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

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

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

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

Genetic maps are available for turkey (Reed et al. 2005) and quail (Kayang et al. …