Genomic Evidence of Rapid and Stable Adaptive Oscillations over Seasonal Time Scales in Drosophila

Bergland, Alan O.; Behrman, Emily L.; O’Brien, Katherine R.; Schmidt, Paul S.; Petrov, Dmitri A.

doi:10.1371/journal.pgen.1004775

Cited by 497 publications

(889 citation statements)

References 136 publications

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“…The fixation probability is also higher if the environmental changes are slower. year (10 generations) (2). Although the oscillations in many of these SNPs are likely driven by linkage to other seasonally selected sites, these data suggest that there are at least some driver alleles with sτ ≈ 1.…”

Section: Discussionmentioning

confidence: 82%

“…For example, drug resistance mutations often carry a cost when the dosage of the drug decays (1), and seasonal variations in climate can differentially select for certain alleles in the summer or winter (2). Similarly, laboratory adaptation to specific temperatures (3,4) or particular nutrient sources (5,6) often leads to declines in fitness in other conditions.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Fate of a mutation in a fluctuating environment

Cvijović

Good

Jerison

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

140

134

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Natural environments are never truly constant, but the evolutionary implications of temporally varying selection pressures remain poorly understood. Here we investigate how the fate of a new mutation in a fluctuating environment depends on the dynamics of environmental variation and on the selective pressures in each condition. We find that even when a mutation experiences many environmental epochs before fixing or going extinct, its fate is not necessarily determined by its time-averaged selective effect. Instead, environmental variability reduces the efficiency of selection across a broad parameter regime, rendering selection unable to distinguish between mutations that are substantially beneficial and substantially deleterious on average. Temporal fluctuations can also dramatically increase fixation probabilities, often making the details of these fluctuations more important than the average selection pressures acting on each new mutation. For example, mutations that result in a trade-off between conditions but are strongly deleterious on average can nevertheless be more likely to fix than mutations that are always neutral or beneficial. These effects can have important implications for patterns of molecular evolution in variable environments, and they suggest that it may often be difficult for populations to maintain specialist traits, even when their loss leads to a decline in time-averaged fitness.population genetics | fixation probability | fluctuating environment | effective diffusion E volutionary trade-offs are widespread: Adaptation to one environment often leads to costs in other conditions. For example, drug resistance mutations often carry a cost when the dosage of the drug decays (1), and seasonal variations in climate can differentially select for certain alleles in the summer or winter (2). Similarly, laboratory adaptation to specific temperatures (3, 4) or particular nutrient sources (5, 6) often leads to declines in fitness in other conditions. Related trade-offs apply to any specialist phenotype or regulatory system that incurs a general cost to confer benefits in specific environmental conditions (7). Despite the ubiquity of these trade-offs, it is not always easy to predict when a specialist phenotype can evolve and persist. How useful must a trait be on average to be maintained? How regularly does it need to be useful? How much easier is it to maintain in a larger population compared with a smaller one?The answers to these questions depend on two major factors. First, how often do new mutations create or destroy a specialist phenotype, and what are their typical costs and benefits across environmental conditions? This is fundamentally an empirical question, which depends on the costs and benefits of the trait in question, as well as its genetic architecture (e.g., the target size for loss-of-function mutations that disable a regulatory system). In this paper, we focus instead on the second major factor: given that a particular mutation occurs, how does its long-term fate depend on its fitn...

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Section: Discussionmentioning

confidence: 82%

mentioning

confidence: 99%

Fate of a mutation in a fluctuating environment

Cvijović

Good

Jerison

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

140

134

View full text Add to dashboard Cite

show abstract

“…This is because both sexes share many metabolic traits which are under selection to optimize contrasting reproductive demands between the sexes. Alternatively, both epistatic (He, Qian, Wang, Li, & Zhang, 2010; Jakubowska & Korona, 2012; Jasnos & Korona, 2007) and/or balancing selection via temporal variation in environmental conditions (Bergland, Behrman, O'Brien, Schmidt, & Petrov, 2014) could also be mechanisms to maintain genetic variance. One study has found season‐dependent oscillating patterns of allele frequency change of central metabolic and nutrient sensing genes (Cogni et al., 2015).…”

Section: Discussionmentioning

confidence: 99%

Dietary choices are influenced by genotype, mating status, and sex in Drosophila melanogaster

Camus

Huang

Reuter

et al. 2018

Ecology and Evolution

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Mating causes many changes in physiology, behavior, and gene expression in a wide range of organisms. These changes are predicted to be sex specific, influenced by the divergent reproductive roles of the sexes. In female insects, mating is associated with an increase in egg production which requires high levels of nutritional input with direct consequences for the physiological needs of individual females. Consequently, females alter their nutritional acquisition in line with the physiological demands imposed by mating. Although much is known about the female mating‐induced nutritional response, far less is known about changes in males. In addition, it is unknown whether variation between genotypes translates into variation in dietary behavioral responses. Here we examine mating‐induced shifts in male and female dietary preferences across genotypes of Drosophila melanogaster. We find sex‐ and genotype‐specific effects on both the quantity and quality of the chosen diet. These results contribute to our understanding of sex‐specific metabolism and reveal genotypic variation that influences responses to physiological demands.

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“…Species that we intend to kill tend to have very large population sizes and short generation times (e.g., insects, weeds, bacteria, viruses), and those species that we care about conserving tend to be larger bodied animals with relatively small population sizes and long generation times (e.g., most vertebrates). Short generation times allow evolutionary change to closely track the pace of environmental change (see, e.g., Bergland, Behrman, O'Brien, Schmidt, Petrov, 2014), thus minimizing the mismatch between physiological tolerance and the degree of environmental change. Large population sizes are important to buffer a species from stochastic extinction following rapid population decline in response to abrupt environmental change (Bell & Gonzalez, 2009).…”

Section: Natural Selection and Adaptive Responses To Rapidly Changingmentioning

confidence: 99%

When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations

Whitehead

Clark

Reid

et al. 2017

Evolutionary Applications

120

102

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For most species, evolutionary adaptation is not expected to be sufficiently rapid to buffer the effects of human‐mediated environmental changes, including environmental pollution. Here we review how key features of populations, the characteristics of environmental pollution, and the genetic architecture underlying adaptive traits, may interact to shape the likelihood of evolutionary rescue from pollution. Large populations of Atlantic killifish (Fundulus heteroclitus) persist in some of the most contaminated estuaries of the United States, and killifish studies have provided some of the first insights into the types of genomic changes that enable rapid evolutionary rescue from complexly degraded environments. We describe how selection by industrial pollutants and other stressors has acted on multiple populations of killifish and posit that extreme nucleotide diversity uniquely positions this species for successful evolutionary adaptation. Mechanistic studies have identified some of the genetic underpinnings of adaptation to a well‐studied class of toxic pollutants; however, multiple genetic regions under selection in wild populations seem to reflect more complex responses to diverse native stressors and/or compensatory responses to primary adaptation. The discovery of these pollution‐adapted killifish populations suggests that the evolutionary influence of anthropogenic stressors as selective agents occurs widely. Yet adaptation to chemical pollution in terrestrial and aquatic vertebrate wildlife may rarely be a successful “solution to pollution” because potentially adaptive phenotypes may be complex and incur fitness costs, and therefore be unlikely to evolve quickly enough, especially in species with small population sizes.

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Genomic Evidence of Rapid and Stable Adaptive Oscillations over Seasonal Time Scales in Drosophila

Cited by 497 publications

References 136 publications

Fate of a mutation in a fluctuating environment

Fate of a mutation in a fluctuating environment

Dietary choices are influenced by genotype, mating status, and sex in Drosophila melanogaster

When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations

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