The recombination landscape of the zebra finch Taeniopygia guttata genome

Abstract

Understanding the causes and consequences of variation in the rate of recombination is essential since this parameter is considered to affect levels of genetic variability, the efficacy of selection, and the design of association and linkage mapping studies. However, there is limited knowledge about the factors governing recombination rate variation. We genotyped 1920 single nucleotide polymorphisms in a multigeneration pedigree of more than 1000 zebra finches (Taeniopygia guttata) to develop a genetic linkage map, and then we used these map data together with the recently available draft genome sequence of the zebra finch to estimate recombination rates in 1 Mb intervals across the genome. The average zebra finch recombination rate (1.5 cM/Mb) is higher than in humans, but significantly lower than in chicken. The local rates of recombination in chicken and zebra finch were only weakly correlated, demonstrating evolutionary turnover of the recombination landscape in birds. The distribution of recombination events was heavily biased toward ends of chromosomes, with a stronger telomere effect than so far seen in any organism. In fact, the recombination rate was as low as 0.1 cM/Mb in intervals up to 100 Mb long in the middle of the larger chromosomes. We found a positive correlation between recombination rate and GC content, as well as GC-rich sequence motifs. Levels of linkage disequilibrium (LD) were significantly higher in regions of low recombination, showing that heterogeneity in recombination rates have left a footprint on the genomic landscape of LD in zebra finch populations.

Meiotic recombination shapes precision of pedigree- and marker-based estimates of inbreeding

“…To our knowledge, all analytical analyses and most of the simulations so far have assumed a uniform distribution of crossovers along chromosomes (see, for example, Franklin, 1977;Stam, 1980;Hill and Weir, 2011;Kardos et al, 2015;Wang, 2016; but see Suarez et al, 1979 andLibiger andSchork, 2007 for Monte Carlo simulations on relatedness). Although this assumption holds more or less for the human genome (Matise et al, 2007), linkage maps from other species have shown that the distribution of recombination along chromosomes can be highly biased toward the telomeres (Gore et al, 2009;Backström et al, 2010). We and others predicted that this results in a more block-like inheritance pattern of genomic segments on a given chromosome which in turn increases the Mendelian noise (Risch and Lange, 1979;Guo, 1995;Forstmeier et al, 2012).…”

“…Similarly, it has been predicted that the distribution of crossovers along chromosomes will influence the amount of variance in IBD (see, for example, Risch and Lange, 1979;Rasmuson, 1993;Guo, 1995;Forstmeier et al, 2012), but to our knowledge it has never received attention in a modeling framework. Here we show that the variance in IBD is much larger in zebra finches than in humans, because in the former almost half of the genome is inherited in only six segments (that is, the interiors of chromosomes Tgu1, Tgu1A, Tgu2, Tgu3, Tgu4 and Tgu5) that only rarely break up by crossovers (Backström et al, 2010). Hill and Weir (2011) provide a formula to calculate the expected s.d.…”

“…Microsatellites used in that study were spread across nine chromosomes, including the macrochromosomes Tgu1, Tgu1A, Tgu2, Tgu3, Tgu5, Tgu6 and Tgu9, that together sum up to half the physical zebra finch genome and rarely break up in meiosis (Backström et al, 2010). Thus, they are potentially more informative than a random set of 'ideal markers' (as considered here).…”

“…For the zebra finch, we used the sex-averaged linkage map described in Backström et al (2010) based on 1395 SNPs and covering 33 chromosomes (data accessible from Schielzeth et al, 2011Schielzeth et al, , 2012. We excluded the sex chromosome and 10 microchromosomes covered by o10 markers (see Supplementary Information for details).…”

“…Our expectation is based on the fact that although the zebra finch genome consists of 39 autosomes compared with only 22 in humans, about half of its autosomal genome is made up of only 6 chromosomes (Tgu1, Tgu1A, Tgu2, Tgu3, Tgu4 and Tgu5) and shows extremely low recombination rates in the centers of these chromosomes (Backström et al, 2010), whereas in humans recombination is distributed quite uniformly on the megabase scale along chromosomes (Matise et al, 2007). We follow the genomes of 159 diploid pedigree founders, who we assume to be unrelated, through an empirical 7-generation pedigree of 3404 individuals.…”