MBE Advance Access originally published online on April 13, 2007
Molecular Biology and Evolution 2007 24(7):1537-1552; doi:10.1093/molbev/msm071
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Research Articles |
Gene Order and Recombination Rate in Homologous Chromosome Regions of the Chicken and a Passerine Bird
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* Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, United Kingdom
Department of Animal Ecology, Lund University, Lund, Sweden
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
E-mail: bengt.hansson{at}zooekol.lu.se.
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Abstract |
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Genome structure has been found to be highly conserved between distantly related birds and recent data for a limited part of the genome suggest that this is true also for the gene order (synteny) within chromosomes. Here, we confirm that synteny is maintained for large chromosomal regions in chicken and a passerine bird, the great reed warbler Acrocephalus arundinaceus, with few rearrangements, but in contrast show that the recombination-based linkage map distances differ substantially between these species. We assigned a chromosomal location based on sequence similarity to the chicken genome sequence to a set of microsatellite loci mapped in a pedigree of great reed warblers. We detected homologous loci on 14 different chromosomes corresponding to chicken chromosomes Gga1–5, 7–9, 13, 19, 20, 24, 25, and Z. It is known that 2 passerine macrochromosomes correspond to the chicken chromosome Gga1. Homology of 2 different great reed warbler linkage groups (LG13 and LG5) to Gga1 allowed us to locate the split to a position between 20.8 and 84.8 Mb on Gga1. Data from the 5 chromosomal regions (on Gga1, 2, 3, 5, and Z) with 3 or more homologous loci showed that synteny was conserved with the exception of 2 large previously unreported inversions on Gga1/LG5 and Gga2/LG3, respectively. Recombination data from the 9 chromosomal regions in which we identified 2 or more homologous loci (accounting for the inversions) showed that the linkage map distances in great reed warblers were only 6.3% and 13.3% of those in chickens for males and females, respectively. This is likely to reflect the true interspecific difference in recombination rate because our markers were not located in potentially low-recombining regions: several linkage groups covered a substantial part of their corresponding chicken chromosomes and were not restricted to centromeres. We conclude that recombination rates may differ strongly between bird species with highly conserved genome structure and synteny and that the chicken linkage map may not be suitable, in terms of genetic distances, as a model for all bird species.
Key Words: genome mapping • linkage • microsatellite • passerine • recombination • synteny
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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The genome sequence of the red jungle fowl Gallus gallus, the ancestor of the domestic chicken Gallus domesticus, was recently released (International Chicken Genome Sequencing Consortium 2004
). This facilitated whole-genomic comparisons with the previously sequenced genomes of human and mouse (International Chicken Genome Sequencing Consortium 2004). The release of the chicken sequence is also expected to have important consequences for future research on other bird species (Ellegren 2005). Comparative work on chicken and several passerines has shown that their genome size (Gregory 2007) and karyotype (Shields 1982; Derjusheva et al. 2004; Itoh and Arnold 2005) have been highly conserved despite 80–100 Myr of independent evolution (Shetty et al. 1999). The main cytogenetic alterations detected so far are that chicken chromosome 1 (Gga1) is homologous to 2 passerine macrochromosomes, whereas chicken chromosome 4 (Gga4) is homologous to 1 macrochromosome and 1 microchromosome in passerines (Derjusheva et al. 2004; Itoh and Arnold 2005). Recent comparative data in chicken and the great reed warbler Acrocephalus arundinaceus for parts of chicken chromosomes 2, 3, and 5 (Dawson et al. 2006) and for the Z chromosome in chicken, zebra finch Taeniopygia guttata (Itoh et al. 2006) and collared flycatcher Ficedula albicollis (Backström, Brandstrom, et al. 2006), respectively, also suggest that gene order (synteny) has been highly conserved, with few rearrangements, between these distantly related birds. Together, these results strongly suggest that the physical map of the chicken (International Chicken Genome Sequencing Consortium 2004) can be used as a framework to predict the genome organization in passerines (Ellegren 2005; Dawson et al. 2006). In the context of evolutionary biology, the chicken genome sequence may be of particular value in underpinning molecular-based approaches, such as linkage mapping and quantitative trait loci (QTL) analyses, in passerine birds. Many passerine study systems have already provided significant insights to evolutionary biology, especially in quantitative genetics (Merilä et al. 2001), natural (Richman and Price 1992) and sexual selection (Norris 1993), hybridization (Veen et al. 2001), speciation (Irwin et al. 2001), and development (Abzhanov et al. 2004).
It would be valuable to evaluate not only genome structure and synteny, but also whether recombination rates and linkage map distances have been conserved to the same extent as the genome structure in chicken and passerines, in order to aid the successful design of linkage mapping experiments and QTL analyses in passerines. The linkage map of the chicken (
4,000 cM; Groenen et al. 2000) is somewhat larger in size than in human (3,700 cM; Dib et al. 1996), despite a much smaller genome size in chicken (1.2 x 109 bp in chicken; 3 x 109 bp in human; International Chicken Genome Sequencing Consortium 2004). This results partly from chicken having 16 more chromosomes (38 vs. 22 autosomes), including both macro- and microchromosomes, each with at least one obligate crossing-over during meiosis (i.e., all autosomes, including the microchromosomes, are expected to span at least 50 cM; Rodionov et al. 1992) and partly from a higher recombination rate per base in chicken for chromosomes of similar size (International Chicken Genome Sequencing Consortium 2004; Schmid et al. 2005). At present, it is not known whether the comparatively high recombination rate and large linkage map in relation to genome size in chicken is a general phenomenon in birds. In fact, we may suspect the contrary because the recombination rate is not always strongly conserved between taxa; for example, it varies between human and chimpanzees (Winckler et al. 2005), between different Drosophila species (True et al. 1996), and even between subspecies and strains of Arabidopsis thaliana (Sanchez-Moran et al. 2002).
In the present study, we compare genome structure, synteny, and map distances between a recently derived partial linkage map of a passerine bird, the great reed warbler (Hansson et al. 2005; Åkesson et al. 2007) and homologous chromosomal regions of the chicken (International Chicken Genome Sequencing Consortium 2004; http://pre.ensembl.org/Gallus_gallus/index.html). We have previously compared synteny for a small region of the genome covered by a subset of the markers included in the present study (Dawson et al. 2006). The great reed warbler is a heterochiasmate species with an approximately 2-fold higher rate of recombination in females than in males (Hansson et al. 2005). Although this feature is not shared with chicken, where the sexes have similar recombination rates (Groenen et al. 2000), heterochiasmy is a well-known phenomenon in other species, including human and mouse (Dietrich et al. 1996; Kong et al. 2002; reviewed by Lenormand and Dutheil 2005). Our present comparative genomic analysis of chicken and great reed warblers was possible because several microsatellites that had been mapped in great reed warblers had homologous sequences in the chicken (see below). We assigned a chromosomal location in chicken to microsatellite loci mapped in great reed warblers based on their sequence similarity to the chicken genome sequence by Blast analyses. The rationale was similar to that of Dawson et al. (2006), but in the present study, we were able to use a much larger data set of homologous loci by using data from recently mapped great reed warbler loci and by using refined Blast methods. We first conducted a direct Blast search of the microsatellites to the chicken genome assembly and, second, loci that remained unmapped were matched against National Center for Biotechnology Information's (NCBI's) library of zebra finch T. guttata whole-genome shotgun (WGS) sequences, which in turn were compared against the chicken genome sequence and assigned a chromosomal location in chicken (see below). In the present paper, we were particularly interested in evaluating whether the linkage map of the chicken can serve as a predictor of recombination fractions and linkage map distances in other birds and whether genome structure and synteny have been conserved across a larger proportion of the genome and to identify any major chromosomal rearrangements.
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Materials and Methods |
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Great Reed Warbler Pedigree, Genotyping and Linkage Map
The great reed warbler A. arundinaceus is a large-sized reed warbler of the family Sylviidae (Helbig and Seibold 1999
). The species is a long-distance migrant that winters in Africa and breeds in reed lakes in Eurasia (Bensch 1996; Hansson et al. 2003). Its karyotype is not yet described, but other studied passerines (e.g., chaffinch Fringilla coelebs, blackbird Turdus merula, redwing Turdus iliacus, and zebra finch) have similar numbers of macro- and microchromosomes (2n = 80; Derjusheva et al. 2004; Itoh and Arnold 2005) to chicken (2n = 78; Masabanda et al. 2004). As in all birds, male great reed warblers are homogametic (ZZ), whereas females are heterogametic (ZW).
In the present study, we use linkage map distances from the mapping study of a great reed warbler pedigree population at Lake Kvismaren, southern central Sweden (Åkesson et al. 2007; cf., Hansson et al. 2005), where a detailed ecological study has been ongoing since 1983 (Bensch 1996; Hasselquist 1998; Hansson, Bensch, Hasselquist 2000). All details concerning the pedigree and genotyping can be found in Hansson et al. (2005) and in Åkesson et al. (2007), but for clarity some details are briefly summarized here. Genotypes came from an extended pedigree containing 812 individuals. Alleles of a large number of markers (microsatellites, amplified fragment length polymorphism (AFLPs), indels, and single nucleotide polymorphism (SNP) were polymerase chain reaction (PCR)–amplified and then separated and visualized using an ABI 3100 or an ABI 3730 capillary sequencer (Applied Biosystems, Foster City, CA). Genotypes were analyzed in GENEMAPPER 3.0 (Applied Biosystems). The linkage groups were constructed in CRIMAP 2.4 (Lander and Green 1987). This program calculates 2-point recombination fractions, provides logarithmic odds (LOD) scores for recombination estimates, and tests marker order. We assigned autosomal markers to linkage groups by calculating the recombination fractions between all pairs of markers with the TWOPOINT option in CRIMAP; markers were considered as significantly linked at a threshold of LOD > 3.0. The Z-linked loci were assigned to this linkage group on the basis of every female (being hemizygous, ZW) having only a single allele at codominant loci and on the basis of the segregation patterns in the pedigree for the dominant AFLP markers. We then determined the most parsimonious ordering of groups of linked loci with the options BUILD, FLIPSn, and FIXED. There was pronounced heterochiasmy in great reed warblers, and all map distances were derived from sex-specific analyses (Hansson et al. 2005). Map distances are given in Kosambi centimorgans (cM).
In total, we have genotype data for 62 microsatellite loci in great reed warblers (53 autosomal loci on LG1–LG15; 6 unlinked autosomal loci, and 3 Z-linked loci; see below). In the present study, we used map distances of the most parsimonious map in the most recent great reed warbler mapping analysis, which included data from both microsatellite and AFLP markers and a few indels and SNPs (Åkesson et al. 2007). The map consists of 21 autosomal LGs (LG1–LG21) each with 2–15 markers (in total 53 microsatellite loci and 50 AFLPs) and spans 552 cM in males and 858 cM in females (Åkesson et al. 2007; cf., Hansson et al. 2005). The LGZ consists of 12 markers (3 microsatellites, 3 indels, 1 SNP, and 5 AFLPs) and is 155 cM (Åkesson et al. 2007; cf. Hansson et al. 2005). The updated linkage map (Åkesson et al. 2007) includes 10 new linkage groups (LG12–LG21) compared with the previous microsatellite-based map (Hansson et al. 2005) and includes 3 additional microsatellites (Titgata02, VeCr08, and DkiD124) on LG3, 2 (Pocc8 and Ase13) on LG6, and a few microsatellites on some newly assigned linkage groups (Ase11 on LG12, Ase27 and Ase43 on LG13, Ase57 on LG14, and Sjr4 on LG15). Six autosomal microsatellites [Aar2, Ase16, G7 (=Aar5), Gf08, Lswµ9, and ZL18] are unlinked to all other markers and may be located on unique chromosomes or chromosome arms (Åkesson et al. 2007). The gene order and map distances are similar for most parts of the linkage groups that appear in both Hansson et al. (2005) and Åkesson et al. (2007), but for LG3 (the homologue of Gga2; from here on the chicken chromosomes are referred to by their Gga-number) the gene order of some loci changed when the order was reassessed after adding more markers (Hansson et al. 2005: Gf15–PAT MP 2-43–Ase32–Ase44–PmaTGAn42–Ase10–Pdoµ4–LOX1; Åkesson et al. 2007: 060F–PAT MP 2-43–Gf15–Pdoµ4–Ase10–Titgata02–VeCr08–PmaTGAn42–Ase32–Ase44–DkiD124–LOX1–136G–360A–216C).
Detection of Homologous Single-Copy Chicken–Passerine Sequences
Dawson et al. (2006) conducted Blast analyses of 550 passerine microsatellite sequences, including most loci used in the great reed warbler mapping study of Hansson et al. (2005), on the 1st draft chicken genome sequence (International Chicken Genome Sequencing Consortium 2004; http://www.ncbi.nlm.nih.gov/genome/guide/chicken/). With the Blast settings in Dawson et al. (2006) (the "relaxed sequence similarity search" at an E value <1 x 10–05) it was possible to detect single homologous sequences and thus to predict a single chicken chromosomal location, for 23 great reed warbler microsatellite loci and 4 indels (supplementary appendix 1 in Dawson et al. 2006).
In the present study, we mapped 8 additional markers in the great reed warbler pedigree (Ase13, Ase16, Ase43, DkiD124, Lswµ9, Pocc8, Titgata02, and VeCr08; Åkesson et al. 2007). We also assigned more loci mapped in the great reed warbler pedigree to chicken chromosomes (see below) than did Dawson et al. (2006) for the following reasons. First, we used sequence data for 2 newly published loci (Titgata02 and VeCr08). Second, we obtained sequence data for loci where such data were previously completely missing (PAT MP 2-43, G7 [=Aar5], G61, and Sjr4) and additional sequence data for locus Pdoµ4 where the original sequence data submitted to GenBank was limited. For the former loci (i.e., PAT MP 2-43, G7 [=Aar5], G61, and Sjr4), we amplified the locus, ligated the PCR-amplified product into pUC-based plasmid, and sequenced it in the forward and reverse orientation using M13 primers to obtain a consensus sequence (accession numbers are provided in table 1). The original (shorter) sequence data for locus Pdoµ4 was run through a Blast search but remained unmapped by Dawson et al. (2006). Only the region of sequence between the Pdoµ4 forward and reverse primers had been submitted to European Molecular Biology Laboratory's sequence database (EMBL) (X93505
[GenBank]
—422 bp; Neumann and Wetton 1996), as opposed to the entire sequence of the MboI restriction fragment originally isolated (Neumann 1996). In an attempt to assign a location in the chicken genome for the locus Pdoµ4, the additional sequence data for the MboI restriction fragment was obtained and submitted to EMBL (AM287191
[GenBank]
—538 bp; extra sequence data kindly provided by Neumann K, personal communication; see Neumann 1996). Third, we performed a Blast search of the sequence data against the most recent chicken genome assembly ("WASHU 2.1" released in May 2006; http://pre.ensembl.org/Gallus_gallus/index.html), which has a higher proportion of sequence data assigned to named chromosomes than the previous draft (increase from ca. 85% to ca. 95%), and particularly so for the Z chromosome (increase from 33.6 to 74.6 Mb), so more hits were expected to be assigned to named chromosomes, though it should be noted that no extra sequence data were added in the new chicken genome assembly release. Fourth, for all loci we applied the most relaxed Blast method used in Dawson et al. (2006) previously used for mapping the sex-linked loci: the Ensembl WU-Blast software (Gish W. 1996–2004; http://blast.wustl.edu) using the Ensembl chicken genome browser and the "distant homologies" search setting, that is, the default setting that is optimized for detecting homology between divergent taxa (http://www.ensembl.org/Gallus_gallus/blastview; an important difference to the Blast method used for the autosomal loci in Dawson et al. (2006) is that the word size is lower, 9 instead of 11). We accepted matches that had an E value of <1 x 10–5 and when more than one significant match occurred the best hit had to be <1 x 10–10 and the next nearest hit had to be more than 1 x 10–10 weaker. When the length of a significant match was less than 70 bp, as was the case for locus Pdoµ6 only, we confirmed the match with the method below utilizing homologous zebra finch sequences (table 1). All contaminating vector or linker sequences were identified where possible and removed before the sequences were run through a Blast search. Finally, all loci that could not be directly assigned a location in the chicken genome were mapped using the zebra finch orthologue of the locus. The orthologous zebra finch sequence was identified by performing a cross-species megaBLAST search in NCBI's zebra finch WGS database (http://www.ncbi.nlm.nih.gov/projects/genome/seq/BlastGen/BlastGen.cgi?pid=12898). Matches that had an E value of <1 x 10–5 were accepted. The homologous zebra finch sequences (including their flanks) were much longer (ca. 700–900 bp) than the original microsatellite sequences, and therefore, when matched against the chicken genome (using the Ensembl distant homologies search settings as above), many could be assigned a location in the chicken genome.
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Linkage Map Distances in Chicken
The homologs of the passerine microsatellite loci are not included on the chicken linkage map, and therefore, their genetic map distances were estimated as follows. For each chicken chromosome, we used the publicly available genetic and physical map data of all sequence tagged site (STS) markers (which are mainly microsatellites; http://www.ncbi.nlm.nih.gov/genome/guide/chicken/). In chicken, the recombination rate varies only slightly over the chromosomes (Schmid et al. 2005
). Therefore, we generated a linear regression equation for each chromosome (using linkage map distance as dependent variable and physical map distance as independent variable) and used this to interpolate the genetic map positions for the homologous sequences in chicken. The approximate location of centromeres was based on Schmid et al. (2005). |
Results |
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Homologous Chicken–Great Reed Warbler Sequences
The direct Blast search of the 62 microsatellites and 4 indels mapped in great reed warbler using the Ensembl chicken genome browser (distant homologies search settings; E value of <1 x 10–05) resulted in 37 loci with a single homologous sequence in the chicken genome (table 1). However, the great reed warbler sequence (EMBL accession number: DQ073914 [GenBank] ) of the indel locus CHD1Z-20, which is Z-linked in the great reed warbler, matched a sequence on chicken chromosome "W_random." Because the homologous CHD genes are known to be located on both the W and the Z chromosome in chicken and other birds (e.g., Griffiths and Korn 1997
), we used the location at GgaZ achieved by a Blast of the chicken CHD sequence (EMBL accession number: AF004397
[GenBank]
) and not the match on W_random obtained for the great reed warbler sequence. Two loci, Ase13 and Ase27, had 2 matching chicken sequences (table 1). Ase13 produced significant matches by 2 different parts of the sequences to 2 different named chicken chromosomes. Part of the forward flank matched a Gga5 location and part of the reverse flank matched a location on Gga10 (table 1). A possible explanation for this is that during the cloning and isolation of this locus, one of the flanks was contaminated with an extra Seychelles warbler (Acrocephalus sechellensis) DNA insert at an unidentifiable (blunt-ended) ligation point, and this extra insert maps to a different part of the genome compared with the rest of the sequence. Extra Seychelles warbler (MboI) DNA inserts had been previously recognized and removed in other clones in this genomic library (Ase12 and Ase48; Dawson DA, unpublished data). Locus Ase27 had one matching sequence on Gga1 and the exact same 118 bp sequence region matched chromosome "Unknown" (i.e., an assembly of sequences not yet assigned to chromosome; http://pre.ensembl.org/Gallus_gallus/index.html). Because, the matching sequence on Gga1 and on the Unknown chromosome were 100% identical in terms of base pair composition and many large 100–1000 bp sections of Gga1 are duplicated on the Unknown chromosome, the most probable reason for a duplicate copy on the Unknown chromosome is that the sequence assigned to Gga1 was not removed from the Unknown chromosome when the genome sequence was compiled. Alternatively Ase13 and Ase27 may have been duplicated in the genome, in which case it is difficult to know which loci represent the orthologous ones. For 19 of the 29 loci that remained unmapped after the direct Blast search, we found homologous zebra finch sequences (table 2) using a cross-species megaBLAST search in NCBI's zebra finch WGS database (http://www.ncbi.nlm.nih.gov/projects/genome/seq/BlastGen/BlastGen.cgi?pid=12898). Of these 19 loci, 9 had a single homologous sequence in the chicken genome (table 2). G61 is Z-linked in great reed warblers but the homologous zebra finch sequence mapped to Gga4 (table 2; discussed below). Utilizing the zebra finch sequences did not change the results for Ase13 and Ase27: the flanking regions of Ase13 matched different zebra finch sequences, which in turn mapped to Gga5 and Gga10, respectively, whereas the zebra finch sequence equivalent of Ase27 matched both Gga1 and GgaUnknown (table 2).
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This means that we could use comparative data for 46 of the 66 loci (70%; including CHD1Z-20 and G61, but excluding the potentially duplicated loci Ase13 and Ase27). Note that we do, however, present data for the homologous sequence on Gga1 for Ase27 (table 1; fig. 1). This is because, using the previous chicken genome assembly (draft 1.0), 4 loci each displayed homology to both a named chromosome and the unknown chromosome (Ase11, Ase21, Ase27; supplementary appendix 1 in Dawson et al. [2006
]; and VeCr08), but when blasted against the present chicken genome assembly (draft 2.1), 3 of these (Ase11, Ase21, and VeCr08) produced only a single unique hit to the named chromosome (table 1), suggesting that when sequences are reassigned to a named chromosome during genome assembly they are not always removed from the Unknown chromosome. This suggests that Ase27 may be located at a unique location on chromosome 1; the next release of the chicken genome sequence may resolve this.
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Synteny in Homologous Chicken–Great Reed Warbler Regions
Loci from the same great reed warbler linkage group matched sequences on a single chicken chromosome in the Blast analyses (fig. 1 and table 3), with the exception of locus G61 on LGZ that mapped to Gga4, whereas the other loci on LGZ mapped to GgaZ. Likewise, most loci on the same chicken chromosome matched sequences on a single great reed warbler linkage group (fig. 1 and table 3), with the exceptions of 1) Gga1, represented by 2 great reed warbler linkage groups (LG5 and LG13), 2) Gga4, represented by markers from LG7 and LGZ, and 3) Gga5, represented by markers on LG6 and 2 unlinked markers (fig. 1 and table 3). This result strongly suggests that the chromosome structure has been highly conserved between chicken and passerines.
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Locus Ase27 mapped to one end of Gga1 (and as mentioned above also had a 2nd hit on the GgaUnknown chromosome), whereas the markers forming the linkage group LG5 mapped onto the opposite end of Gga1 (fig. 1 and table 3). This suggests that Ase27 (and locus Ase43 and 4 AFLP markers that together with Ase27 constitute LG13; Åkesson et al. 2007) and LG5 are located on the 2 different passerine macrochromosomes, which, as mentioned above, are both homologous to Gga1 (Derjusheva et al. 2004
; Itoh and Arnold 2005). Thus, the separation of the reported split of Gga1 to form 2 macrochromosomes should be located on Gga1 at a position between 20.8 and 84.8 Mb (between Ase27 and Pdoµ6; fig. 1 and table 3;).
Surprisingly, locus G61, which is Z-linked in great reed warbler, mapped to Gga4. Gga4 is known to be homologous to 1 macrochromosome and 1 microchromosome in passerines (Derjusheva et al. 2004; Itoh and Arnold 2005), but there are no data that suggest that Gga4 has homologous regions in the passerine Z chromosome, which may suggest that this match is spurious. Alternatively, the match is correct and may instead mirror a more complex history of locus G61 (e.g., a duplication, followed by a translocation and a deletion in chicken).
The Blast analysis located Aar2 and Lswµ9 on Gga5 (tables 1 and 3) but these markers were not significantly linked to the markers on LG6 (match Gga5) or with each other in the 2-point analysis (Åkesson et al. 2007). This may be explained by the fact that these markers (Aar2 and Lswµ9) and also other markers on LG6 had few informative meioses and therefore low power in the linkage analyses (Hansson et al. 2005; Åkesson et al. 2007) or that these loci are located in the telomeric region, which may have a higher recombination rate, as found in other species (Nachman and Churchill 1996). Indeed, these 2 loci are located close to the end of Gga5 in chicken (positions 60.3 and 61.2 Mb, respectively; Gga5 has a total size 62.2 Mb; fig. 1). Alternatively, this may indicate that homology has been less conserved for this region of Gga5. In contrast, the chromosomal region of Gga5 from 12.3–49.0 Mb appears to be remarkably well conserved, as indicated by the E values and the conserved synteny for the loci mapped to this region (table 3).
Nine different great reed warbler linkage groups and chicken chromosomes shared at least 2 homologous loci (LG–Gga: 1–3, 3–2, 5–1, 6–5, 8–8, 9–13, 10–9, 11–7, and Z-Z) and, of these, 5 regions shared at least 3 homologous loci (LG–Gga: 1–3, 3–2, 5–1, 6–5, and Z-Z; fig. 1 and table 3). Synteny was fully conserved for both LG1–Gga3 and LG6–Gga5 (fig. 1 and table 3;). LG3–Gga2 showed a large inversion involving at least 48.8 Mb of Gga2; (markers Pdoµ4, Ase10, Titgata02, VeCr08, PmaTGAn42, and Ase32; fig. 2). Within the inversion, synteny was also fully conserved with the exception of locus Titgata02, which was located between Ase10 and VeCr08 in the great reed warbler and between Ase10 and Pdoµ4 in chicken. Note, however, that for Titgata02, the map location assigned based on the mapping of the great reed warbler pedigree is not a single unambiguous location: a 2nd possible position, between Pdoµ4 and Ase10, does not differ significantly from the most parsimonious position between Ase10 and VeCr08 indicated in figure 2 (Åkesson et al. 2007). Thus, we can conclude that synteny was conserved within the inversion for all so-called framework loci with a robust and unambiguous position on the great reed warbler map (i.e., Ase10, VeCr08, PmaTGAn42, and Ase32) and that if Titgata02 was inverted within the inversion then this 2nd inversion was small. A 2nd inversion was detected for LG5–Gga1. Here, a 51.7-Mb region toward the end of Gga1 has been inverted in great reed warblers. There is a striking difference in linkage for markers Pdoµ6 and Ase38 in the 2 species, with very tight linkage in great reed warblers (6.4 cM in males and 0.0 cM in females) and wide separation in chicken (110.8 Mb; fig. 2). This may suggest that the split of Gga1 to form 2 macrochromosomes was followed by additional chromosomal rearrangements. If we ignore locus G61 (and its match to Gga4), there was only slight deviation from synteny for LGZ–GgaZ involving the joint location of the loci BRM-12, BRM-15, and VLDLR9. However, these 3 loci are extremely tightly linked in great reed warblers (within 1 cM; table 3), and their relative ordering is not fully resolved (Åkesson et al. 2007). The most parsimonious ordering provided in table 3 does not differ from the order suggested by the chicken data (Åkesson et al. 2007).
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Linkage Map Distances in Chicken and Great Reed Warblers
Available linkage map and sequence position data for 479 chicken STS markers were analyzed with linear regression to interpolate the linkage map positions for the homologous chicken sequences (table 3). Three of the 479 STSs were obvious outliers (detected by studentized residual test and by eye) in the linear regression analyses (locus–chromosome: LEI0138–Gga1, ADL0314–Gga1, and MCW0324–Gga2) and were therefore excluded from the data set before calculating regression lines. In total, we used data from 476 STSs on the 9 chromosomes (ranging from 19 STSs on Gga9 to 141 STSs on Gga1) to calculate regression lines and for estimating map positions of the homologous loci (table 3). The homologous regions covered between 5% (LG11–Gga7) and 66% (LG1–Gga3 and LG3–Gga2) of their respective chicken chromosome lengths (table 3, fig. 3).
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Our result shows that the recombination-based linkage map distances were substantially smaller in great reed warblers than in chicken (table 3 and fig. 3). The summed map distance of male (58 cM) and female (111 cM) great reed warblers was only 6.3% and 13.3% of that of the chicken in the homologous chromosomal regions (915 cM in males and 830 cM in females; table 2 and fig. 3). The great reed warbler had smaller map distance than chicken in all 9 chromosome comparisons (table 3), and the pattern was significant for both male and female great reed warbler map distance data (paired t-test: males, t = 3.40, degree of freedom [df] = 8, P = 0.009; females, t = 2.99, df = 7, P = 0.020). The inversion on LG3–Gga2 did not affect the recombination rate analysis because there were informative noninverted markers flanking both sides of it at either end of the chromosome (PAT MP 2-43 and Gf15, and Ase44 and LOX1, respectively; table 3); and for LG5–Gga1, we use data for the inverted region (table 3 and fig. 3).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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We have conducted comparative gene mapping in great reed warblers and chicken by using data from 46 of the 66 loci (70%) mapped in great reed warblers. As previously suggested from a smaller data set of homologous chicken–great reed warbler loci (Dawson et al. 2006
), our results confirm that genome structure and synteny have been remarkably conserved between chicken and great reed warblers, with the exception of the newly identified rather large inversions on LG3–Gga2 and LG5–Gga1. However, there are as yet large regions of the genome to be comparatively analyzed including the entirety of Gga6 and the regions of poor coverage across the chromosomes 1, 4, 7, and 8. Moreover, we are with the present low-density map unlikely to detect small-scale inversions. It therefore seems likely that future studies will identify other large- and small-scale inversions in passerines and chicken.
Loci from the same great reed warbler linkage groups matched sequences on a single chicken chromosome in the Blast analyses (with the exception of Ase13 on LG6 that had a match to both Gga5 and Gga10 and Ase27 on LG13 that mapped to both Gga1 and GgaUnknown). Likewise, most loci on the same chicken chromosome matched sequences on a single great reed warbler linkage group, with the exception of the following 1) chromosome Gga1, which was, if we consider the homologous sequence on Gga1 for Ase27, represented by 2 great reed warbler linkage groups (LG5 and LG13), 2) Gga4, represented by markers from LG7 and LGZ, and 3) Gga5, represented by markers on LG6 and 2 unlinked markers. This result strongly suggests that the chromosome structure has been highly conserved between chicken and passerines. Synteny was fully conserved for both LG1–Gga3 and LG6–Gga5 and possibly for LGZ–GgaZ. For LG3–Gga2, we detected a previously unknown large inversion, involving 6 loci and at least 48.8 Mb up to 81.5 Mb (32–53%) (fig. 2). Four of the 6 inverted great reed warbler loci (Ase10, VeCr08, PmaTGAn42, and Ase32) and 2 flanking loci on each side of the inversion (060F and Gf15, and LOX1 and 136G, respectively) have unambiguous map locations and are so-called framework loci (Åkesson et al. 2007). A 2nd inversion was detected for LG5–Gga1. Here a 51.7-Mb region near the end of Gga1 has been inverted in great reed warblers. We can rule out the possibility that these inversions were due to errors in the assembly of the chicken genome sequence because the sequence orientation was supported by the order of the STSs on the chicken linkage map. The detected inversions suggest that one may expect occasional intrachromosomal rearrangements between chicken and passerines, in addition to the already-described main cytogenetic alterations (i.e., that Gga1 is homologous to 2 passerine macrochromosomes and that Gga4 is homologous to 1 macrochromosome and 1 microchromosome in passerines; Derjusheva et al. 2004; Itoh and Arnold 2005).
Because only one marker on LG7 mapped to Gga4, we were unable to identify the location of the split of this chromosome into 2 passerine chromosomes. If we accept the match of Ase27 to Gga1, our result identifies the region where Gga1 splits into 2 macrochromosomes to be between 20.8 and 84.8 Mb, and adding new markers will provide the potential to pinpoint more precisely where this split has occurred. In addition, the detected inversion on LG5–Gga1 may suggest that the split of Gga1 was followed by additional chromosome rearrangements. Two markers at the end of Gga5 in chicken are unlinked to the other markers on this chromosome (LG6) in great reed warblers, which may suggest that the end of Gga5 (60.3–61.2 Mb region) comprises a separate passerine microchromosome. Alternatively, linkage between these markers and markers on LG6 could not be verified because these loci had few informative meioses and consequently low statistical power (Hansson et al. 2005; Åkesson et al. 2007) or because they were located very close to the telomere (which is the case in chicken; see fig. 1), which may have a higher recombination rate, as found for telomeric markers in other species, for example, Drosophila (Nachman and Churchill 1996).
There are so far no comparable data available for the autosomes of other passerine species, but 2 independent studies have recently conducted comparative analyses of the Z chromosome in chicken and zebra finch T. guttata (Itoh et al. 2006) and collared flycatcher F. albicollis (Backström, Brandstrom, et al. 2006), respectively. In accordance with our present findings, there was a high degree of synteny between chicken and each of these passerines, with few rearrangements (one in each comparison). As in our study, Backström, Brandstrom, et al. (2006) compare passerine linkage map data to chicken sequence data. However, they used data from a previous chicken genome assembly (draft 1.1), which differed substantially, particularly so for the Z chromosome, from the recently released assembly (draft 2.1) used in the present study. This complicates a direct comparison between their and our results for this chromosome, although the high degree of synteny in both studies supports our conclusions of conserved synteny.
We observed that there is variation between chromosomes in the number of loci being mapped and, for instance, not a single locus was mapped on Gga6 and relatively few loci on Gga1, 4, 7, and 8 (see fig. 1). In contrast, both Gga2 and Gga5 have a high number of mapped markers per base pair of sequence. It is possible that the number of loci mapped per base pair of sequence indicates which regions of the genome are more conserved and that the strength (E value) of the Blast hits may show how strongly each region is conserved between chicken and passerine. In regions where more sequence variation between passerine and chicken has been observed, it may be acceptable to reduce the word size (W) in future Blast analyses to enable more markers to be mapped. For example, an Ensembl Blast search for the Darwin's finch (Geospiza fortis) microsatellite sequence for locus Gf15 in the chicken genome that used the distant homologies settings and a word size of 6 instead of 9 enabled the chromosomal location for this locus to be identified on Gga2 at 43.5 Mb with a confident E value of 4 x 10-10. This location is in agreement with the assigned location that we obtained by identifying a longer homologous zebra finch genome sequence and comparing this with chicken (table 2). Because it is not always possible to identify an homologous zebra finch sequence, reducing the word length to assign a chromosomal location locus is a useful approach. However, changing the Blast settings to lower the threshold should be done with caution because this increases the risk of including non-homologous loci in the analyses.
Our results clearly show that the great reed warbler has substantially shorter linkage map distances than chicken at the compared homologous chromosomal regions. This contrast is probably a result of a true interspecific difference in recombination rate, but first we have to rule out some obvious alternative explanations. It may be hypothesized that the detected difference was caused simply by the linkage groups being located in low-recombining parts of the great reed warbler genome, such as the centromeres (Hulten 1974; Lynn et al. 2000). We may expect such a bias in this type of analysis because linkage between typed markers is most readily detected when the recombination rate is low. However, against this hypothesis, several of the linkage groups covered a substantial part of their corresponding chicken chromosomes (up to 66%; table 3) and were not restricted to centromeres (figs. 1 and 3). Another possible explanation for the observed differences in recombination rate is that the great reed warbler has a substantially smaller genome than chicken. However, although we cannot rule out this possibility completely, it is difficult to imagine a 5 to 10-fold genome reduction in the great reed warbler without the loss of too many functionally important genes, especially considering that chicken already has a comparatively compact genome (1.25 pg; Gregory 2007). Moreover, the genome sizes of 62 other passerine species studied so far (mean 1.37 pg; range 1.04–1.93 pg; the 4 species of Sylviidae range between 1.09–1.47 pg) are comparable to or at least not much smaller than that of chicken (Gregory 2007).
Cytological work in many species suggests that each chromosome will have at least one chiasma for efficient chromosome pairing and segregation (Rodionov et al. 1992). Although there are exceptions to this general picture, most notably the lack of recombination in Drosophila males, species with at least some recombination seem to have at least one chiasma per chromosome. This is the case in chicken, which means that all chromosomes (except the W chromosome) are expected to span approximately 50 cM (Rodionov et al. 1992; Ellegren 2005; Schmid et al. 2005; Groenen MAM, personal communication), and explains why microchromosomes have a much higher recombination rate per base pair than the macrochromosomes (International Chicken Genome Sequencing Consortium 2004). If this applies also to great reed warblers, then each linkage group should be 50 cM or larger. This would imply that the microchromosomes may be of similar length and have similar high rate of recombination in the 2 species. Nevertheless, it appears safe to conclude that the contrasting genetic map distances for the macrochromosomes (table 3 and fig. 3) result from true interspecific differences in recombination rate. This is not a controversial result because research on other taxa has shown that the recombination rates sometimes differ substantially, even between closely related species and subspecies (True et al. 1996; Sanchez-Moran et al. 2002; Winckler et al. 2005).
One may ask why these 2 bird species with strongly conserved genome structure and highly maintained synteny have such a pronounced difference in recombination rate for the macrochromosomes. The chicken mapping families almost all originate from domesticated lines that have undergone several generations of strong directional selection; one mapping family was derived from a backcross between a partially inbred jungle fowl line and a highly inbred white leghorn line, whereas the other 2 families were derived from highly inbred lines (Groenen et al. 2000). The domestication process and inbreeding may select for high recombination. Some recombination rate models predict a higher recombination rate in inbred populations, and it has been observed cytologically that inbreeding plant species can have greater chiasma frequency compared with outcrossing relatives (reviewed in Charlesworth et al. 1977, 1979). However, if inbreeding selected for a rapid increase in the recombination rate in chicken, one might expect the different families used in the mapping analyses to differ more in map size than they actually did (Groenen et al. 2000). Moreover, a previous study comparing inbreeding and outcrossing species (A. thaliana and A. lyrata) detected only slightly higher rates of recombination in the inbreeder (Hansson et al. 2006). Thus, although a hypothesis based on selection for increased rate of recombination during domestication in chicken may explain our observation, alternative hypotheses cannot be excluded. For instance, high diversity (i.e., greater sequence differences between alleles) in outbred populations has been suggested to inhibit recombination (Borts and Haber 1987). However, even though one may expect low sequence diversity in chicken due to directional selection during domestication, this hypothesis cannot be tested until comparable sequence data have been gathered in both species. Also, even though the great reed warbler currently has a very large population size, suggesting it could harbor extensive sequence diversity, data from both mitochondrial and nuclear genes suggest that its long-term population size is much smaller, and its genetic diversity reduced because of population contractions during the last, and probably previous, glaciations (Bensch and Hasselquist 1999; Hansson and Richardson 2005). Another scenario is that the processes causing the pronounced heterochiasmy in great reed warblers (Hansson et al. 2005) have simultaneously caused a general decline in recombination rate. Unfortunately, this hypothesis is also difficult to test because it is based on, and requires, estimates of haploid selection pressures and selection on imprinted genes (Lenormand and Dutheil 2005).
As mentioned above, the linkage maps of chicken and human are of similar size (4000 cM in chicken, Groenen et al. [2000]; 3700 cM in Human, Dib et al. [1996]), despite a much smaller genome size in chicken (1.2 x 109 bp in chicken and 3 x 109 bp in human; International Chicken Genome Sequencing Consortium 2004). This results partly from chickens having more chromosomes, each with at least one obligate crossing-over during meiosis (Rodionov et al. 1992), and partly from a higher recombination rate per base in chicken (International Chicken Genome Sequencing Consortium 2004; Schmid et al. 2005). Edwards and Dillon (2004) studied recombination in the red-winged blackbird Agelaius phoeniceus within a restricted region of the chromosome corresponding to Gga16 (a microchromosome). The evaluation of the per-site recombination rate suggested that recombination in blackbirds is up to 2 orders of magnitude higher than in humans, resembling those in Drosophila (and then also chicken) more than those in humans (Edwards and Dillon 2004). However, studies of fine-scale recombination rate in human, for instance, have shown that the presence of recombination hotspots makes it difficult to predict the large-scale pattern of recombination from that deduced at the smaller scale (Nachman 2002; Ptak et al. 2004; Winckler et al. 2005). Furthermore, the recombination rate may differ substantially between the macro- and microchromosomes, so it remains to be evaluated whether the result applies also to the macrochromosomes. Moreover, the blackbird study explored sequence and haplotype based data with a coalescent approach and the resulting estimates of recombination rate depend on assumptions about parameters that are difficult to estimate, such as coalescence time and effective population size (Edwards and Dillon 2004). It is therefore too early to conclude that the overall recombination rate in red-winged blackbirds is comparable to the high levels found in chicken.
Instead, our data suggest that recombination rates differ between some bird species and that the chicken linkage map may not be suitable, in terms of genetic distances, as a model for all bird species. If other passerines also have as low a recombination rate (this study) and as pronounced heterochiasmy (Hansson et al. 2005) as the great reed warbler, it will be easier to build basic linkage maps in this group than if recombination were as frequent as in chicken. Relatively few markers will be needed to cover the total genome sufficiently. For instance, the 9 homologous regions, which can be mapped by less than 41 microsatellites in great reed warblers, correspond to a total of 317 Mb in chicken (table 3). This implies a coverage of 44% for these 7 chromosomes (317 Mb of a total of 721 Mb) and of 26% for the whole genome in chicken (317 Mb of a total of 1,200 Mb). However, a low recombination rate also implies some restrictions. For instance, in the context of parentage analyses and marker-based inbreeding analyses it is crucial to use independent loci. If markers are picked randomly, a low recombination rate will increase the risk of cosegregation. This problem may be circumvented by using chicken sequence data to design primers to amplify polymorphisms at predicted locations of the genome, for example, on different chromosomes or chromosome arms (Ellegren 2005; Dawson et al. 2006). In QTL analyses, a low recombination rate would facilitate the work initially by increasing the amount of information per marker and thereby increase the probability to detect QTLs (Lynch and Walsh 1998). However, once a QTL has been detected, little can be concluded about the number and position of the underlying functional genes because their true locations may be dispersed over a large part of the chromosome due to the imprecision of genetic mapping.
The low recombination rate in great reed warblers is interesting in light of the previously detected association between marker-based heterozygosity and variation in fitness-associated traits in the species (Hansson et al. 2001, 2004). This heterozygosity–fitness correlation was hypothesized to be caused by relatively high levels of linkage disequilibrium in the study population (Hansson et al. 2004) and not by partial inbreeding (cf. Hansson and Westerberg 2002; Slate et al. 2004). Preliminary analyses (Hansson B, Csilléry K, unpublished data) suggest that the level of linkage disequilibrium in the great reed warbler is comparable to the high levels detected in some extremely bottlenecked populations, such as the Scandinavian wolf population (Bensch et al. 2006) and in some domesticated species (McRae et al. 2002; Sutter et al. 2004), rather than those in human and other wild bird and wild mammal populations (Dunning et al. 2000; Winckler et al. 2005; Backström, Qvarnstrom, et al. 2006). One possibility is that the strong linkage disequilibrium observed in the studied great reed warbler population was caused by the species' recent bottleneck-and-expansion in the region (Hansson et al. 2004). A low recombination rate will maintain linkage disequilibrium also between loci separated by relatively large physical distances, thus increasing the possibility that a locus will be a marker for linked fitness loci. Low recombination rate could also lead to a general depletion of the nucleotide diversity, for example, due to background selection, hitchhiking, or a combination of these processes. A correlation between recombination rate and nucleotide diversity has been demonstrated for a variety of organisms, from plants to humans (e.g., Begun and Aquadro 1992; Kraft et al. 1998; Nachman 2001), which points to the joint effects of linkage and selection in shaping patterns of genetic variation (Nachman 2002).
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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We would like to thank S. Bensch and D. Hasselquist for initiating the great reed warbler project, all field workers at Lake Kvismaren for their efforts, T. Thomasson for genotyping, G. Horsburgh and K. Neumann for providing sequence data, D. Charlesworth for discussion and references, and Scott Edwards and reviewers for comments. The work was supported by a postdoctoral grant from the Swedish Research Council (to B.H.), by a Marie-Curie postdoctoral fellowship (to B.H. and J.M.P.), the Natural Environmental Research Council, UK (to D.A.D. and T.B. and to LEB Kruuk, J.M.P. and B.H.), Lunds Djurskyddsfond (to B.H.), Berggrens Stiftelse (to B.H.), Schwartz Stiftelse (to B.H.), and Kvismare Bird Observatory (report number 143).
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Scott Edwards, Associate Editor
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
|---|
Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ. Bmp4 and morphological variation of beaks in Darwin's finches. Science (2004) 305:1462–1465.
Åkesson M, Hansson B, Hasselquist D, Bench S. Linkage mapping of AFLP markers in a wild population of great reed warblers: importance of heterozygosity and number of genotyped individuals. Mol Ecol (2007) doi:10.1111/j.1365-294X.2007.03290.x.
Backström N, Brandstrom M, Gustafsson L, Qvarnstrom A, Cheng H, Ellegren H. Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome. Genetics (2006) 174:377–386.
Backström N, Qvarnstrom A, Gustafsson L, Ellegren H. Levels of linkage disequilibrium in a wild bird population. Biol Lett (2006) 2:435–438.
Begun DJ, Aquadro CF. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature (1992) 356:519–520.[CrossRef][Medline]
Bensch S. Female mating status and reproductive success in the great reed warbler: is there a potential cost of polygyny that requires compensation? J Anim Ecol (1996) 65:283–296.[CrossRef]
Bensch S, Andrén H, Hansson B, Pedersen HC, Sand H, Sejberg D, Wabakken P, Åkesson M, Liberg O. Selection for heterozygosity gives hope to a wild population of inbred wolves. PLoS One (2006) e72:1–7.
Bensch S, Hasselquist D. Phylogeographic population structure of great reed warblers: an analysis of mtDNA control region sequences. Biol J Linn Soc (1999) 66:171–185.[CrossRef][Web of Science]
Bensch S, Price T, Kohn J. Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol Ecol (1997) 6:91–92.[CrossRef][Medline]
Borts RH, Haber JE. Meiotic recombination in yeast: alteration by multiple heterozygosities. Science (1987) 237:1459–1465.
Charlesworth D, Charlesworth B, Strobeck C. Effects of selfing on selection for recombination. Genetics (1977) 68:213–226.
Charlesworth D, Charlesworth B, Strobeck C. Selection for recombination in self-fertilising species. Genetics (1979) 93:237–244.
Dawson DA, Burke TA, Hansson B, Pandhal J, Hale MC, Hinten GN, Slate J. A predicted microsatellite map of the passerine genome based on chicken-passerine sequence homology. Mol Ecol (2006) 15:1299–1320.[CrossRef][Medline]
Degnan SM, Robertson BC, Clegg SB, Moritz CC. Microsatellite primers for studies of gene flow and mating systems in white-eyes (Zosterops). Mol Ecol (1999) 8:159–160.[CrossRef][Medline]
Derjusheva S, Kurganova A, Habermann F, Gaginskaya E. High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res (2004) 12:715–723.[CrossRef][Web of Science][Medline]
Dib C, Faure S, Fizames C. (14 co-authors). A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature (1996) 380:152–154.[CrossRef][Medline]
Dietrich WF, Miller J, Steen R. (20 co-authors). A comprehensive genetic map of the mouse genome. Nature (1996) 380:149–152.[CrossRef][Medline]
Double MC, Dawson D, Burke T, Cockburn A. Finding the fathers in the least faithful bird: a microsatellite-based genotyping system for the superb fairy-wren Malurus cyaneus. Mol Ecol (1997) 6:691–693.[CrossRef]
Dunning AM, Durocher F, Healey CS, et al. The extent of linkage disequilibrium in four populations with distinct demographic histories. Am J Hum Genet (2000) 67:1544–1554.[CrossRef][Web of Science][Medline]
Edwards SV, Dillon M. Hitchhiking and recombination in birds: evidence from Mhc-linked and unlinked loci in red-winged blackbirds (Agelaius phoeniceus). Genet Res (2004) 84:175–192.[CrossRef][Web of Science][Medline]
Ellegren H. The avian genome uncovered. Trends Ecol Evol (2005) 20:180–186.[CrossRef][Medline]
Frentiu FD, Lange CL, Burke T, Owens IPF. Isolation of microsatellite loci in the Capricorn silvereye, Zosterops lateralis chlorocephalus (Aves: Zosteropidae). Mol Ecol Notes (2003) 3:462–464.[CrossRef][Web of Science]
Gibbs HL, Tabak LM, Hobson K. Characterization of microsatellite DNA loci for a neotropical migrant songbird, the Swainson's thrush (Catharus ustulatus). Mol Ecol (1999) 8:1551–1552.[CrossRef][Medline]
Gregory TR. Animal genome size database [Internet] (2007) Available from: http://www.genomesize.com. Accessed 21 May 2007.
Griffiths R, Korn RM. A CHD1 gene is Z chromosome linked in the chicken Gallus domesticus. Gene (1997) 197:225–229.[CrossRef][Web of Science][Medline]
Groenen MAM, Cheng HH, Bumstead N. (15 co-authors). A consensus linkage map of the chicken genome. Genome Res (2000) 10:137–147.
Hanotte O, Zanon C, Greig C, Dixon A, Burke T. Isolation and characterization of microsatellite loci in a passerine bird: the reed bunting Emberiza schoeniclus. Mol Ecol (1994) 3:529–530.[Medline]
Hansson B, Åkesson M, Slate J, Pemberton JM. Linkage mapping reveals sex-dimorphic map distances in a passerine bird. Proc R Soc B (2005) 272:2289–2298.[Medline]
Hansson B, Bensch S, Hasselquist D. Patterns of nest predation contribute to polygyny in the great reed warbler. Ecology (2000) 81:319–328.[CrossRef][Web of Science]
Hansson B, Bensch S, Hasselquist D, Åkesson M. Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc R Soc B (2001) 268:1287–1291.[Medline]
Hansson B, Bensch S, Hasselquist D, Lillandt B-G, Wennerberg L, von Schantz T. Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol Ecol (2000) 9:1529–1538.[CrossRef][Medline]
Hansson B, Gavrilov E, Gavrilov A. Hybridisation between great reed warblers Acrocephalus arundinaceus and clamorous reed warblers A. stentoreus: morphological and molecular evidence. Avian Sci (2003) 3:145–151.
Hansson B, Kawabe A, Preuss S, Kuittinen H, Charlesworth D. Comparative gene mapping in Arabidopsis lyrata chromosomes 1 and 2 and the corresponding A. thaliana chromosome 1: recombination rates, rearrangements and centromere location. Genet Res (2006) 87:75–85.[CrossRef][Web of Science][Medline]
Hansson B, Richardson DS. Genetic variation in two endangered Acrocephalus species compared to a widespread congener: estimates based on functional and random loci. Anim Conserv (2005) 8:83–90.[CrossRef]
Hansson B, Westerberg L. On the correlation between heterozygosity and fitness in natural populations. Mol Ecol (2002) 11:2467–2474.[CrossRef][Medline]
Hansson B, Westerdahl H, Bensch S, Hasselquist D, Åkesson M. Does linkage disequilibrium generate heterozygosity-fitness correlations in great reed warblers? Evolution (2004) 58:870–879.[CrossRef][Web of Science][Medline]
Hasselquist D. Polygyny in the great reed warbler: a long-term study of factors contributing to male fitness. Ecology (1998) 79:2376–2390.[CrossRef][Web of Science]
Helbig AJ, Seibold I. Molecular phylogeny of the Palearctic-African Acrocephalus and Hippolais warblers (Aves: Sylviidae). Mol Phylogenet Evol (1999) 11:246–260.[CrossRef][Web of Science][Medline]
Hulten M. Chiasma distribution at diakinesis in normal human male. Hereditas (1974) 76:55–78.[Web of Science][Medline]
International Chicken Genome Sequencing Consortium. Sequencing and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature (2004) 432:695–716.[CrossRef][Medline]
Irwin DE, Bensch S, Price TD. Speciation in a ring. Nature (2001) 409:333–337.[CrossRef][Medline]
Ishibashi Y, Mikami O, Abe S. Isolation and characterization of microsatellite loci in the Japanese marsh warbler Locustella pryeri. Mol Ecol (2000) 9:373–375.[CrossRef][Medline]
Itoh Y, Arnold AP. Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res (2005) 13:47–56.[CrossRef][Web of Science][Medline]
Itoh Y, Kampf K, Arnold AP. Comparison of the chicken and zebra finch Z chromosomes shows evolutionary rearrangements. Chromosome Res (2006) 14:805–815.[CrossRef][Web of Science][Medline]
King TL, Eackles MS, Henderson AP, Bocetti CI, Currie D, Wunderle JM Jr. Microsatellite DNA markers for delineating population structure and kinship among the endangered Kirtland's warbler (Dendroica kirtlandii). Mol Ecol Notes (2005) 5:569–571.[CrossRef][Web of Science]
Kong A, Gudbjartsson DF, Sainz J. (16 co-authors). A high-resolution recombination map of the human genome. Nat Genet (2002) 31:241–247.[CrossRef][Web of Science][Medline]
Kraft T, Sall T, Magnusson-Rading I, Nilsson NO, Hallden C. Positive correlation between recombination rates and levels of genetic variation in natural populations of sea beet (Beta vulgaris subsp. maritima). Genetics (1998) 150:1239–1244.
Lander ES, Green P. Construction of multilocus genetic-linkage maps in humans. Proc Natl Acad Sci USA (1987) 84:2363–2367.
Lenormand T, Dutheil J. Recombination difference between sexes: a role for haploid selection. PLoS Biol (2005) 3:e63.[CrossRef][Medline]
Lynch M, Walsh B. Genetics and analysis of quantitative traits (1998) Sunderland (MA): Sinauer Associates, Inc.
Lynn A, Kashuk C, Petersen MB, Bailey JA, Cox DR, Antonarakis SE, Chakravarti A. Patterns of meiotic recombination on the long arm of human chromosome 21. Genome Res (2000) 10:1319–1332.
Martinez JG, Soler JJ, Soler M, Møller AP, Burke T. Comparative population structure and gene flow of a brood parasite, the great spotted cuckoo (Clamator glandarius), and its primary host, the magpie (Pica pica). Evolution (1999) 53:269–278.[CrossRef][Web of Science]
Masabanda JS, Burt DW, O'Brien PCM. (15 co-authors). Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics (2004) 166:1367–1373.
McRae SB, Amos W. Characterization of hypervariable microsatellites in the cooperatively breeding white-browed sparrow weaver Plocepasser mahali. Mol Ecol (1999) 8:903–904.[Medline]
McRae AF, McEwan JC, Dodds KG, Wilson T, Crawford AM, Slate J. Linkage disequilibrium in domestic sheep. Genetics (2002) 160:1113–1122.
Merilä J, Kruuk LEB, Sheldon BC. Cryptic evolution in a wild bird population. Nature (2001) 412:76–79.[CrossRef][Medline]
Nachman MW. Single nucleotide polymorphisms and recombination rate in humans. Trends Genet (2001) 17:481–485.[CrossRef][Web of Science][Medline]
Nachman MW. Variation in recombination rate across the genome: evidence and implications. Curr Opin Genet Dev (2002) 12:657–663.[CrossRef][Web of Science][Medline]
Nachman MW, Churchill GA. Heterogeneity in rates of recombination across the mouse genome. Genetics (1996) 142:537–548.[Abstract]
Neumann K. Isolation and characterization of microsatellite markers in the house sparrow (Passer domesticus L). [PhD thesis] (1996) Nottingham (UK): University of Nottingham.
Neumann K, Wetton JH. Highly polymorphic microsatellites in the house sparrow Passer domesticus. Mol Ecol (1996) 5:307–309.[CrossRef][Medline]
Nishiumi I, Yamagishi S, Maekawa H, Shimoda C. Paternal expenditure is related to brood sex ratio in polygynous great reed warblers. Behav Ecol Sociobiol (1996) 39:211–217.[CrossRef][Web of Science]
Norris K. Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature (1993) 362:537–539.[CrossRef][Web of Science]
Otsuka R, Nishiumi I, Wada M. Characterization of 12 polymorphic microsatellite loci in the Japanese bush warbler Cettia diphone. Mol Ecol Notes (2003) 3:44–46.[CrossRef][Web of Science]
Otter K, Ratcliffe L, Michaud D, Boag PT. Do female black-capped chickadees prefer high-ranking males as extra-pair partners? Behav Ecol Sociobiol (1998) 43:25–36.[CrossRef][Web of Science]
Petren K. Microsatellite primers from Geospiza fortis and cross-species amplification in Darwin's finches. Mol Ecol (1998) 7:1782–1784.[Medline]
Piertney SB, Marquiss M, Summers R. Characterization of tetranucleotide microsatellite markers in the Scottish crossbill (Loxia scotica). Mol Ecol (1998) 7:1261–1263.[Medline]
Primmer CR, Møller AP, Ellegren H. Resolving genetic relationship with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol Ecol (1995) 4:493–498.[Medline]
Ptak SE, Roeder AD, Stephens M, Gilad Y, Pääbo S, Przeworski M. Absence of the TAP2 human recombination hotspot in chimpanzees. PLoS Biol (2004) 2:e155.[CrossRef][Medline]
Richardson DS, Jury FL, Dawson DA, Salgueiro P, Komdeur J, Burke T. Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol Ecol (2000) 9:2226–2231.[Medline]
Richman AD, Price T. Evolution of ecological differences in the Old World leaf warblers. Nature (1992) 355:817–821.[CrossRef][Medline]
Rodionov AV, Chelysheva LA, Solovei IV, Miakoshina YA. Chiasma distribution in the lampbrush chromosomes of the chicken Gallus gallus domesticus: hot spots of recombination and their possible role in proper dysjunction of homologous chromosomes at the first meiotic division. Genetika (1992) 28:151–160.[Web of Science][Medline]
Saladin V, Bonfils D, Binz T, Richner H. Isolation and characterization of 16 microsatellite loci in the great tit Parus major. Mol Ecol Notes (2003) 3:520–522.[CrossRef][Web of Science]
Sanchez-Moran E, Armstrong SJ, Santos JL, Franklin FC, Jones GH. Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics (2002) 162:1415–1422.
Schmid M, Nanda I, Hoehn H. (42 co-authors). Second report on chicken genes and chromosomes 2005. Cytogenet Genome Res (2005) 109:415–479.[CrossRef][Web of Science][Medline]
Shetty S, Griffin DK, Graves JA. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res (1999) 7:289–295.[CrossRef][Web of Science][Medline]
Shields GF. Comparative avian cytogenetics. Condor (1982) 84:45–58.
Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE, McEwan JC. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity (2004) 93:255–265.[CrossRef][Web of Science][Medline]
Stenzler LM, Fraser R, Lovette IJ. Isolation and characterization of 12 microsatellite loci from golden-winged warblers (Vermivora chrysoptera) with broad cross-taxon utility in emberizine songbirds. Mol Ecol Notes (2004) 4:602–604.[CrossRef][Web of Science]
Sutter NB, Eberle MA, Parker HG, Pullar BJ, Kirkness EF, Kruglyak L, Ostrander EA. Extensive and breed-specific linkage disequilibrium in Canis familiaris. Genome Res (2004) 14:2388–2396.
True JR, Mercer JM, Laurie CC. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics (1996) 142:507–523.[Abstract]
Veen T, Borge T, Griffith SC, Saetre GP, Bures S, Gustafsson L, Sheldon BC. Hybridization and adaptive mate choice in flycatchers. Nature (2001) 411:45–50.[CrossRef][Medline]
Wang MT, Hsu YC, Yao CT, Li SH. Isolation and characterization of 12 tetranucleotide repeat microsatellite loci from the green-backed tit (Parus monticolus). Mol Ecol Notes (2005) 5:439–442.[CrossRef][Web of Science]
Winckler W, Myers SR, Richter DJ. (11 co-authors). Comparison of fine-scale recombination rates in humans and chimpanzees. Science (2005) 308:107–111.
Winker K, Glenn TC, Graves GR. Dinucleotide microsatellite loci in a migratory wood warbler (Parulidae: Limnothlypis swainsonii) and amplification among other songbirds. Mol Ecol (1999) 8:1553–1556.[CrossRef]
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