Varied Genomic Responses to Maladaptive Gene Flow and Their Evidence

Roesti, Marius

doi:10.3390/genes9060298

Cited by 14 publications

(19 citation statements)

References 120 publications

(168 reference statements)

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“…However, these estimates are upwardly biased since only significant QTLs are considered and effects of QTLs in low recombination regions are generally overestimated (Noor et al. 2001; Roesti 2018).…”

Section: Resultsmentioning

confidence: 99%

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Genetic variation for adaptive traits is associated with polymorphic inversions inLittorina saxatilis

et al. 2021

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Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance for local adaptation we need to know their influence on phenotypes under divergent selection. For this, the marine snail Littorina saxatilis provides an ideal study system. Divergent ecotypes adapted to wave action and crab predation occur in close proximity on intertidal shores with gene flow between them. Here, we used F2 individuals obtained from crosses between the ecotypes to test for associations between genomic regions and traits distinguishing the Crab‐/Wave‐adapted ecotypes including size, shape, shell thickness, and behavior. We show that most of these traits are influenced by two previously detected inversion regions that are divergent between ecotypes. We thus gain a better understanding of one important underlying mechanism responsible for the rapid and repeated formation of ecotypes: divergent selection acting on inversions. We also found that some inversions contributed to more than one trait suggesting that they may contain several loci involved in adaptation, consistent with the hypothesis that suppression of recombination within inversions facilitates differentiation in the presence of gene flow.

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Section: Resultsmentioning

confidence: 99%

“…However, inversions, large blocks with little to no recombination, may lead to a detection bias toward these regions (Noor et al. 2001; Roesti 2018). Even without a clustering of important loci in these regions, statistical power for any association analysis between genetic markers and phenotypes is increased.…”

Section: Discussionmentioning

confidence: 99%

Genetic variation for adaptive traits is associated with polymorphic inversions inLittorina saxatilis

et al. 2021

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“…On the positive side, peripheral populations are prone to be under environmentally driven heterogeneous selection that is necessary for local adaptation to occur (Gavrilets, 2004). On the negative side, theory predicts that the genetic and demographic characteristics of marginal populations counteract local selection with varying intensities, causing 'maladaptation' sometimes, enhancing the evolutionary potential of small populations others (Kawecki, 2008;Roesti, 2018).…”

Section: Challenges To Local Adaptation Inferencesmentioning

confidence: 99%

Adaptive Introgression Promotes Fast Adaptation In Oaks Marginal Populations

Goicoechea

Guillardín

Fernández‐Ibarrondo

et al. 2019

Preprint

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Range shifts and species range limits are two fundamental, related processes in population and evolutionary genetics that have received much attention since a large impact of climate change in species' distributions was predicted. In general, there is a broad consensus on the effects of abiotic interactions on range limits, but comprehensive evidence supporting/rejecting the impact of biotic interactions is lacking. Hybridization has long been recognized as a biotic interaction favoring marginal populations establishment and range expansion through transgressive segregation or adaptive introgression, but recently new roles have been claimed for hybridization, such as the trigger of adaptive radiations, or indirect effects on population sizes that would allow persistence until new mutations arises or the environment changes. In this work, we selected two Mediterranean oak species with ecological discrimination based on soil pH, and intensively sampled three interspecific pairs of marginal populations from taxon-extreme environments under heterogeneous climate conditions. We genotyped 110 EST-SSR markers evenly distributed across their genomes and applied a variety of population and landscape genetics models to validate candidate genes for local adaptation. Then, several introgression screens on shared candidates showed that the three inter-specific population pairs contain evidences of adaptive introgression and that events occur in both directions. Other significant findings from our work are: (i) Aproximate Bayesian Computation coupled to coalescent simulations supports small hybridization rates since recent secondary contact in two population pairs affected by Quaternary climatic oscillations but continuous old interspecific gene flow in the pair less affected by climate, (ii) introgression at loci involved in local adaptations leads to strong geographic structure of marginal oak populations when sampling is large enough, and (iii) sampling efforts can be targeted to reveal different components of populations structure. Finally, we review evidences that support our conclusions and discuss some evolutionary implications of adaptive introgression on range expansion. Latitude Cross validation score Populations Populations K = 4 K = 5 d e f CAB CJA SN E FRO Q.faginea Q.pyrenaica

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“…Gene flow can be beneficial for maintaining population connectivity and genetic diversity by introducing novel genetic variation but it can also impede local adaptation by introducing maladaptive foreign alleles into a locally adapted populations (Bolnick & Nosil 2007). One potential evolutionary ‘solution’ that may minimize maladaptive effects of gene flow is for selection to favor clustered architectures of adaptation, where adaptive alleles are tightly linked and locally favorable combinations of alleles are protected from disruption via low recombination (Yeaman 2013; Roesti 2018).…”

Section: Introductionmentioning

confidence: 99%

“…This process can produce islands of differentiation spanning multiple megabases, as free recombination among populations is reduced due to assortative mating (Via 2012). Genomic rearrangements, such as chromosomal inversions, can also facilitate adaptation in the face of high gene flow and lead to genomic islands of differentiation (Hoffmann & Rieseberg 2008; Yeaman 2013; Tigano & Friesen 2016; Roesti 2018; Wellenreuther & Bernatchez 2018; Aguirre Liguori et al . 2019; Huang et al .…”

Section: Introductionmentioning

confidence: 99%

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

Shi

Bouska

et al. 2021

Preprint

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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.

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Varied Genomic Responses to Maladaptive Gene Flow and Their Evidence

Cited by 14 publications

References 120 publications

Genetic variation for adaptive traits is associated with polymorphic inversions inLittorina saxatilis

Genetic variation for adaptive traits is associated with polymorphic inversions inLittorina saxatilis

Adaptive Introgression Promotes Fast Adaptation In Oaks Marginal Populations

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

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