Genome-wide recombination patterns and their implications in threespine stickleback fish

[This post is by Marius Rösti; I am just putting it up.  -B.]

During meiosis – the characteristic cell division in sexually reproducing organisms – the mother cell that gives rise to sperm or ova has to multiply and reduce the number of chromosomes from two full sets to one. During this process, the two homologous chromosomes (one from each parent) can exchange DNA segments. This process is called meiotic recombination. In a paper just published in Molecular Ecology, we demonstrate in one of the prime model systems in evolutionary biology (threespine stickleback fish) that recombination is distributed highly heterogeneously within the genome, and highlight implications for genome evolution and its empirical investigation.

A threespine stickleback, Gasterosteus aculeatus

Heterogeneous recombination rate

Threespine stickleback (Gasterosteus aculeatus) offer a powerful model system in evolutionary biology. Some of the reasons are the well-known natural history and ecology of this fish, as well as the availability of many genetic and genomic tools. However, a detailed analysis of recombination in stickleback has been missing so far. To do this, we first reassembled and improved the stickleback’s reference genome. Based on 300 individuals and approximately 2000 genome-wide SNP markers, we find that the recombination rate is highly elevated in the chromosome peripheries relative to the chromosome centers. A similar distribution of recombination events along chromosomes has recently been found in several other taxa, including humans. We further detected a minimum of one recombination event per chromosome (but not chromosome arm) per meiosis event. These findings likely point to strong functional constraints on the rate and distribution of recombination within the genome.

Heterogeneous recombination rate drives patterns of genetic diversity and population divergence

Incorporating genome-wide sequence data from four natural stickleback populations inhabiting ecologically different lake and stream habitats, we can demonstrate clear associations between recombination rate and the magnitude of allele frequency shifts between populations, and between recombination rate and genetic diversity within populations. In these young (only a few thousand years old) populations experiencing divergent natural selection, these patterns certainly reflect genome-wide heterogeneity in the effect of selection on linked sites, which has proved hard to demonstrate convincingly in non-ecological (genetic) model systems such as Drosophila flies. This recombination-driven heterogeneity in signatures of selection has a potentially important methodological implication: ecological genome scans will detect divergence outliers more easily in low-recombination regions. Furthermore, we detected a strong association between recombination rate and GC nucleotide content. As suggested in other organisms, this pattern perhaps arises from GC-biased gene conversion, potentially reflecting a direct influence of recombination on genome evolution.

Recombination and sex chromosome evolution

As in humans, in threespine stickleback  males are the heterogametic sex: males carry an X and a Y sex chromosome, while females carry two X’s. We were able to confirm and narrow down the physical boundaries of a previously inferred small ‘pseudoautosomal’ region within the sex chromosome where recombination between the X and Y still occurs. The rest of the X chromosome does not recombine with the Y any more, but it does exhibit two regions characterized by distinct levels of differentiation between the X and the Y. Such ‘evolutionary strata’ of Y-degeneration are expected when the suppression of recombination between the X and Y occurred in discrete pulses across large chromosomal regions. This first demonstration of evolutionary strata of Y-degeneration in a fish species highlights the devastating effects of suppressed recombination during the evolution of sex chromosomes.

Paper reference

Roesti, M., Moser, D. and Berner, D. (2013). Recombination in the threespine stickleback genome—patterns and consequences. Molecular Ecology. doi: 10.1111/mec.12322