Fast Evolution from Precast Bricks: Genomics of Young Freshwater Populations of Threespine Stickleback Gasterosteus aculeatus

Abstract

Adaptation is driven by natural selection; however, many adaptations are caused by weak selection acting over large timescales, complicating its study. Therefore, it is rarely possible to study selection comprehensively in natural environments. The threespine stickleback (Gasterosteus aculeatus) is a well-studied model organism with a short generation time, small genome size, and many genetic and genomic tools available. Within this originally marine species, populations have recurrently adapted to freshwater all over its range. This evolution involved extensive parallelism: pre-existing alleles that adapt sticklebacks to freshwater habitats, but are also present at low frequencies in marine populations, have been recruited repeatedly. While a number of genomic regions responsible for this adaptation have been identified, the details of selection remain poorly understood. Using whole-genome resequencing, we compare pooled genomic samples from marine and freshwater populations of the White Sea basin, and identify 19 short genomic regions that are highly divergent between them, including three known inversions. 17 of these regions overlap protein-coding genes, including a number of genes with predicted functions that are relevant for adaptation to the freshwater environment. We then analyze four additional independently derived young freshwater populations of known ages, two natural and two artificially established, and use the observed shifts of allelic frequencies to estimate the strength of positive selection. Adaptation turns out to be quite rapid, indicating strong selection acting simultaneously at multiple regions of the genome, with selection coefficients of up to 0.27. High divergence between marine and freshwater genotypes, lack of reduction in polymorphism in regions responsible for adaptation, and high frequencies of freshwater alleles observed even in young freshwater populations are all consistent with rapid assembly of G. aculeatus freshwater genotypes from pre-existing genomic regions of adaptive variation, with strong selection that favors this assembly acting simultaneously at multiple loci.

Genomic tools for new insights to variation, adaptation, and evolution in the salmonid fishes: a perspective for charr

“…At present, the feasibility of whole genome resequencing for ecological genomics depends somewhat on genome size and complexity, as well as budget. In ecological genomics of fishes more generally, stickleback fishes (genome size 675 Mb) are now often whole genome resequenced (Jones et al, 2012;Terekhanova et al, 2014) as are some cichlids (genome size *1 Gb) either with few individuals at high coverage (e.g. Brawand et al, 2014) or with individuals pooled and overall lower coverage focusing on fixed differences (e.g.…”

Regulatory architecture of gene expression variation in the threespine stickleback, Gasterosteus aculeatus

“…One way in which these regions could exert such pleiotropic effects is by harboring loci that influence the expression of many genes, i.e., eQTL hotspots. However, only one of the trans-eQTL hotspots n (continued) found in this study (Chr12a) overlapped with genomic regions repeatedly found to be associated with marine/freshwater divergence by Hohenlohe et al (2010), Jones et al (2012), or Terekhanova et al (2014. Nevertheless, several studies indicate that adaptation to novel aquatic environments may also involve parts of the genome outside these large target regions (DeFaveri et al 2011;Leinonen et al 2012;Ellis et al 2015;Erickson et al 2016;Ferchaud and Hansen 2016).…”

“…Association of eQTL with regions under selection Hohenlohe et al (2010), Jones et al (2012), and Terekhanova et al (2014) documented parallel regions of the genome divergent between marine and freshwater sticklebacks on chromosomes 1, 4 (three regions), 7, 11, and 21. We investigated whether these regions harbored important trans regulators that might contribute to adaptation to different aquatic habitats by comparing the location of these regions with the location of our identified trans-eQTL hotspots.…”

“…The species is also distributed throughout semimarine environments with large temperature and salinity gradients, such as estuaries and the brackish water Baltic Sea (McCairns and Bernatchez 2010;Guo et al 2015;Konijnendijk et al 2015). Successful colonization of these diverse habitats necessitates behavioral, morphological, and physiological adaptation to novel environmental conditions including changed temperature, salinity, oxygen, light, parasite and predator regimens, a process that can occur rapidly (Kitano et al 2010;Barrett et al 2011;Terekhanova et al 2014;Lescak et al 2015;Huang et al 2016, Rennison et al 2016. Parallel adaptations between independently founded freshwater populations frequently involve the same regions of the genome and arise from preexisting genetic variation in the marine population (Colosimo et al 2005;Hohenlohe et al 2010;Jones et al 2012;Liu et al 2014;Conte et al 2015, but see DeFaveri et al 2011Leinonen et al 2012;Ellis et al 2015;Ferchaud and Hansen 2016).…”

Analysis of distribution of chromatin marks across "divergence islands" in three-spined stickleback (Gasterosteus aculeatus)

“…We selected histone modification peaks in "divergence islands" regions, which are highly divergent between marine and freshwater populations of sticklebacks 2 . We observed that the majority (17 out of 19) of the islands showed the same chromatin marks (H3K4me1, H3K4me3 and H3K27ac) in fresh water species in their natural salinity (FF) and fresh water species placed into a marine environment (FM).…”