Predictable genome-wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish.

Quiterie Haenel,Andrew D C Maccoll,Daniel Berner,Marius Roesti,Dario Moser

doi:10.1002/evl3.99

Abstract

Genomic studies of parallel (or convergent) evolution often compare multiple populations diverged into two ecologically different habitats to search for loci repeatedly involved in adaptation. Because the shared ancestor of these populations is generally unavailable, the source of the alleles at adaptation loci, and the direction in which their frequencies were shifted during evolution, remain elusive. To shed light on these issues, we here use multiple populations of threespine stickleback fish adapted to two different types of derived freshwater habitats—basic and acidic lakes on the island of North Uist, Outer Hebrides, Scotland—and the present‐day proxy of their marine ancestor. In a first step, we combine genome‐wide pooled sequencing and targeted individual‐level sequencing to demonstrate that ecological and phenotypic parallelism in basic‐acidic divergence is reflected by genomic parallelism in dozens of genome regions. Exploiting data from the ancestor, we next show that the acidic populations, residing in ecologically more extreme derived habitats, have adapted by accumulating alleles rare in the ancestor, whereas the basic populations have retained alleles common in the ancestor. Genomic responses to selection are thus predictable from the ecological difference of each derived habitat type from the ancestral one. This asymmetric sorting of standing genetic variation at loci important to basic‐acidic divergence has further resulted in more numerous selective sweeps in the acidic populations. Finally, our data suggest that the maintenance in marine fish of standing variation important to adaptive basic‐acidic differentiation does not require extensive hybridization between the marine and freshwater populations. Overall, our study reveals striking genome‐wide determinism in both the loci involved in parallel divergence, and in the direction in which alleles at these loci have been selected.

Highlights

While well documented at the phenotypic level, the genomic underpinnings of such parallel evolution remain elusive—to what extent is phenotypic parallelism reflected by genomic parallelism, and where do the genetic variants used for repeated adaptation originate? To examine these questions, we study young populations of stickleback fish displaying striking phenotypic similarity within multiple basic and acidic lakes on the island of North Uist, Scotland
BASIC AND ACIDIC STICKLEBACK ECOTYPES ON NORTH UIST HAVE EVOLVED INDEPENDENTLY In our nuclear single-nucleotide polymorphisms (SNPs) phylogeny based on synthetic genotypes, basic and acidic populations appeared well-mixed across the genealogical tree
Ordination of the populations indicated the absence of genetic similarity by ecotype (Fig. 2B). (See the weak correlations in allele frequencies estimated by BayPass for all population combinations except FEIT and GROG, Supporting Information Fig. S5B; these two populations may not qualify as fully independent.) These genetic patterns, combined with the geographic separation of the basic and acidic habitats due to surface geology, render the major alternative to parallel evolution—the single origin of a basic and an acidic ecotype followed by admixture between the ecotypes during secondary contact in different localities (Bierne et al 2013)— highly implausible

Summary

Introduction

Genetic loci important to differential adaptation are identified by screening the populations for exceptionally strong habitat-related genetic differentiation relative to the genome-wide background level (e.g., Roesti et al 2015; Lamichhaney et al 2016; Reid et al 2016; Yeaman et al 2016; Marques et al 2017) This approach is informative when multiple populations adapted independently to each habitat type are available, as such “parallel” (or convergent; Arendt and Reznick 2008) evolution helps distinguish deterministic selective from stochastic genetic differentiation (Berner and Salzburger 2015). An obvious obstacle to such genomic investigation, is that natural systems providing access to the ancestor of populations adapted in parallel to multiple derived habitats are rare

Methods

Results

Conclusion