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

Abstract

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

Extensive linkage disequilibrium in a wild bird population

“…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][5][6][7][8], estimation of the extent of linkage disequilibrium [9,10], and syntenic comparison between related species [7,8,[11][12][13][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.…”

The genomic landscape of species divergence in Ficedula flycatchers

“…The naturally hybridizing collared flycatcher and pied flycatcher are important avian speciation models [2][3][4][5][6][7] that show pre-as well as postzygotic isolation 8,9 . We sequenced and assembled the 1.1-Gb flycatcher genome, physically mapped the assembly to chromosomes using a low-density linkage map 10 and re-sequenced population samples of each species. Here we show that the genomic landscape of species differentiation is highly heterogeneous with approximately 50 'divergence islands' showing up to 50-fold higher sequence divergence than the genomic background.…”

“…The sequenced bird was heterozygous at 3.66 million positions, corresponding to an average of one segregating site every 330 bp. A lowdensity linkage map of collared flycatcher 10 anchors 73% of the assembly to chromosomes and orients scaffolds along them ( Supplementary Fig. 3).…”

“…However, avian microchromosomes are generally acro-or telocentric 18 . An attempt to approximate the location of centromeres on flycatcher macrochromosomes was made using information on the location of centromeres in the karyotype of zebra finch, coupled with the high degree of flycatcher-zebra-finch synteny conservation 10 ( Supplementary Fig. 4).…”

Speciation genetics

“…In brief, the 1.13 Gb flycatcher genome was assembled de novo using modern sequencing techniques, and large chunks of sequence ('scaffolds') were linked to chromosomes using an available linkage map (Backström et al, 2008) and-under the reasonable assumption of high degree of synteny in birds-the zebra finch genome sequence (Warren et al, 2010). In the next phase of analyses, the authors re-sequenced the genomes of 10 unrelated males of each of the two flycatcher species.…”