The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res

Department of Evolutionary Biology, Uppsala University, SE-752 36 Uppsala, Sweden.
Genome Research (Impact Factor: 14.63). 03/2010; 20(4):485-95. DOI: 10.1101/gr.101410.109
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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.

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    • "The study concluded that " recombination rate is likely of little importance " in relation to plant domestication (Ross-Ibarra 2004). The study of Burt and Bell (1987), in which chiasmata counts for domestic mammals are reported, is often cited as evidence that domestic animals have higher recombination rate than their wild counterparts (see Schmidt-Hempel and Jokela 2002; Dumont and Payseur 2008; Groenen et al. 2009; Backström et al. 2010; Poissant et al. 2010; Smukowski and Noor 2011). "
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    ABSTRACT: Recombination rates vary in intensity and location at the species, individual, sex and chromosome levels. Despite the fundamental biological importance of this process, the selective forces that operate to shape recombination rate and patterns are unclear. Domestication offers a unique opportunity to study the interplay between recombination and selection. In domesticates, intense selection for particular traits is imposed on small populations over many generations, resulting in organisms that differ, sometimes dramatically, in morphology and physiology from their wild ancestor. Although earlier studies suggested increased recombination rate in domesticates, a formal comparison of recombination rates between domestic mammals and their wild congeners was missing. In order to determine broad-scale recombination rate, we used immunolabeling detection of MLH1 foci as crossover markers in spermatocytes in three pairs of closely related wild and domestic species (dog and wolf, goat and ibex, and sheep and mouflon). In the three pairs, and contrary to previous suggestions, our data show that contemporary recombination rate is higher in the wild species. Subsequently, we inferred recombination breakpoints in sequence data for 16 genomic regions in dogs and wolves, each containing a locus associated with a dog phenotype potentially under selection during domestication. No difference in the number and distribution of recombination breakpoints was found between dogs and wolves. We conclude that our data indicate that strong directional selection did not result in changes in recombination in domestic mammals, and that both upper and lower bounds for crossover rates may be tightly regulated.
    Molecular Biology and Evolution 11/2014; 32(2). DOI:10.1093/molbev/msu322 · 9.11 Impact Factor
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    • "Intrachromosomal rearrangements, which have occurred between the three bird species considered (reviewed by Ellegren 2010, 2014; see also van Oers et al. 2014), should not make the test counterconservative . This is because, for macrochromosomes, shuffling genes between the ends and the central parts is expected to homogenize differences in recombination frequency , whereas for microchromosomes, genetic maps in all species studied to date suggest recombination rates are roughly constant along the length of the chromosome (Backströ m et al. 2010; Stapley et al. 2010; van Oers et al. 2014). There is evidence that GC content is not at statistical equilibrium in multiple avian lineages and that GC-biased gene "
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    ABSTRACT: Determining the rate of protein evolution and identifying the causes of its variation across the genome are powerful ways to understand forces that are important for genome evolution. By using a multi-tissue transcriptome data set from great tit (Parus major), we analysed patterns of molecular evolution between two passerine birds, great tit and zebra finch (Taeniopygia guttata), using the chicken genome (Gallus gallus) as an outgroup. We investigated whether a special feature of avian genomes, the highly variable recombinational landscape, modulates the efficacy of natural selection through the effects of Hill-Robertson interference, which predicts that selection should be more effective in removing deleterious mutations and incorporating beneficial mutations in high-recombination regions than in low-recombination regions. In agreement with these predictions, genes located in low-recombination regions tend to have a high proportion of neutrally evolving sites and relaxed selective constraint on sites subject to purifying selection, whereas genes that show strong support for past episodes of positive selection appear disproportionally in high-recombination regions. There is also evidence that genes located in high-recombination regions tend to have higher gene expression specificity than those located in low-recombination regions. Furthermore, more compact genes (i.e., those with fewer/shorter introns or shorter proteins) evolve faster than less compact ones. In sum, our results demonstrate that transcriptome sequencing is a powerful method to answer fundamental questions about genome evolution in non-model organisms.
    Genome Biology and Evolution 07/2014; 6(8). DOI:10.1093/gbe/evu157 · 4.23 Impact Factor
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    • "There are multiple signatures of strong selection in the Ficedula divergence islands – including reduced diversity, a skewed allele frequency spectrum, and higher linkage disequilibrium (LD) – and they largely coincide with centromeres, regions known to have reduced recombination in syntenic bird genomes (e.g. Backstr€ om et al. 2010). Together with the lower values of absolute divergence, the data better support a model in which regions of 50-fold higher 'divergence' instead indicate regions of 50-fold lower polymorphism and that many of these islands have been subject to recurrent selection since before the species split. "
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    ABSTRACT: The metaphor of “genomic islands of speciation” was first used to describe heterogeneous differentiation among loci between the genomes of closely related species. The biological model proposed to explain these differences was that the regions showing high levels of differentiation were resistant to gene flow between species, while the remainder of the genome was being homogenized by gene flow and consequently showed lower levels of differentiation. However, the conditions under which such differentiation can occur at multiple unlinked loci are restrictive; additionally, essentially all previous analyses have been carried out using relative measures of divergence, which can be misleading when regions with different levels of recombination are compared. Here we test the model of differential gene flow by asking whether absolute divergence is also higher in the previously identified “islands.” Using five species-pairs for which full sequence data is available, we find that absolute measures of divergence are not higher in genomic islands. Instead, in all cases examined we find reduced diversity in these regions, a consequence of which is that relative measures of divergence are abnormally high. These data therefore do not support a model of differential gene flow among loci, though islands of relative divergence may represent loci involved in local adaptation. Simulations using the program IMa2 further suggest that inferences of any gene flow may be incorrect in many comparisons. We instead present an alternative explanation for heterogeneous patterns of differentiation, one in which post-speciation selection generates patterns consistent with multiple aspects of the data.This article is protected by copyright. All rights reserved.
    Molecular Ecology 05/2014; 23(13). DOI:10.1111/mec.12796 · 6.49 Impact Factor
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