Different mechanisms drive the maintenance of polymorphism at loci subject to strong versus weak fluctuating selection
The long-running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally oscillating polymorphisms in wild Drosophila, possibly stabilized by an alternating summer-winter selection regime. Historically, there has been...
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Published in | Evolution Vol. 73; no. 5; pp. 883 - 896 |
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Main Authors | , |
Format | Journal Article |
Language | English |
Published |
United States
Wiley
01.05.2019
Oxford University Press |
Subjects | |
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Abstract | The long-running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally oscillating polymorphisms in wild Drosophila, possibly stabilized by an alternating summer-winter selection regime. Historically, there has been skepticism about the potential of temporal variation to balance polymorphism, because selection must be strong to have a meaningful stabilizing effect—unless dominance also varies over time (“reversal of dominance”). Here, we develop a simplified model of seasonally variable selection that simultaneously incorporates four different stabilizing mechanisms, including two genetic mechanisms (“cumulative overdominance” and reversal of dominance), as well as ecological “storage” (“protection from selection” and boom-bust demography). We use our model to compare the stabilizing effects of these mechanisms. Although reversal of dominance has by far the greatest stabilizing effect, we argue that the three other mechanisms could also stabilize polymorphism under plausible conditions, particularly when all three are present. With many loci subject to diminishing returns epistasis, reversal of dominance stabilizes many alleles of small effect. This makes the combination of the other three mechanisms, which are incapable of stabilizing small effect alleles, a better candidate for stabilizing the detectable frequency oscillations of large effect alleles. |
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AbstractList | The long‐running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally oscillating polymorphisms in wild Drosophila, possibly stabilized by an alternating summer‐winter selection regime. Historically, there has been skepticism about the potential of temporal variation to balance polymorphism, because selection must be strong to have a meaningful stabilizing effect—unless dominance also varies over time (“reversal of dominance”). Here, we develop a simplified model of seasonally variable selection that simultaneously incorporates four different stabilizing mechanisms, including two genetic mechanisms (“cumulative overdominance” and reversal of dominance), as well as ecological “storage” (“protection from selection” and boom‐bust demography). We use our model to compare the stabilizing effects of these mechanisms. Although reversal of dominance has by far the greatest stabilizing effect, we argue that the three other mechanisms could also stabilize polymorphism under plausible conditions, particularly when all three are present. With many loci subject to diminishing returns epistasis, reversal of dominance stabilizes many alleles of small effect. This makes the combination of the other three mechanisms, which are incapable of stabilizing small effect alleles, a better candidate for stabilizing the detectable frequency oscillations of large effect alleles. The long-running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally oscillating polymorphisms in wild Drosophila, possibly stabilized by an alternating summer-winter selection regime. Historically, there has been skepticism about the potential of temporal variation to balance polymorphism, because selection must be strong to have a meaningful stabilizing effect-unless dominance also varies over time ("reversal of dominance"). Here, we develop a simplified model of seasonally variable selection that simultaneously incorporates four different stabilizing mechanisms, including two genetic mechanisms ("cumulative overdominance" and reversal of dominance), as well as ecological "storage" ("protection from selection" and boom-bust demography). We use our model to compare the stabilizing effects of these mechanisms. Although reversal of dominance has by far the greatest stabilizing effect, we argue that the three other mechanisms could also stabilize polymorphism under plausible conditions, particularly when all three are present. With many loci subject to diminishing returns epistasis, reversal of dominance stabilizes many alleles of small effect. This makes the combination of the other three mechanisms, which are incapable of stabilizing small effect alleles, a better candidate for stabilizing the detectable frequency oscillations of large effect alleles. The long-running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally oscillating polymorphisms in wild Drosophila, possibly stabilized by an alternating summer-winter selection regime. Historically, there has been skepticism about the potential of temporal variation to balance polymorphism, because selection must be strong to have a meaningful stabilizing effect-unless dominance also varies over time ("reversal of dominance"). Here, we develop a simplified model of seasonally variable selection that simultaneously incorporates four different stabilizing mechanisms, including two genetic mechanisms ("cumulative overdominance" and reversal of dominance), as well as ecological "storage" ("protection from selection" and boom-bust demography). We use our model to compare the stabilizing effects of these mechanisms. Although reversal of dominance has by far the greatest stabilizing effect, we argue that the three other mechanisms could also stabilize polymorphism under plausible conditions, particularly when all three are present. With many loci subject to diminishing returns epistasis, reversal of dominance stabilizes many alleles of small effect. This makes the combination of the other three mechanisms, which are incapable of stabilizing small effect alleles, a better candidate for stabilizing the detectable frequency oscillations of large effect alleles.The long-running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally oscillating polymorphisms in wild Drosophila, possibly stabilized by an alternating summer-winter selection regime. Historically, there has been skepticism about the potential of temporal variation to balance polymorphism, because selection must be strong to have a meaningful stabilizing effect-unless dominance also varies over time ("reversal of dominance"). Here, we develop a simplified model of seasonally variable selection that simultaneously incorporates four different stabilizing mechanisms, including two genetic mechanisms ("cumulative overdominance" and reversal of dominance), as well as ecological "storage" ("protection from selection" and boom-bust demography). We use our model to compare the stabilizing effects of these mechanisms. Although reversal of dominance has by far the greatest stabilizing effect, we argue that the three other mechanisms could also stabilize polymorphism under plausible conditions, particularly when all three are present. With many loci subject to diminishing returns epistasis, reversal of dominance stabilizes many alleles of small effect. This makes the combination of the other three mechanisms, which are incapable of stabilizing small effect alleles, a better candidate for stabilizing the detectable frequency oscillations of large effect alleles. |
Author | Bertram, Jason Masel, Joanna |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30883731$$D View this record in MEDLINE/PubMed |
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Snippet | The long-running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally... The long‐running debate about the role of selection in maintaining genetic variation has been given new impetus by the discovery of hundreds of seasonally... |
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SubjectTerms | Alleles Autosomal dominant inheritance Balancing selection Demography Dominance Economic conditions eco‐evolutionary dynamics Epistasis Fruit flies Genetic diversity Loci ORIGINAL ARTICLE Oscillations polygenic adaptation Polymorphism rapid adaptation Temporal variations |
Title | Different mechanisms drive the maintenance of polymorphism at loci subject to strong versus weak fluctuating selection |
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