Sweeping genomic remodeling through repeated selection of alternatively adapted haplotypes occurs in the first decades after marine stickleback colonize new freshwater ponds

Abstract

Heterogeneous genetic divergence can accumulate across the genome when populations adapt to different habitats while still exchanging alleles. How long does diversification take and how much of the genome is affected? When divergence occurs in parallel from standing genetic variation, how often are the same haplotypes used? We explore these questions using RAD-seq genotyping data, and show that broadscale genomic re-patterning, fueled by standing variation, can emerge in just dozens of generations in replicate natural populations of threespine stickleback fish (Gasterosteus aculeatus). After the catastrophic 1964 Alaskan earthquake, marine stickleback colonized newly created ponds on seismically uplifted islands. We find that freshwater fish in these young ponds differ from their marine ancestors across the same genomic segments previously shown to have diverged in much older lake populations. Outside of these core divergent regions the genome shows no population structure across the ocean-freshwater divide, consistent with strong local selection acting in alternative environments on stickleback populations still connected by significant gene flow. Reinforcing this inference, a majority of divergent haplotypes that are at high frequency in ponds are shared across independent freshwater populations and are detectable, at low frequency, in the sea even across great geographic distances. Building upon previous work in this model species for population genomics, our data suggest that a long history of divergent selection and gene flow across stickleback in oceanic and freshwater habitats has created balanced polymorphism in large genomic blocks of alternatively adapted DNA sequences, ultimately stoking -and potentially channelingrapid, parallel evolution. contemporary evolution -ecological divergence -population genomics -Gasterosteus aculeatus -threespine stickleback 1

Genomic parallelism and lack thereof in contrasting systems of three‐spined sticklebacks

“…Studies of recently colonized stickleback populations provide results supporting this (Bassham et al, 2017;Lescak et al, 2015;Terekhanova et al, 2014). However, as pointed out by, for example, Kaeuffer, Peichel, Bolnick, and Hendry (2012), the degree of nonparallelism (in the present case, 79.4% of outliers) is just as important LIU ET AL.…”

“…Studies of recently colonized stickleback populations provide results supporting this (Bassham et al., ; Lescak et al., ; Terekhanova et al., ). However, as pointed out by, for example, Kaeuffer, Peichel, Bolnick, and Hendry (), the degree of nonparallelism (in the present case, 79.4% of outliers) is just as important to consider as parallelism, as this could both indicate idiosyncratic responses to similar selection regimes and responses to differences in selection regimes across environments.…”

“…Evolution occurs over generations rather than years, and it is at least theoretically possible that the more generations elapsed in the Danish system could result in reduced genomic parallelism in Denmark relative to Greenland. Adaptation to freshwater conditions after colonization by marine sticklebacks has been found to occur rapidly at both phenotypic and genomic levels (Bassham et al, 2017;Bell, Aguirre, & Buck, 2004;Le Rouzic et al, 2011;Lescak et al, 2015;Terekhanova et al, 2014), so this would imply that the (Figure 5c). Here, it should be considered, however, that we do not know whether these loci mark genomic regions associated with, for example, morphological traits favoured by selection in Mos and marine populations, or whether they mark regions associated with adaptation to marine and freshwater sensu stricto, such as physiological traits.…”

“…In this study, RAD sequencing using the restriction enzyme SbfI was unlikely to detect all selection ongoing in the genome, which was also not the purpose of the study. However, it represents a random sample of the genome (Catchen et al., ; Hohenlohe et al., ) and has been shown to detect regions of the genome under parallel selection in three‐spined stickleback (Bassham, Catchen, Lescak, Von Hippel, & Cresko, ; Hohenlohe et al., ). We already knew that parallelism was low in the temperate region in Denmark, both at the trait of lateral plating and at the genomic level.…”

The Genetic Architecture Underlying the Evolution of a Rare Piscivorous Life History Form in Brown Trout after Secondary Contact and Strong Introgression

“…In contrast to nucleotide diversity, the haplotype-based diversity measures take the full diversity within the RAD locus into account, and more than two haplotypes can exist for a locus. Gene diversity is the probability that two randomly chosen haplotypes for a given locus are different, and haplotype diversity, is scaled to the substitution distance between two randomly chosen haplotypes [ 68 , 89 , 90 ]. Values were smoothed and plotted along the genome using the loess smoothing method (span = 0.1) in the geom_smooth function of ggplot2 .…”