When maladaptive gene flow does not increase selection

Rolshausen, Gregor; Muttalib, Shahin; Oke, Krista B.; Hanson, Dieta; Hendry, Andrew P.

doi:10.1111/evo.12739

Cited by 12 publications

(17 citation statements)

References 93 publications

(148 reference statements)

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“…Thus, the effects of any population‐specific selective sweeps were balanced between comparisons of regimes. It should be noted that the connection between gene flow and the strength of selection is by no means well characterized—indeed under some circumstances, gene flow may actually decrease the strength of divergent selection (Rolshausen et al., ), and selection itself often alters the overall migration rate (Peterson, Hilborn, & Hauser, ).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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“…We performed a multivariate analysis of variance (MANOVA) using Wilks' lambda (k) as the test statistic. The PCs derived from the 36 Procrustes residuals were allometrically adjusted for centroid size and body depth using the common within-group slope approach described above (Reist, 1986;Lleonart et al, 2000;Rolshausen et al, 2015). The PCs were then used as the dependent variables with presence of steelhead, presence of sculpin and population as fixed explanatory variables.…”

Section: Geometric Morphometricsmentioning

confidence: 99%

Adaptation in temporally variable environments: stickleback armor in periodically breaching bar‐built estuaries

Paccard

Wasserman

Hanson

et al. 2018

J of Evolutionary Biology

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The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar-built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re-form within a few weeks or months, thereby re-isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within-population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes Eda and Pitx1 and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among-population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within-population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype and the presence of predators, thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within-population variation while reducing, but not eliminating, among-population variation driven by spatial environmental variation.

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“…A second limitation is that the strong circumstantial evidence for adaptive divergence (inferred from parallel evolution and/or regions of high genomic divergence; see Table S1), is not backed up by clear experimental or observational support for reciprocal divergent natural selection in nature. Lake and stream stickleback have been subjected to multiple transplant experiments and markrecapture studies to test for local adaptation or divergent selection (Hendry et al 2002;Räsänen and Hendry 2008;Raeymaekers et al 2010;Räsänen et al 2012;Rolshausen et al 2015;Stutz and Bolnick unpubl. ms.).…”

Section: Study Systemmentioning

confidence: 99%

“…An unpublished study by Stutz and Bolnick similarly found an advantage of stream fish in both habitats, which would not lead to genetic divergence. Other studies have failed to detect phenotypic selection against lake-like phenotypes in one or more streams (e.g., Rolshausen et al 2015). It is certainly possible that such studies simply have been unlucky (conducted in years when habitat-specific selection is low or absent), examined a life-history stage or trait on which selection is weak, or been underpowered.…”

Section: Study Systemmentioning

confidence: 99%

Partitioning the effects of isolation by distance, environment, and physical barriers on genomic divergence between parapatric threespine stickleback

et al. 2016

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Genetic divergence between populations is shaped by a combination of drift, migration, and selection, yielding patterns of isolation-by-distance (IBD) and isolation-by-environment (IBE). Unfortunately, IBD and IBE may be confounded when comparing divergence across habitat boundaries. For instance, parapatric lake and stream threespine stickleback (Gasterosteus aculeatus) may have diverged due to selection against migrants (IBE), or mere spatial separation (IBD). To quantitatively partition the strength of IBE and IBD, we used recently developed population genetic software (BEDASSLE) to analyze partial genomic data from three lake-stream clines on Vancouver Island. We find support for IBD within each of three outlet streams (unlike prior studies of lake-stream stickleback). In addition, we find evidence for IBE (controlling for geographic distance): the genetic effect of habitat is equivalent to geographic separation of ∼1.9 km of IBD. Remarkably, of our three lake-stream pairs, IBE is strongest where migration between habitats is easiest. Such microgeographic genetic divergence would require exceptionally strong divergent selection, which multiple experiments have failed to detect. Instead, we propose that nonrandom dispersal (e.g., habitat choice) contributes to IBE. Supporting this conclusion, we show that the few migrants between habitats are a nonrandom subset of the phenotype distribution of the source population.

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When maladaptive gene flow does not increase selection

Cited by 12 publications

References 93 publications

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

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

Adaptation in temporally variable environments: stickleback armor in periodically breaching bar‐built estuaries

Partitioning the effects of isolation by distance, environment, and physical barriers on genomic divergence between parapatric threespine stickleback

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