Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome

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 approximately 50% that of chicken, challenging the widely held view that birds generally have high recombination rates.

Figure 1.—

Correlation between intron size (in base pairs) in chicken and collared flycatcher (y = 0.81x + 74.7).

Figure 2.—

A framework linkage map of the collared flycatcher Z chromosome. Positions are given as the cumulative genetic position of gene markers in the linkage map. Unordered markers are shown to the right with alternative locations indicated by vertical bars. Note that most unordered markers can be placed with statistical support in either of two locations.

Figure 3.—

A best-order linkage map of the collared flycatcher chromosome based on all gene markers genotyped in the pedigree. Positions are given as the cumulative genetic position of gene markers in the linkage map.

Figure 4.—

A comparison of the relative location of orthologous genes on the chicken and collared flycatcher Z chromosome maps. Gene order in collared flycatcher is from the framework linkage map presented in Figure 2. In chicken, data are from the draft genome assembly updated with information from linkage mapping.

Figure 5.—

A comparison of the relative location of orthologous genes on the chicken and collared flycatcher Z chromosome maps. Gene order in collared flycatcher is from the best-order linkage map presented in Figure 3. In chicken, data are from the draft genome assembly updated with information from linkage mapping.