Genomics of local adaptation with gene flow

Abstract

Gene flow is a fundamental evolutionary force in adaptation that is especially important to understand as humans are rapidly changing both the natural environment and natural levels of gene flow. Theory proposes a multifaceted role for gene flow in adaptation, but it focuses mainly on the disruptive effect that gene flow has on adaptation when selection is not strong enough to prevent the loss of locally adapted alleles. The role of gene flow in adaptation is now better understood due to the recent development of both genomic models of adaptive evolution and genomic techniques, which both point to the importance of genetic architecture in the origin and maintenance of adaptation with gene flow. In this review, we discuss three main topics on the genomics of adaptation with gene flow. First, we investigate selection on migration and gene flow. Second, we discuss the three potential sources of adaptive variation in relation to the role of gene flow in the origin of adaptation. Third, we explain how local adaptation is maintained despite gene flow: we provide a synthesis of recent genomic models of adaptation, discuss the genomic mechanisms and review empirical studies on the genomics of adaptation with gene flow. Despite predictions on the disruptive effect of gene flow in adaptation, an increasing number of studies show that gene flow can promote adaptation, that local adaptations can be maintained despite high gene flow, and that genetic architecture plays a fundamental role in the origin and maintenance of local adaptation with gene flow.

Outlier analyses to test for local adaptation to breeding grounds in a migratory arctic seabird

“…Whole‐genome analyses are starting to show that this heterogeneous genomic landscape is due not only to locally varying gene flow‐selection balance but also to varying recombination rates across the genome, based on the observation that areas of differentiation seem often to be localized in areas of low recombination (Burri et al., 2015; Tigano & Friesen, 2016). In the future, higher genomic coverage will allow us to test the role of recombination in maintaining few differentiated loci against a homogeneous genomic background in this study system.…”

“…Adaptation is predicted to evolve faster in large populations compared to small ones (Lanfear, Kokko, & Eyre‐Walker, 2014), and murres have large genetically effective population sizes (Birt‐Friesen, Montevecchi, Gaston, & Davidson, 1992). Gene flow can hamper adaptation (reviewed in Tigano & Friesen, 2016), but gene flow among thick‐billed murres from different colonies is probably very low because of their strong philopatry (Gaston, DeForest, Donaldson, & Noble, 1994; Steiner & Gaston, 2005). However, previous studies based on mitochondrial and microsatellite markers indicated that population structure is lacking within the Atlantic Ocean in thick‐billed murres, despite their philopatric behavior (Birt‐Friesen et al., 1992; Tigano et al., 2015).…”

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

“…Local adaptation, however, is a balance between selection and gene flow. When gene flow is high, gene swamping can replace locally-adapted alleles with maladaptive ones, and genetic differences between populations are eroded (Tigano and Friesen, 2016). If selection is strong enough to overwhelm the homogenizing effects of gene flow, then locally adapted alleles maintain moderate levels of frequency in the population, and genetic variation is maintained.…”

Towards the Genomic Basis of Local Adaptation in Landraces

“…Adaptive divergence in quantitative traits is negatively correlated with the rate of population mixing [38], which suggests that LA should be also common in recently introduced landraces (i.e., a relatively reduced number of generations experiencing specific selective regimes). On the other hand, gene flow between populations, which is generally seen as a disruptive force for LA in the absence of strong adaptive selection [39], is more frequent for landraces within some centers of origin [40].…”

“…Adaptive divergence in quantitative traits is negatively correlated with the rate of population mixing [38], which suggests that LA should be also common in recently introduced landraces (i.e., a relatively reduced number of generations experiencing specific selective regimes). On the other hand, gene flow between populations, which is generally seen as a disruptive force for LA in the absence of strong adaptive selection [39], is more frequent for landraces within some centers of origin [40].Establishing how populations respond to environmental conditions is not an easy challenge in agriculture as well asevolutionary biology [41]. The positive features of landraces are often linked to specific growing techniques and environmental conditions that cannot be easily reproduced in experimental stations, such as low-fertility soil [42].…”