Genetic Mapping in a Natural Population of Collared Flycatchers (Ficedula Albicollis): Conserved Synteny but Gene Order Rearrangements on the Avian Z Chromosome

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ABSTRACT

Data from completely sequenced genomes are likely to open the way for novel studies of the genetics of nonmodel organisms, in particular when it comes to the identification and analysis of genes responsible for traits that are under selection in natural populations. Here we use the draft sequence of the chicken genome as a starting point for linkage mapping in a wild bird species, the collared flycatcher-one of the most well-studied avian species in ecological and evolutionary research. A pedigree of 365 flycatchers was established and genotyped for single nucleotide polymorphisms in 23 genes selected from (and spread over most of) the chicken Z chromosome. All genes were also found to be located on the Z chromosome in the collared flycatcher, confirming conserved synteny at the level of gene content across distantly related avian lineages. This high degree of conservation mimics the situation seen for the mammalian X chromosome and may thus be a general feature in sex chromosome evolution, irrespective of whether there is male or female heterogamety. Alternatively, such unprecedented chromosomal conservation may be characteristic of most chromosomes in avian genome evolution. However, several internal rearrangements were observed, meaning that the transfer of map information from chicken to nonmodel bird species cannot always assume conserved gene orders. Interestingly, the rate of recombination on the Z chromosome of collared flycatchers was only ∼50% that of chicken, challenging the widely held view that birds generally have high recombination rates.

THE possibility of identifying genes coding for traits that are under selection in natural populations and, given the availability of such knowledge, subsequently studying key aspects of evolutionary biology has only recently become a realistic goal (FEDER and MITCHELL-OLDS 2003; SLATE 2005; VASEMAGI and PRIMMER 2005). Examples of questions that should be possible to address are how local adaptation relates to genotypic variation and how genetic variation can be maintained for fitness-related traits by, for instance, genotype-environment interaction (STEARNS 1992). Various approaches may be taken to attack the missing link between genotypes and phenotypes in wild populations of nonmodel organisms, including candidate gene approaches (TABOR et al. 2002), transcriptome profiling through EST sequencing (LE QUERE et al. 2004) or microarray-based hybridization (DRNEVICH et al. 2004), genome scans for regions subject to selective sweeps (STORZ 2005), and linkage/quantitative trait loci (QTL) mapping (SLATE 2005). To various extents, all these approaches require some prior knowledge of the genetics of the species under study, which until recently has been a major limiting factor in the case of most natural populations. This is particularly true for genetic mapping approaches in which a large number of polymorphic markers have to be developed and placed on a primary linkage map.

However, an increasing number of linkage maps are now being reported from natural populations of organisms, such as butterflies (JIGGINS et al. 2004), fishes (CHISTIAKOV et al. 2005), fungi (MARRA et al. 2004), insects (LORENZEN et al. 2005), molluscs (HUBERT and HEDGECOCK 2004), and amphibians (SMITH et al. 2005). They are so far generally limited to 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 pedigrees necessary for linkage analysis. Unfortunately, this is not the case for most species of birds. In addition to the well-established linkage map of the chicken (GROENEN et al. 2001), mapping is underway in some domestic galliforms of agricultural interest, including quail (KIKUCHI et al. 2005) and turkey (REED et al. 2005), but there are only preliminary attempts at linkage mapping in wild species, notably by the work of HANSSON et al. (2005). …