific loci, and spanned 10.6 cM in females and 48.9 cM in males. Eighty-one of the mapped loci could be ordered on a framework map with odds of >1000:1 covering a total size of 809.6 cM in females and 694.2 cM in males. Significant sex specific distortions towards reduced male recombination rates were revealed in the entire best-position map as well as within two autosomal linkage groups. Comparative mapping between Siberian jay and chicken anchored 22 homologous loci on 6 different linkage groups corresponding to chicken chromosomes Gga1, 2, 3, 4, 5, and Z. Quite a few cases of intra-chromosomal rearrangements within the autosomes and three cases of inter-chromosomal rearrangement between the Siberian jay autosomal linkage groups (LG1, LG2 and LG3) and the chicken sex chromosome GgaZ were observed, suggesting a conserved synteny, but changes in marker order, within autosomes during about 100 million years of avian evolution. Conclusion: The constructed linkage map represents a valuable resource for intraspecific genomics of Siberian jay, as well as for avian comparative genomic studies. Apart from providing novel insights into sex-specific recombination rates and patterns, the described maps – from a previously genomically uncharacterized superfamily (Corvidae) of passerine birds – provide new insights into avian genome evolution. In combination with high-resolution data on quantitative trait variability from the study population, they also provide a foundation for QTL-mapping studies. Published: 3 January 2009 BMC Genomics 2009, 10:1 doi:10.1186/1471-2164-10-1 Received: 16 July 2008 Accepted: 3 January 2009 This article is available from: http://www.biomedcentral.com/1471-2164/10/1 © 2009 Jaari et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 2 of 17 (page number not for citation purposes) Background Under various completed or ongoing projects, rapid progress has been attained in the generation of genomic resources for model organisms and domestic animals of medical, economic, or agricultural importance (e.g. [13]). However, genomic resources for the majority of freeliving vertebrates of ecological and evolutionary importance are still scarce. For instance, in wild birds, development of genomic resources are still in their infancy, and only few initial efforts in linkage mapping [4-8], estimation of the extent of linkage disequilibrium [9,10], and syntenic comparison between related species [7,8,11-14] ] have been conducted. Hence, very limited information on the genome structure of wild bird species is available for further synthesis, as well as to study and characterize molecular underpinnings of phenotypic traits. Since wild passerine birds are important 'model' organisms in ecology and evolutionary biology, and in studies of life history evolution (e.g. [15]), behaviour (e.g. [16,17]) and evolutionary quantitative genetics in particular (e.g. [18-20]), knowledge of their genome structure and organization is vital to advance our understanding of the genetic basis of ecologically important traits [21]. Genetic maps constitute essential and powerful organizational tools for genomic research [22]. Among the most important applications of genetic maps in genomic analyses is in that they provide a platform to support studies utilizing or aiming to apply candidate gene approaches [21,23], QTL mapping [24], comparative genomics [25], and genome annotation [26]. However, construction of genetic linkage maps for non-model organisms is complicated by several factors [27,28]. One of the major obstacles for the construction of linkage maps in passerine birds (but see [4]) is the scarcity of informative genetic markers. Among a variety of molecular makers previously employed in linkage mapping in different organisms, microsatellite markers have often proven most useful due to their hypervariability, fast evolutionary rates, codominance, wide distribution throughout the genomes, and the relative ease with which they can be developed and genotyped using the polymerase chain reaction (PCR; e.g. [29]). While genetic maps exist in one form or another for various species, it is worth noticing that the studies are so far generally limited to domestic animals or natural populations of wild species that can easily be bred in captivity, or where sufficiently large litter sizes are being produced in natural settings and are accessible to sampling to allow the establishment of the pedigree necessary for linkage analysis [9]. Unfortunately, the characteristics that make populations practical for linkage mapping [9] are found only among a small fraction of species studied by ecologist and evolutionary biologists. Linkage maps have now been constructed in four populations of non-model animals for which long-term individual-based datasets are available (see also: [8]), and where natural long-term pedigrees (rather than experimental breeding programmes) have been used to follow the co-segregation of marker alleles [28]. Two of these mapping populations are in ungulate species (soay sheep, Ovis aries [24]; red deer, Cervus elaphus [27]) and two are in passerine birds (great reed warbler, Acrocephalus arundinaceus [4,6,13]; collared flycatcher, Ficedula albicollis [5,9,11]). The Siberian jay (Perisoreus infaustus) is a passerine bird which has been subject to considerable ecological and evolutionary research during the past decades. Studies in its breeding biology [30-33], mating system [34,35], foraging behaviour [36], reproductive success [37], parental care and dispersal pattern [38,39], family structure [40], phenotypic plasticity [41] and levels of inbreeding [42] have been conducted. Thus, these previous studies form an appropriate setting in an initiative to explore the integration of genomics with the domain of ecology and evolutionary biology [43], provided that at least some basic knowledge of the species' genome can be obtained. With an access to detailed pedigrees of a Siberian jay population monitored over 30 years [40,42], as well as access to a novel set of polymorphic microsatellites developed for this species [44], construction of a linkage map is now realistic. In an evolutionary context, the chicken genome sequence [45] released recently facilitates genomic studies in other bird species by comparative genomic approaches [13,25]. Moreover, given the early divergence of avian lineages between passeriforms and galliforms (≈ 100 million years ago; [46]) and the high level of phylogenetic divergence between jays belonging to the Corvidae family and the other passerines for which linkage maps have been published (e.g. [47,48]), a linkage map of the Siberian jay may provide new insights into avian genome evolution, and thereby also to the extensive morphological, life historical and behavioural diversification within the order Passeriformes (see [47]). The aim of this study was to develop a first-generation genetic linkage map for a wild population of Siberian jays on the basis of 117 microsatellites, including a novel set of 108 markers. To this end, a framework map was constructed to identify markers whose local relative orders were statistically well supported with an unambiguous location in the map. Since heterochiasmy has been observed in previous studies of many species (e.g. zebrafish [49]; and great reed warbler [4]), sex-specific variation in the recombination rate and the genetic map distance were also investigated. Furthermore, to provide a comparative perspective to address the evolution of genome organisation the extent of synteny and locus order conservation between Siberian jay and chicken was evaluated by a BLAST analysis against the chicken genome sequence. BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 3 of 17 (page number not for citation purposes) Results Characteristics of polymorphic microsatellites Of the 117 microsatellites scored, six loci (SJ009, SJ046, SJ048, SJ069, SJ083 and SJ108) were assigned to the Zchromosome by observation of complete cosegregation with sex and the observation of heterozygosity in some males but none of the females in the pedigrees. None of the markers examined appeared to be situated in W-chromosome since all the markers had alleles in the males. The number of informative meioses varied from 33 (SJ047) to 474 (CKL5) with an average of 284.63 informative meioses per locus. More details about levels of genetic variability (HO, HE and PIC) are shown in Additional File 1. Genetic linkage maps An overview of the linkage data is given in Figures 1, 2 and Table 1 depicting the best-position and framework linkage maps and their characteristics. Of the 117 microsatellites, 107 loci (91%) were assembled into 9 autosomal linkage groups (LG1 – LG9) and one Z-chromosome linkage group (LGZ), and the other 10 polymorphic microsatellites (SJ002, SJ003, SJ005, SJ020, SJ030, SJ034, SJ118, MJG1, PER1 and LTML8) appeared to be unlinked to any other marker by two-point analysis with LOD scores < 3.0. Of the ten unmapped markers, six had less than 60 informative meioses while four had more than 200 informative meioses. Of the nine autosomal LGs, seven comprised of six or more loci and the remaining three LGs each contained two or three loci, with an average of ca. 11 microsatellites per LG. For the sex-average autosomal LGs in the best-position map (Figure 1), the meiotic lengths, evaluated as the distance between the outermost markers on each LG, ranged from 10.6 cM (LG09) to 185.6 cM (LG01) spanning in total 862.8 cM of the Siberian jay genome. The average marker interval was 9.69 cM calculated as the arithmetic mean of the map distances between adjacent markers (Table 1). On the maps, 35.9% (33/92) of the intervals between markers varied from 0 to 5 cM, 31.5% (29/92) ranged from 5 to 10 cM, and 20.7% (19/ 92) from 10 to 20 cM, and 12% (11/92) were > 20 cM. Sex-specific autosomal maps were also constructed (Figure 1). The sum of the length of all autosomal LGs was 774.0 cM in males and 988.4 cM in females, with an average intermarker spacing of 8.6 cM and 12.1 cM, respectively. The male map comprises LGs ranging in length from 7.7 cM to 171.1 cM while the female map contains LGs with a length from 9.2 cM to 229.2 cM (Table 1). Out of the nine pairs of male and female LGs, seven were larger in the female map and two were larger in the male map. In total, the autosomal LGs were smaller in males as compared to females with a female-to-male map ratio of 1.28. The sex-average map was intermediate in length between sex-specific maps, and 1.12 times longer than the male map. Framework markers, which could be ordered with LOD score of 3.0 or greater (indicating odds of 1000:1), are indicated in bold fonts in the best-position map (Figure 1). Of the total 107 mapped markers, 81 loci were significantly ordered in the framework map and most (16/24) of the remaining loci could be placed with significant support in either of two alternative intervals. When only the framework markers were considered, the total size of autosomal linkage groups was 692.1 cM in the sex-average map, 649.4 cM in the male map, and 799 cM in the female Table 1: Characteristics of the best-position and framework maps for Siberian jay LG Best-position map (cM) Framework map (cM) No. of loci Sex average 씸씹Average intermarker distancea Ratio of 씸/ 씹 maps No. of loci Sex average 씸씹Average intermarker distancea Ratio of 씸/ 씹 maps LG1 29 185.6 213.6 168.3 6.87 1.27 20 167.0 182.8 156.7 8.35 1.17 LG2 27 181.5 229.2 141.3 6.72 1.62 21 141.3 212.1 116.8 6.73 1.82 LG3 13 182.6 197.9 171.1 16.6 1.16 10 170.2 175.5 171.3 17.02 1.02 LG4 11 98.2 110 86.7 9.82 1.27 9 76.0 88.3 63.8 8.44 1.38 LG5 8 85.2 92.9 82.1 12.17 1.13 7 83.9 93.4 78.4 11.99 1.19 LG6 6 78.2 98.9 65.4 15.64 1.51 3 14.4 15.5 13.2 4.80 1.17 LG7 3 26.4 24.3 32.3 13.2 0.75 2 14.2 9.8 22.4 7.10 0.44 LG8 2 14.5 9.2 19.1 15.5 0.48 2 14.5 9.2 19.1 7.25 0.48 LG9 2 10.6 12.4 7.7 10.6 1.61 2 10.6 12.4 7.7 5.30 1.61 LGAb101 862.8 988.4 774 9.69 1.28 76 692.1 799 649.4 9.11 1.23 LGZ 6 23.8 10.6 48.9 4.76 0.22 5 22.1 10.6 44.8 4.42 0.24 씸 Female-specific linkage groups 씹 Male-specific linkage groups a The average inter-marker distance is based on the sex-average map b total autosomal linkage groups BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 4 of 17 (page number not for citation purposes) The best-position linkage groups (male-specific, M; sex-average, A; and female-specific; F) in Kosambi centimorgans for the Siberian jayFigure 1 The best-position linkage groups (male-specific, M; sex-average, A; and female-specific; F) in Kosambi centimorgans for the Siberian jay. The markers in boldface font are framework loci with unambiguous relative position between each other. BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 5 of 17 (page number not for citation purposes) The framework linkage groups (male-specific, M; sex-average, A; and female-specific; F) in Kosambi centimorgans for the Sibe-rian jayFigure 2 The framework linkage groups (male-specific, M; sex-average, A; and female-specific; F) in Kosambi centimorgans for the Siberian jay. BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 6 of 17 (page number not for citation purposes) map (Figure 2 and Table 1). We compared recombination distances between adjacent framework markers that were mapped on both the best-position map and the framework map and overall the female-to-male ratio for the framework map was 1.23, slightly lower than the ratio of 1.28 observed above in the best-position map. Among the Z-linked microsatellites, all six markers showed highly significant linkage between each other with LODs > 37.0. This linkage group spanned 23.8 cM in the sex-average map, 48.9 cM in the male map and 10.6 cM in female map, which corresponds to a female-to-male ratio of 0.22. The female linkage map indicates the position and approximate extent of a pseudoautosomal region (PAR) from SJ069 to beyond SJ048. In females, no recombination was observed between SJ083 and SJ046 and no heterozygosity was observed for these markers; therefore they must lie outside the pseudoautosomal region, suggesting that the pseudoautosomal boundary lies between SJ048 and SJ046. As expected, there is considerable difference in male and female recombination rates for the pseudoautosomal region of the Z-chromosome, with the male distance between SJ108 and SJ069 being 41.7 cM as compared to the female distance of 5.1 cM. This increased sexspecific recombination rate between the three pseudoautosomal loci was similar to the observations in the pseudoautosomal regions of the mammalian sex chromosomes, for example in humans [50], ovines [51] and bovines [52]. In the sex-average map, the map density was 4.0 cM/marker among all Z-linked markers and 3.3 cM/marker among the five framework loci. Differences in recombination rate between sexes In addition to a much shorter total length of autosomal linkage maps in males than in females, the maps allowed comparison of meiotic recombination rate between sexes. The sexes show significant differences in recombination rates, both in general and for specific pairs of linked markers (Wilcoxon's signed-rank test, P = 0.037; Figure 3 and Table 2). In the best-position map (Figure 1), the proportion of intervals in the autosomal linkage groups that demonstrated a higher recombination fraction in females was 54.3%. Among all adjacent autosomal markers the recombination fraction was 1.28 times higher in females than in the males. However, there were exceptions to this in some LGs, and in some specific intervals within LGs. For instance, LG7 and LG8 exhibited higher recombination fractions in males than in females (Table 2). The number of intervals that show higher recombination fractions in the male map relative to the female map was less, but not negligible (Figure 3). When investigating the distortions over the autosomal linkage groups, two of the nine linkage groups showed significant (P < 0.05) difference in recombination rate between the sex-specific maps (Table 2). This was also observed when the overall map length was investigated for sex-specific difference. All in all, these results suggest that overall recombination is significantly suppressed in male meiosis as compared to female meiosis. Comparative mapping The BLAST searches under both settings generated the same set of significant hits at 1e-10. We found 25 homologous (21.4%, 25/117) zebra finch sequences using a cross-species MEGABLAST search in NCBI's zebra finch genome database (Table 3). By BLAST searching using two methods, in total 22 mapped (20.5%, 22/107) and three unlinked loci for which a homologous sequence could be identified in chicken were assigned to a chromosomal location in the chicken genome (Table 3). The 10 Siberian jay LGs corresponded to five different autosomal and one Z chromosome in chicken. Loci from the same Siberian jay LG matched sequences on a single chicken chromosome in the BLAST analysis (Figure 4 and Table 3), with the exception of loci SJ039, SJ101 and SJ076 on the autosomal LGs (LG1, LG2, and LG3, respectively) that mapped to chicken chromosome Z (GgaZ), whereas the other loci on these LGs mapped to the chicken autosomes. Table 2: The Wilcoxon's signed-rank test results for recombination fraction ( θ ) between sexes with linkage groups Linkage groups NaAverage θ FbAverage θ Mc θ F/ θ MWilcoxon's signed-rank test (P)d LG1 28 0.071 0.055 1.29 0.174 LG2 26 0.085 0.054 1.57 0.046 * LG3 12 0.152 0.133 1.14 0.323 LG4 10 0.101 0.077 1.31 0.038 * LG5 7 0.127 0.110 1.15 0.687 LG6 5 0.178 0.126 1.41 0.192 LG7 2 0.115 0.145 0.79 0.5 LG8 1 0.09 0.18 0.5 - LG9 1 0.12 0.08 1.5 - Total autosomal 92 0.101 0.079 1.28 0.037 * LGZ 5 0.02 0.094 0.21 0.025* a number of intervals; b average recombination fraction in females; c average recombination fractions in males; d *, significant, P < 0.05. BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 7 of 17 (page number not for citation purposes) Likewise, most loci on the same chicken chromosome matched sequences on a single Siberian jay LG, with the exceptions of three unlinked loci (SJ005, SJ020 and SJ034) and loci SJ009, SJ039, SJ101 and SJ076 on GgaZ that mapped to four different LGs, LGZ and LG1, LG2, and LG3, respectively. The relative order of the markers mapped to the Siberian jay LGs was compared with the same loci on chicken chromosomes in Figure 4. The chicken-Siberian jay comparison indicated that the order of loci was strikingly different between the chicken macrochromosomes Gga1, Gga2 and Siberian jay LG1, LG2 in the best-position map, respectively. Although some loci shared the same relative order in the two species, large rearrangements of the chromosome would have been necessary to give rise to the different orders found here. The cases of interand intrachromosomal rearrangements were involved mostly in the framework loci and represented a large proportion of Gga-LG1 that spanned around a 120-cM Siberian jay/20Mb chicken interval. The three unlinked loci, SJ005, SJ020, and SJ034, were located at the distal ends of two chicken macrochromosomes, Gga1 and Gga2. Discussion This study constitutes the first mapping effort of the Siberian jay genome, and is among the first ones to present a preliminary linkage map for any entirely natural vertebrate species from the wild (reviewed in [28]). The linkage map was composed using 107 polymorphic microsatellite loci typed on ca. 350 animals, making it one of the most detailed linkage maps available for natural animal popuFemale vs. male recombination fraction for 97 pairs of adjacent markers from the 10 linkage groups in the Siberian jayFigure 3 Female vs. male recombination fraction for 97 pairs of adjacent markers from the 10 linkage groups in the Siberian jay. BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 8 of 17 (page number not for citation purposes) lations [28]. In fact, it is one of only a few genetic linkage maps of wild bird species to date. Apart from the revealing evidence for sex differences in recombination rates, the constructed maps represent an excellent resource from which the markers may be selected for future mapping projects in this and related species, as well as for comparative genomic studies of genome organisation. In what follows, we will discuss the salient features of the constructed linkage maps in comparison to similar maps and results from earlier studies. In particular, we will pay attention to sex-specific differences in recombination rates, map coverage and some other issues deserving future attention. Genotyping in the mapping population The constructed map contains 107 microsatellites, of which 101 are autosomal, three Z-chromosome-specific and three pseudoautosomal loci (see below). The ideal set of molecular marker data for linkage mapping has no missing values, no genotyping errors and the markers segregate in the expected ratio for the specific type of population [53]. In practice, however, mapping data is compromised in all of these respects. However, as simulated and concluded in previous research [53], the effect of missing genotypes depends greatly on the sample size: the smaller the sample, the more severe the effects are likely to be. In comparison to published simulations, in Table 3: The homologous loci of microsatellites mapped in Siberian jay on the chicken and zebra finch genome assigned using BLAST analyses of the clone sequences of the microsatellites and the homologous zebra finch WGS sequences. Locus Linkage group Zebra finch Ensemble ID Chicken Ensemble ID Gga aChicken genome start position (bp) SJ010 LG1 gb|AC188472.1 NW_001471554.1 Gga1_WGA51_2b1 9,129,918 SJ016 LG1 - NW_001471545.1 Gga1_WGA43_2b1 9,256,107 SJ022 LG1 - NW_001471526.1 Gga1_WGA26_2b1 2,462,620 SJ025 LG1 gb|AC188472.1 NW_001471534.1 Gga1_WGA33_2b1 20,407,077 SJ057 LG1 - NW_001471554.1 Gga1_WGA51_2b1 7,801,901 SJ094 LG1 - NW_001471554.1 Gga1_WGA51_2b1 22,042,793 SJ113 LG1 - NW_001471545.1 Gga1_WGA43_2b1 8,757,200 SJ020 unlinked - NW_001471529.1 Gga1_WGA29_2b1 1,098,266 SJ005 unlinked gb|AC188184.3 NW_001471513.1 Gga1_WGA14_2c1 2,080,202 SJ036 LG2 - NW_001471639.1 Gga2_WGA66_2b2 20,469,429 SJ072 LG2 - NW_001471633.1 Gga2_WGA60_2b2 32,273,874 CK.1B5D LG2 gb|AC225878.2 NW_001471639.1 Gga2_WGA66_2b2 23,539,833 SJ026 LG2 gb|AC206427.2 NW_001471639.1 Gga2_WGA66_2c2 21,465,630 SJ054 LG2 gb|AC188186.2 NW_001471633.1 Gga2_WGA60_2c2 6,229,425 SJ116 LG2 gb|AC148379.2 NW_001471633.1 Gga2_WGA60_2c2 22,279,892 SJ034 unlinked - NW_001471654.1 Gga2_WGA81_2b2 2,075,856 SJ015 LG3 gb|AC188188.2 NW_001471673.1 Gga3_WGA106_2c3 3,458,567 SJ032 LG7 - NW_001471681.1 Gga4_WGA107_2b4 8,679,773 SJ087 LG7 gb|AC155211.2 NW_001471681.1 Gga4_WGA107_2c4 4,015,500 SJ117 LG7 - NW_001471681.1 Gga4_WGA107_2b4 8,679,607 SJ049 LG4 - NW_001471710.1 Gga5_WGA136_2b5 9,314,084 SJ009 LGZ - NW_001488876.1 GgaZ_WGA457_2bZ 1,412,682 SJ101 LG2 gb|AC213969.2 NW_001488849.1 GgaZ_WGA430_2bZ 1,097,987 SJ039 LG1 gb|AC231254.2 NW_001488882.1 GgaZ_WGA463_2cZ 1,315,022 SJ076 LG3 gb|AC188376.1 NW_001488862.1 GgaZ_WGA443_2cZ825,441 SJ050 LG1 gb|AC189030.1 - - - SJ051 LG1 gb|AC189030.1 - - - SJ055 LG1 gb|AC189030.1 - - - SJ064 LG1 gb|AC206426.2 - - - SJ112 LG1 gb|AC192320.2 - - - CK.2A5A LG1 gb|AC188469.1 - - - SJ029 LG4 gb|AC188184.3 - - - SJ033 LG4 gb|AC188469.1 - - - SJ106 LG4 gb|AC188184.3 - - - SJ017 LG5 gb|AC192320.2 - - - SJ041 LG9 gb|AC210531.1 - - - SJ069 LGZ gb|AC188466.2 - - - SJ083 LGZ gb|AC229626.2 - - - a Chicken chromosome number; b Via the clone sequences of the Siberian jay microsatellites; c Via the homologous zebra finch WGS sequences BMC Genomics 2009, 10:1 http://www.biomedcentral.com/1471-2164/10/1 Page 9 of 17 (page number not for citation purposes) Comparison of the whole of all sex-average linkage groups in the Siberian jay and the whole of chicken chromosomesFigure 4 Comparison of the whole of all sex-average linkage groups in the Siberian jay and the whole of chicken chromosomes. 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