Gene flow influences the genomic architecture of local adaptation in six riverine fish species

Abstract

Understanding how gene flow influences adaptive divergence is important for predicting adaptive responses. Theoretical studies suggest that when gene flow is high, clustering of adaptive genes in fewer genomic regions would protect adaptive alleles from among-population recombination and thus be selected for, but few studies have tested this hypothesis with empirical data. Here, we used RADseq to generate genomic data for six fish species with contrasting life histories from six reaches of the Upper Mississippi River System, USA. We then conducted genome scans for genomic islands of divergence to examine the distribution of adaptive loci and investigated whether these loci were found in inversions. We found that gene flow varied among species, and adaptive loci were clustered more tightly in species with higher gene flow. For example, the two species with the highest overall F ST (0.03 -0.07) and therefore lowest gene flow showed little evidence of clusters of adaptive loci, with adaptive loci spread uniformly across the genome. In contrast, nearly all adaptive loci in the species with the lowest F ST (0.0004) were found in a single large putative inversion. Two other species with intermediate gene flow (F ST ~ 0.004) also showed clustered genomic architectures, with most islands of divergence clustered on a few chromosomes. These results provide important empirical evidence to support the hypothesis that increasingly clustered architectures of local adaptation are associated with high gene flow. Our study utilized a unique system with species spanning a large gradient of life histories to highlight the importance of gene flow in shaping adaptive divergence.

Inversion invasions: when the genetic basis of local adaptation is concentrated within inversions in the face of gene flow

“…A highly polygenic, genotypically redundant (as in [29]) architecture can allow for LA to occur even when the alleles are individually prone to swamping by migration (hereafter: swamping-prone alleles; [27]). Therefore, the question remains as to whether genomes with multiple, large and old inversions involved in LA under high gene flow could be consistent with a highly polygenic architecture, and whether inversions could establish as a means of accumulation (as opposed to capture, as previous theory/simulations have assumed) of small-effect alleles [30].…”

An allozyme polymorphism is associated with a large chromosomal inversion in the marine snail Littorina fabalis

“…Chromosomal rearrangements, and inversions, in particular, are known to reduce effective recombination among alleles at different loci involved in local adaption, facilitating local adaptation under gene flow (Jones et al, 2012 ; Kirkpatrick & Barton, 2006 ; Mérot et al, 2020 ). Using new sequencing approaches, an increasing number of empirical examples of rearrangements involved in local adaptation have been reported (Le Moan et al, 2021 ; Shi et al, 2021 ; Tepolt et al, 2022 ; Whiting et al, 2021 ). For instance, in the marine snail, Littorina saxatilis , polymorphism in several chromosomal inversions underlies major genetic differences between a large ecotype adapted to crab predation and a small ecotype adapted to wave action (Faria et al, 2019 ; Morales et al, 2019 ).…”

High‐density genomic data reveal fine‐scale population structure and pronounced islands of adaptive divergence in lake whitefish (Coregonus clupeaformis) from Lake Michigan

“…Both theoretical simulation studies and empirical studies have shown that increased gene flow will lead to the increasingly concentrated genomic architecture of local adaptation (Shi et al, 2021 ; Via, 2012 ; Yeaman, 2013 ; Yeaman & Whitlock, 2011 ). In a species with high gene flow across heterogeneous environments, adaptive differentiation is often restricted to genomic islands of divergence that can resist the homogenizing effects of gene flow (Via, 2012 ).…”

“…To estimate linkage disequilibrium (LD) of each candidate region, we calculated r 2 using PLINK v1.9 (‐‐ld‐window 999999999 ‐‐ld‐window‐kb 30000 ‐‐ld‐window‐r2 0.05) for SNPs with MAF ≥0.01 and located at least 400 bp from one another for each chromosome with a candidate region. We compared LD between pcadapt outliers within a candidate region and random SNPs (chromosomal background) on the same chromosome, visualized the differences using boxplots, and tested for significance using permutation tests with 10,000 iterations following the permutation test procedures described in Shi et al ( 2021 ). Briefly, this involved drawing 10,000 samples of random SNPs equal to the number of pcadapt outliers within the candidate region to generate the null distribution for that chromosome.…”

“…Moreover, genomic approaches may be useful for identifying locally adaptive variants that are key to long‐term species persistence but that could be overlooked when establishing management units based on neutral or genome‐wide variation (Funk et al, 2012 ; Nielsen et al, 2012 ). In species that experience high gene flow across heterogeneous environments, likely the case for lake whitefish in Lake Michigan, adaptive loci are expected to be tightly clustered, generating pronounced genomic islands of adaptive divergence (Shi et al, 2021 ).…”