Replicated high-density genetic maps of two great tit populations reveal fine-scale genomic departures from sex-equal recombination rates

Abstract

Linking variation in quantitative traits to variation in the genome is an important, but challenging task in the study of life-history evolution. Linkage maps provide a valuable tool for the unravelling of such trait-gene associations. Moreover, they give insight into recombination landscapes and between-species karyotype evolution. Here we used genotype data, generated from a 10k single-nucleotide polymorphism (SNP) chip, of over 2000 individuals to produce high-density linkage maps of the great tit (Parus major), a passerine bird that serves as a model species for ecological and evolutionary questions. We created independent maps from two distinct populations: a captive F2-cross from The Netherlands (NL) and a wild population from the United Kingdom (UK). The two maps contained 6554 SNPs in 32 linkage groups, spanning 2010 cM and 1917 cM for the NL and UK populations, respectively, and were similar in size and marker order. Subtle levels of heterochiasmy within and between chromosomes were remarkably consistent between the populations, suggesting that the local departures from sex-equal recombination rates have evolved. This key and surprising result would have been impossible to detect if only one population was mapped. A comparison with zebra finch Taeniopygia guttata, chicken Gallus gallus and the green anole lizard Anolis carolinensis genomes provided further insight into the evolution of avian karyotypes.

Figure 1

Total map size for each chromosome of the NL maps plotted against the map length of the UK maps. The line shows the expected value if map lengths from both populations were identical.

Figure 2

Comparison of levels of heterochiasmy per linkage group for the NL and the UK populations. Heterochiasmy is indicated as the size dimorphism index (SDI). Negative SDI values indicate larger male linkage groups compared with female linkage groups. The solid line represents the y=x line, the dotted line the outcome of the reduced major axis regression (y=0.72x+0.04). Only linkage groups larger than 10 cM are plotted. Linkage groups that deviate significantly from 1:1 are indicated with *.

Figure 3

Size Dimorphism Index (SDI) calculated for windows of 20 SNP markers on the NL (orange) and UK (blue) framework maps. Subsequent windows were chosen by sliding the window five SNP markers along the linkage group. Positive SDI indicates that female recombination rates within the 20 SNP window was higher; negative values indicate greater recombination rates in males. Only linkage groups with at least three windows are plotted.

Figure 4

Comparative maps for six example great tit linkage groups, with the great tit linkage map positions plotted against the predicted physical position on the zebra finch (TGU; left panels) and chicken (GGA; right panels) genomes. (a) PMA19 is highly conserved across avian lineages; no rearrangements relative to TGU or GGA, (b) PMA14 is an example of a rearrangement specific to the great tit lineage; an inversion relative to marker order in both TGU and GGA, (c) PMA10 is an example of a TGU-specific rearrangement; an inversion between PMA and TGU, (d) PMA6 is an example of a difference between passerines and galliformes; rearrangement relative to GGA but not TGU, (e) and (f) are chromosomes that are generally evolutionarily less stable across avian genomes, where (e) PMA1; inversions compared with TGU, and both inversions and rearrangements compared with GGA, and (f) PMA7; distinct inversions when PMA is compared with TGU and GGA.

Figure 5

Great tit-green anole lizard (Anolis carolinensis; ACA) synteny map. The horizontal bars represent the six A. carolinensis macrochromosomes ACA1–ACA6 and three microchromosomes LGa, LGb and LGc, to which aligned SNPs or blocks of SNPs could be ordered. Each coloured block represents a great tit (PMA) chromosome as is indicated in the lower part of the graph. Adjusted from (Alfoldi et al., 2011).