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Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila.

Bergland AO, Behrman EL, O'Brien KR, Schmidt PS, Petrov DA - PLoS Genet. (2014)

Bottom Line: We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection.We show that these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes.In addition, our results suggest that adaptively oscillating polymorphisms are likely millions of years old, with some possibly predating the divergence between D. melanogaster and D. simulans.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Stanford University, Stanford, California, United States of America.

ABSTRACT
In many species, genomic data have revealed pervasive adaptive evolution indicated by the fixation of beneficial alleles. However, when selection pressures are highly variable along a species' range or through time adaptive alleles may persist at intermediate frequencies for long periods. So called "balanced polymorphisms" have long been understood to be an important component of standing genetic variation, yet direct evidence of the strength of balancing selection and the stability and prevalence of balanced polymorphisms has remained elusive. We hypothesized that environmental fluctuations among seasons in a North American orchard would impose temporally variable selection on Drosophila melanogaster that would drive repeatable adaptive oscillations at balanced polymorphisms. We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection. We show that these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes. In addition, our results suggest that adaptively oscillating polymorphisms are likely millions of years old, with some possibly predating the divergence between D. melanogaster and D. simulans. Taken together, our results are consistent with a model of balancing selection wherein rapid temporal fluctuations in climate over generational time promotes adaptive genetic diversity at loci underlying polygenic variation in fitness related phenotypes.

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Demographic models.(A) Expected value of FST between simulated spring and fall samples (y-axis), conditional on overwintering effective population size and the number of seasonally adaptive alleles (color key). Dotted line represents observed average, genome-wide after FST between spring and fall samples from the Pennsylvanian population. (B) Expected number of SNPs that would vary repeatedly between seasons three times in a row conditional on founding deme size for a simple model of recolonization of the orchard population. Dotted line represents the observed number of seasonal SNPs and the corresponding founding deme size required, in this case 5 flies. (C) Minimum population size (y-axis) for the required for varying number of seasonally selected loci (x-axis) under a truncation selection model assuming independent response to selection at each locus. Dotted line represents our best guess of fall population size and corresponding number of loci that could independently respond to truncation selection. Confidence bands based on resampling of observed allele frequency change at seasonal SNPs.
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pgen-1004775-g007: Demographic models.(A) Expected value of FST between simulated spring and fall samples (y-axis), conditional on overwintering effective population size and the number of seasonally adaptive alleles (color key). Dotted line represents observed average, genome-wide after FST between spring and fall samples from the Pennsylvanian population. (B) Expected number of SNPs that would vary repeatedly between seasons three times in a row conditional on founding deme size for a simple model of recolonization of the orchard population. Dotted line represents the observed number of seasonal SNPs and the corresponding founding deme size required, in this case 5 flies. (C) Minimum population size (y-axis) for the required for varying number of seasonally selected loci (x-axis) under a truncation selection model assuming independent response to selection at each locus. Dotted line represents our best guess of fall population size and corresponding number of loci that could independently respond to truncation selection. Confidence bands based on resampling of observed allele frequency change at seasonal SNPs.

Mentions: In the absence of seasonal selection, these forward simulations suggest that overwintering Ne would have to be exceedingly low (∼20; Fig. 7A) to generate levels of FST between spring and fall as high as we observe in our data (arrow in Fig. 1C). However, with overwintering Ne of 200 and 5–10 seasonally adaptive SNPs per chromosome arm, simulated FST at neutral loci is on the order of 0.002 (Fig. 7A), which we observe in our data (arrow in Fig. 1C). While we do not know overwintering population size, we speculate it could be on the order of 200 flies or likely substantially larger [61], [62] and conclude that at least 25–50 (5–10 per main chromosome arm) loci are sufficient to generate patterns of differentiation we observe through time. Note that increasing the overwintering population size requires concomitant increase in number of seasonally selected loci.


Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila.

Bergland AO, Behrman EL, O'Brien KR, Schmidt PS, Petrov DA - PLoS Genet. (2014)

Demographic models.(A) Expected value of FST between simulated spring and fall samples (y-axis), conditional on overwintering effective population size and the number of seasonally adaptive alleles (color key). Dotted line represents observed average, genome-wide after FST between spring and fall samples from the Pennsylvanian population. (B) Expected number of SNPs that would vary repeatedly between seasons three times in a row conditional on founding deme size for a simple model of recolonization of the orchard population. Dotted line represents the observed number of seasonal SNPs and the corresponding founding deme size required, in this case 5 flies. (C) Minimum population size (y-axis) for the required for varying number of seasonally selected loci (x-axis) under a truncation selection model assuming independent response to selection at each locus. Dotted line represents our best guess of fall population size and corresponding number of loci that could independently respond to truncation selection. Confidence bands based on resampling of observed allele frequency change at seasonal SNPs.
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getmorefigures.php?uid=PMC4222749&req=5

pgen-1004775-g007: Demographic models.(A) Expected value of FST between simulated spring and fall samples (y-axis), conditional on overwintering effective population size and the number of seasonally adaptive alleles (color key). Dotted line represents observed average, genome-wide after FST between spring and fall samples from the Pennsylvanian population. (B) Expected number of SNPs that would vary repeatedly between seasons three times in a row conditional on founding deme size for a simple model of recolonization of the orchard population. Dotted line represents the observed number of seasonal SNPs and the corresponding founding deme size required, in this case 5 flies. (C) Minimum population size (y-axis) for the required for varying number of seasonally selected loci (x-axis) under a truncation selection model assuming independent response to selection at each locus. Dotted line represents our best guess of fall population size and corresponding number of loci that could independently respond to truncation selection. Confidence bands based on resampling of observed allele frequency change at seasonal SNPs.
Mentions: In the absence of seasonal selection, these forward simulations suggest that overwintering Ne would have to be exceedingly low (∼20; Fig. 7A) to generate levels of FST between spring and fall as high as we observe in our data (arrow in Fig. 1C). However, with overwintering Ne of 200 and 5–10 seasonally adaptive SNPs per chromosome arm, simulated FST at neutral loci is on the order of 0.002 (Fig. 7A), which we observe in our data (arrow in Fig. 1C). While we do not know overwintering population size, we speculate it could be on the order of 200 flies or likely substantially larger [61], [62] and conclude that at least 25–50 (5–10 per main chromosome arm) loci are sufficient to generate patterns of differentiation we observe through time. Note that increasing the overwintering population size requires concomitant increase in number of seasonally selected loci.

Bottom Line: We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection.We show that these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes.In addition, our results suggest that adaptively oscillating polymorphisms are likely millions of years old, with some possibly predating the divergence between D. melanogaster and D. simulans.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Stanford University, Stanford, California, United States of America.

ABSTRACT
In many species, genomic data have revealed pervasive adaptive evolution indicated by the fixation of beneficial alleles. However, when selection pressures are highly variable along a species' range or through time adaptive alleles may persist at intermediate frequencies for long periods. So called "balanced polymorphisms" have long been understood to be an important component of standing genetic variation, yet direct evidence of the strength of balancing selection and the stability and prevalence of balanced polymorphisms has remained elusive. We hypothesized that environmental fluctuations among seasons in a North American orchard would impose temporally variable selection on Drosophila melanogaster that would drive repeatable adaptive oscillations at balanced polymorphisms. We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection. We show that these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes. In addition, our results suggest that adaptively oscillating polymorphisms are likely millions of years old, with some possibly predating the divergence between D. melanogaster and D. simulans. Taken together, our results are consistent with a model of balancing selection wherein rapid temporal fluctuations in climate over generational time promotes adaptive genetic diversity at loci underlying polygenic variation in fitness related phenotypes.

Show MeSH
Related in: MedlinePlus