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 FST (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 FST (0.0004) were found in a single large putative inversion. Two other species with intermediate gene flow (FST ~ 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].…”

A chromosomal inversion may facilitate adaptation despite periodic gene flow in a freshwater fish

“…We used a reduced representation approach to genotype n = 345 walleye from three different waterbodies in North America at 46,342 genetic markers. Walleye of the Canadian lakes diverged from each other despite three scenarios for gene flow: a connecting river, stocking of fry throughout the 20th century, and flooding in 1882, 1902, 1904, 2011, and 2014 (and gence between Lake Winnipeg and Lake Manitoba walleye (Shi et al, 2021;Wellenreuther & Bernatchez, 2018), and three expressed genes (i.e., mRNA transcripts) within it indicate at least the potential for functional significance of the putative inversion.…”

“…According to a simulation study, intermediate-to-large inversions have been linked to local adaptation, but small inversions were preferentially fixed in directly beneficial mutation models and contributed the most to genome evolution in neutral and underdominant scenarios (Connallon & Olito, 2021). Among fishes, chromosomal inversions have largely been characterized in well studied groups of species such as representative salmonids (Arostegui et al, 2019;Leitwein et al, 2017;McKinney et al, 2020;Pearse et al, 2014) and gadids (Berg et al, 2016(Berg et al, , 2017Kirubakaran et al, 2016;Puncher et al, 2019;Sinclair-Waters et al, 2018;Sodeland et al, 2016), but little information exists on the importance of inversions in most taxa, especially in obligate freshwater inhabitants (Penso-Dolfin et al, 2020;Roesti et al, 2015;Shi et al, 2021).…”

“…Differences in genomic architecture such as structural variants may help to facilitate local adaptation by suppressing recombination and protecting co‐adapted alleles, and are therefore key mechanisms of eco‐evolutionary processes (Dorant et al, 2020; Shi et al, 2021; Tigano & Friesen, 2016; Wellenreuther & Bernatchez, 2018). One type of structural variant, chromosomal inversions, are taxonomically widespread reversed regions of DNA that have been linked to both adaptation and speciation (reviewed in Wellenreuther & Bernatchez, 2018).…”

An introgression breakthrough left by an anthropogenic contact between two ascidians

“…Briefly, the HMM characterizes and sorts genomic regions according to their level of differentiation, and is generally used to detect island of divergence (e.g. Soria-Carrasco et al, 2014, Shi et al, 2021. Here, the HMM was applied to detect regions of introgression by contrasting regions with high-background differentiation (with an F ST value of one) from regions with intermediate differentiation (with F ST normally distributed around the 15% lower quantile) and low differentiation (with F ST normally distributed around the 5% lower quantile) using a modify version of the R script available from Marques et al (2016).…”