Gene flow and selection interact to promote adaptive divergence in regions of low recombination

Abstract

Adaptation to new environments often occurs in the face of gene flow. Under these conditions, gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potentially favouring divergence and adaptive evolution in these regions over others. Here, we compiled a global genomic data set of over 1,300 individual threespine stickleback from 52 populations and compared the tendency for adaptive alleles to occur in regions of low recombination between populations that diverged with or without gene flow. In support of theory, we found that putatively adaptive alleles (F and d outliers) tend to occur more often in regions of low recombination in populations where divergent selection and gene flow have jointly occurred. This result remained significant when we employed different genomic window sizes, controlled for the effects of mutation rate and gene density, controlled for overall genetic differentiation, varied the genetic map used to estimate recombination and used a continuous (rather than discrete) measure of geographic distance as proxy for gene flow/shared ancestry. We argue that our study provides the first statistical evidence that the interaction of gene flow and selection biases divergence toward regions of low recombination.

Ancient genomic variation underlies repeated ecological adaptation in young stickleback populations

“…; Samuk et al. ) and emphasizes the degree to which gene flow among divergently adapted stickleback populations has impacted global genomic diversity.…”

“…; Samuk et al. ). Marine stickleback have repeatedly colonized freshwater lakes and streams (Bell and Foster ; Jones et al.…”

Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa

“…Outlier detection software that scan the genome for large effect loci are thus not capable of providing a complete picture of the genetic architecture of thermal tolerance in corals. However, when gene flow is high, as in most broadcast-spawning corals, adaptation favors the tight clustering of these small effect loci into regions of reduced genetic distance and into areas under low recombination (Thompson and Jiggins, 2014;Samuk et al, 2017). In this case, even though a large number of genes may contribute to phenotypic variation, specific chromosomal regions may play a particularly important role in driving evolutionary change.…”

“…Experimental designs taking advantage of phenotypic variation within and among populations spread across variable environments may help identify these regions. The best example of this in natural populations comes from a recent metaanalysis on threespine stickelbacks, where genomic data from 52 populations showed statistically that adaptive alleles tend to cluster together on chromosomal regions of low recombination (Samuk et al, 2017).…”

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

“…Linkage disequilibrium, and thereby the ability to detect genomic regions showing high divergence, varied across populations but was overall stronger in the Danish relative to the Greenlandic system, and yet it was the system in Greenland that showed pronounced genomic parallelism. There is also emerging evidence that adaptive alleles are not randomly distributed across genomes but tend to accumulate in low‐recombining regions (Berner & Roesti, ; Samuk et al., ). However, it seems unlikely that differences should exist in low‐recombining regions between the Danish and Greenlandic systems that could explain the different outcomes with respect to parallelism.…”