Genome divergence during evolutionary diversification as revealed in replicate lake–stream stickleback population pairs

Abstract

Evolutionary diversification is often initiated by adaptive divergence between populations occupying ecologically distinct environments while still exchanging genes. The genetic foundations of this divergence process are largely unknown and are here explored through genome scans in multiple independent lake-stream population pairs of threespine stickleback. We find that across the pairs, overall genomic divergence is associated with the magnitude of divergence in phenotypes known to be under divergent selection. Along this same axis of increasing diversification, genomic divergence becomes increasingly biased towards the centre of chromosomes as opposed to the peripheries. We explain this pattern by within-chromosome variation in the physical extent of hitchhiking, as recombination is greatly reduced in chromosome centres. Correcting for this effect suggests that a great number of genes distributed widely across the genome are involved in the divergence into lake vs. stream habitats. Analyzing additional allopatric population pairs, however, reveals that strong divergence in some genomic regions has been driven by selection unrelated to lake-stream ecology. Our study highlights a major contribution of large-scale variation in recombination rate to generating heterogeneous genomic divergence and indicates that elucidating the genetic basis of adaptive divergence might be more challenging than currently recognized.

Key questions in the genetics and genomics of eco-evolutionary dynamics

“…The actual number of genes, however, will be much higher, because (1) multiple genes are present in each genomic region and (2) the focus was only on regions showing parallel divergence across all comparisons. Not surprisingly, then, other work has found many more genes that differ between freshwater and marine stickleback (Shimada et al, 2010;Jones et al, 2012b), and similar results have been obtained for lake versus stream stickleback (Roesti et al, 2012), benthic versus limnetic stickleback (Jones et al, 2012a), and dwarf versus normal whitefish (Renaut et al, 2011). In short, genome scans typically implicate divergence in many genes; and yet these scans still remain biased against genes of small effect.…”

The puzzling phylogeography of the haplochromine cichlid fishAstatotilapia burtoni

“…Libraries were prepared according to the protocol described in Roesti, Hendry, Salzburger, and Berner (2012). In short, a DNA concentration of 20 ng/μl was used for library preparation allowing for a deviation of ±1 ng/μl.…”

Physiological and genetic basis for variation in migratory behavior in the three-spined stickleback, Gasterosteus aculeatus

“…Therefore, the gap between model and non-model organisms is becoming increasingly blurred. Next-generation sequencers would facilitate genome scan analyses by using sequenced RAD (Baird et al 2008;Hohenlohe et al 2010;Rowe et al 2011;Roesti et al 2012) and transcriptome analyses by RNA-sequencing in non-model organisms (Vera et al 2008). Applications of such genomic tools to non-model organisms that exhibit diverse migratory behaviors will enable us to elucidate whether the same sets of genes are important in the divergence of migratory behaviors across diverse taxa.…”

“…Recent progress in next-generation sequencers is making it possible to find an increasing number of genetic markers at relatively low costs (Hudson 2008;Stapley et al 2010;Davey et al 2011;Elmer and Meyer 2011). For example, SNP analysis with sequenced RAD is a powerful method to identify a signature of divergent selection (Baird et al 2008;Hohenlohe et al 2010;Roesti et al 2012). Because the genome sequences of Gasterosteus aculeatus are relatively small (\450 Mb) and the reference genome sequence is available (Kingsley and Peichel 2007;Jones et al 2012b), wholegenome re-sequencing of G. aculeatus is relatively easy by using next-generation sequencers (Jones et al 2012b).…”