scholarly journals Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster

2019 ◽  
Author(s):  
Seth M. Rudman ◽  
Sharon Greenblum ◽  
Rachel C. Hughes ◽  
Subhash Rajpurohit ◽  
Ozan Kiratli ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Rapid Evolution ◽  
Natural Populations ◽  
Genomic Data ◽  
Allele Frequencies ◽  
Frequency Change ◽  
Microbiome Composition ◽  
Population Genomic ◽  
Genome Wide ◽  
Microbial Group

AbstractPopulation genomic data has revealed patterns of genetic variation associated with adaptation in many taxa. Yet understanding the adaptive process that drives such patterns is challenging - it requires disentangling the ecological agents of selection, determining the relevant timescales over which evolution occurs, and elucidating the genetic architecture of adaptation. Doing so for the adaptation of hosts to their microbiome is of particular interest with growing recognition of the importance and complexity of host-microbe interactions. Here, we track the pace and genomic architecture of adaptation to an experimental microbiome manipulation in replicate populations of Drosophila melanogaster in field mesocosms. Manipulation of the microbiome altered population dynamics and increased divergence between treatments in allele frequencies genome-wide, with regions showing strong divergence found on all chromosomes. Moreover, at divergent loci previously associated with adaptation across natural populations, we found that the more common allele in fly populations experimentally enriched for a certain microbial group was also more common in natural populations with high relative abundance of that microbial group. These results suggest that microbiomes may be an agent of selection that shapes the pattern and process of adaptation and, more broadly, that variation in a single ecological factor within a complex environment can drive rapid, polygenic adaptation over short timescales.Significance statementNatural selection can drive evolution over short timescales. However, there is little understanding of which ecological factors are capable of driving rapid evolution and how this rapid evolution alters allele frequencies across the genome. Here we combine a field experiment with population genomic data from natural populations across a latitudinal gradient to assess whether and how microbiome composition drives rapid genomic evolution of host populations. We find that differences in microbiome composition cause divergence in allele frequencies genome-wide, including in genes previously associated with local adaptation. Moreover, we observed concordance between experimental and natural populations in terms of the direction of allele frequency change, suggesting that microbiome composition may be an agent of selection that drives adaptation in the wild.

scholarly journals Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster

2019 ◽  
Vol 116 (40) ◽  
pp. 20025-20032 ◽  
Author(s):  
Seth M. Rudman ◽  
Sharon Greenblum ◽  
Rachel C. Hughes ◽  
Subhash Rajpurohit ◽  
Ozan Kiratli ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Natural Populations ◽  
Microbiome Composition ◽  
Adaptive Process ◽  
Population Genomic ◽  
Polygenic Adaptation ◽  
Microbial Group ◽  
Genomic Adaptation ◽  
Microbe Interactions ◽  
Host Microbe Interactions

Population genomic data has revealed patterns of genetic variation associated with adaptation in many taxa. Yet understanding the adaptive process that drives such patterns is challenging; it requires disentangling the ecological agents of selection, determining the relevant timescales over which evolution occurs, and elucidating the genetic architecture of adaptation. Doing so for the adaptation of hosts to their microbiome is of particular interest with growing recognition of the importance and complexity of host–microbe interactions. Here, we track the pace and genomic architecture of adaptation to an experimental microbiome manipulation in replicate populations of Drosophila melanogaster in field mesocosms. Shifts in microbiome composition altered population dynamics and led to divergence between treatments in allele frequencies, with regions showing strong divergence found on all chromosomes. Moreover, at divergent loci previously associated with adaptation across natural populations, we found that the more common allele in fly populations experimentally enriched for a certain microbial group was also more common in natural populations with high relative abundance of that microbial group. These results suggest that microbiomes may be an agent of selection that shapes the pattern and process of adaptation and, more broadly, that variation in a single ecological factor within a complex environment can drive rapid, polygenic adaptation over short timescales.

scholarly journals Estimating the genome-wide contribution of selection to temporal allele frequency change

2019 ◽  
Author(s):  
Vince Buffalo ◽  
Graham Coop
Keyword(s):  
Allele Frequency ◽  
Genetic Drift ◽  
Genomic Data ◽  
Allele Frequencies ◽  
Frequency Change ◽  
Standing Variation ◽  
Genome Wide ◽  
Selection Experiments ◽  
Frequency Changes ◽  
Linked Selection

AbstractRapid phenotypic adaptation is often observed in natural populations and selection experiments. However, detecting the genome-wide impact of this selection is difficult, since adaptation often proceeds from standing variation and selection on polygenic traits, both of which may leave faint genomic signals indistinguishable from a noisy background of genetic drift. One promising signal comes from the genome-wide covariance between allele frequency changes observable from temporal genomic data, e.g. evolve-and-resequence studies. These temporal covariances reflect how heritable fitness variation in the population leads changes in allele frequencies at one timepoint to be predictive of the changes at later timepoints, as alleles are indirectly selected due to remaining associations with selected alleles. Since genetic drift does not lead to temporal covariance, we can use these covariances to estimate what fraction of the variation in allele frequency change through time is driven by linked selection. Here, we reanalyze three selection experiments to quantify the effects of linked selection over short timescales using covariance among time-points and across replicates. We estimate that at least 17% to 37% of allele frequency change is driven by selection in these experiments. Against this background of positive genome-wide temporal covariances we also identify signals of negative temporal covariance corresponding to reversals in the direction of selection for a reasonable proportion of loci over the time course of a selection experiment. Overall, we find that in the three studies we analyzed, linked selection has a large impact on short-term allele frequency dynamics that is readily distinguishable from genetic drift.Significance StatementA long-standing problem in evolutionary biology is to understand the processes that shape the genetic composition of populations. In a population without migration, the two processes that change allele frequencies are selection, which increases beneficial alleles and removes deleterious ones, and genetic drift which randomly changes frequencies as some parents contribute more or less alleles to the next generation. Previous efforts to disentangle these processes have used genomic samples from a single timepoint and models of how selection affects neighboring sites (linked selection). Here, we use genomic data taken through time to quantify the contributions of selection and drift to genome-wide frequency changes. We show selection acts over short timescales in three evolve-and-resequence studies and has a sizable genome-wide impact.

When a Fly Has to Fly to Reproduce: Selection against Conditional Recessive Lethals in Drosophila

2010 ◽  
Vol 72 (1) ◽  
pp. 12-15 ◽  
Author(s):  
Andrea D. Plunkett ◽  
Lev Y. Yampolsky
Keyword(s):  
Drosophila Melanogaster ◽  
Allele Frequency ◽  
Experimental Model ◽  
Food Source ◽  
Allele Frequencies ◽  
Frequency Change ◽  
Evolutionary Patterns ◽  
Visible Marker ◽  
Meaningful Comparison ◽  
Marker Alleles

We propose an experimental model suitable for demonstrating allele frequency change in Drosophila melanogaster populations caused by selection against an easily scorable conditional lethal, namely recessive flightless alleles such as apterous and vestigial. Homozygotes for these alleles are excluded from reproduction because the food source used to establish each generation is accessible only by flight. The observed dynamics of flightless-allele frequencies generally follows the theoretically predicted pattern, with slight deviation toward less intense selection. We also suggest observing selection against flight-independent visible marker alleles in the same population as a meaningful comparison. The proposed experiments can easily be scheduled within one semester, and the expected data provide ample opportunities for discussion of quantitative evolutionary patterns.

scholarly journals The P-element strikes again: the recent invasion of naturalDrosophila simulanspopulations

2015 ◽  
Author(s):  
Robert Kofler ◽  
Tom Hill ◽  
Viola Nolte ◽  
Andrea Betancourt ◽  
Christian Schlötterer
Keyword(s):  
Drosophila Melanogaster ◽  
Defense Mechanisms ◽  
Natural Populations ◽  
Genomic Data ◽  
P Element ◽  
Expression Data ◽  
Transfer Event ◽  
P Elements ◽  
Origins Of Replication ◽  
Close Relatives

The P-element is one of the best understood eukaryotic transposable elements. It invadedDrosophila melanogasterpopulations within a few decades, but was thought to be absent from close relatives, includingD. simulans. Five decades after the spread inD. melanogaster, we provide evidence that the P-element has also invadedD. simulans. P-elements inD. simulansappear to have been acquired recently fromD. melanogasterprobably via a single horizontal transfer event. Expression data indicate that the P-element is processed in the germline ofD. simulans, and genomic data show an enrichment of P-element insertions in putative origins of replication, similar to that seen inD. melanogaster. This ongoing spread of the P-element in natural populations provides an unique opportunity to understand the dynamics of transposable element spreads and the associated piRNA defense mechanisms.

scholarly journals Pervasive Linked Selection and Intermediate-Frequency Alleles Are Implicated in an Evolve-and-Resequencing Experiment of Drosophila simulans

Genetics ◽  
2018 ◽  
Vol 211 (3) ◽  
pp. 943-961 ◽  
Author(s):  
John K. Kelly ◽  
Kimberly A. Hughes
Keyword(s):  
Balancing Selection ◽  
Parallel Evolution ◽  
Rapid Evolution ◽  
Natural Populations ◽  
Intermediate Frequency ◽  
Drosophila Simulans ◽  
Data Sets ◽  
Sequencing Data ◽  
Simulation Tools ◽  
Genome Wide

We develop analytical and simulation tools for evolve-and-resequencing experiments and apply them to a new study of rapid evolution in Drosophila simulans. Likelihood test statistics applied to pooled population sequencing data suggest parallel evolution of 138 SNPs across the genome. This number is reduced by orders of magnitude from previous studies (thousands or tens of thousands), owing to differences in both experimental design and statistical analysis. Whole genome simulations calibrated from Drosophila genetic data sets indicate that major features of the genome-wide response could be explained by as few as 30 loci under strong directional selection with a corresponding hitchhiking effect. Smaller effect loci are likely also responding, but are below the detection limit of the experiment. Finally, SNPs showing strong parallel evolution in the experiment are intermediate in frequency in the natural population (usually 30–70%) indicative of balancing selection in nature. These loci also exhibit elevated differentiation among natural populations of D. simulans, suggesting environmental heterogeneity as a potential balancing mechanism.

GENETIC ANALYSIS OF NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER IN JAPAN. IV. NATURAL SELECTION ON THE INDUCIBILITY, BUT NOT ON THE STRUCTURAL GENES, OF AMYLASE LOCI

Genetics ◽  
1984 ◽  
Vol 108 (4) ◽  
pp. 879-896
Author(s):  
Yoshinori Matsuo ◽  
Tsuneyuki Yamazaki
Keyword(s):  
Drosophila Melanogaster ◽  
Natural Selection ◽  
Specific Activity ◽  
Natural Populations ◽  
Fold Increase ◽  
Developmental Time ◽  
Frequency Change ◽  
Inducing Factors ◽  
Highly Correlated ◽  
The One

ABSTRACT To test the validity of previous results the inducibility of amylase as well as other biochemical parameters was measured using 45 homozygous strains of Drosophila melanogaster from Akayu, Japan. Only the inducibility (but not protein contents or specific activity of the enzyme) was highly correlated with productivity measured using a starch food regime (rp = 0.41, P < 0.005, rg = 0.73 ± 0.21). Inducibility was also negatively correlated with developmental time using starch food; namely, the one with high inducibility developed the fastest. Population cage experiments using 1600 genomes from the same natural population showed that the inducibility responded positively to natural selection (1.6-fold increase in inducibility in cages using starch food relative to those using normal food), but little frequency change of allozymes was observed. All of these results were consistent and indicated that polymorphisms of inducing factors or regulatory genes were major determinants of fitness differences in a particular environment and may be the genetic materials responsible for the adaptive evolution of organisms, at least in amylase loci.

scholarly journals Rapid Evolution of a Coadapted Gene Complex: Evidence From the Segregation Distorter (SD) System of Meiotic Drive in Drosophila melanogaster

Genetics ◽  
1996 ◽  
Vol 143 (4) ◽  
pp. 1675-1688 ◽  
Author(s):  
Michael F Palopoli ◽  
Chung-I Wu
Keyword(s):  
Drosophila Melanogaster ◽  
Rapid Evolution ◽  
Natural Populations ◽  
Meiotic Drive ◽  
Pericentromeric Region ◽  
Genomic Region ◽  
Gene Complex ◽  
Segregation Distorter ◽  
Normal Homologue ◽  
Coadapted Gene Complex

Abstract Segregation Distorter (SD) is a system of meiotic drive found in natural populations of Drosophila melanogaster. Males heterozygous for an SD second chromosome and a normal homologue (SD  +) produce predominantly SD-bearing sperm. The coadapted gene complex responsible for this transmission advantage spans the second chromosome centromere, consisting of three major and several minor interacting loci. To investigate the evolutionary history of this system, we surveyed levels of polymorphism and divergence at six genes that together encompass this pericentromeric region and span seven map units. Interestingly, there was no discernible divergence between SD and SD  + chromosomes for any of these molecular markers. Furthermore, SD chromosomes harbored much less polymorphism than did SD  + chromosomes. The results suggest that the SD system evolved recently, swept to appreciable frequencies worldwide, and carried with it the entire second chromosome centromeric region (roughly 10% of the genome). Despite its well-documented genetic complexity, this coadapted system appears to have evolved on a time scale that is much shorter than can be gauged using nucleotide substitution data. Finally, the large genomic region hitchhiking with SD indicates that a multilocus, epistatically selected system could affect the levels of DNA polymorphism observed in regions of reduced recombination.

scholarly journals Natural selection and parallel clinal and seasonal changes in Drosophila melanogaster

2020 ◽  
Author(s):  
Murillo F. Rodrigues ◽  
Maria D. Vibranovski ◽  
Rodrigo Cogni
Keyword(s):  
Drosophila Melanogaster ◽  
Seasonal Variation ◽  
Natural Selection ◽  
Allele Frequency ◽  
Allele Frequencies ◽  
Clinal Variation ◽  
Spatial And Seasonal Variation ◽  
Genome Wide ◽  
A Genome

AbstractSpatial and seasonal variation in the environment are ubiquitous. Environmental heterogeneity can affect natural populations and lead to covariation between environment and allele frequencies. Drosophila melanogaster is known to harbor polymorphisms that change both with latitude and seasons. Identifying the role of selection in driving these changes is not trivial, because non-adaptive processes can cause similar patterns. Given the environment changes in similar ways across seasons and along the latitudinal gradient, one promising approach may be to look for parallelism between clinal and seasonal change. Here, we test whether there is a genome-wide relationship between clinal and seasonal variation, and whether the pattern is consistent with selection. We investigate the role of natural selection in driving these allele frequency changes. Allele frequency estimates were obtained from pooled samples from seven different locations along the east coast of the US, and across seasons within Pennsylvania. We show that there is a genome-wide pattern of clinal variation mirroring seasonal variation, which cannot be explained by linked selection alone. This pattern is stronger for coding than intergenic regions, consistent with natural selection. We find that the genome-wide relationship between clinal and seasonal variation could be explained by about 4% of the common autosomal variants being under selection. Our results highlight the contribution of natural selection in driving fluctuations in allele frequencies in D. melanogaster.

scholarly journals Cross-Species association statistics for genome-wide studies of host and parasite polymorphism data

2019 ◽  
Author(s):  
Hanna Märkle ◽  
Aurélien Tellier ◽  
Sona John
Keyword(s):  
Statistical Power ◽  
Association Studies ◽  
Natural Populations ◽  
Genomic Data ◽  
Genome Wide Association Studies ◽  
Full Genome ◽  
Species Association ◽  
Genome Data ◽  
Genome Wide ◽  
The Cross

AbstractUncovering the genes governing host-parasite coevolution is of importance for disease management in agriculture and human medicine. The availability of increasing amounts of host and parasite full genome-data in recent times allows to perform cross-species genome-wide association studies based on sampling of genomic data of infected hosts and their associated parasites strains. We aim to understand the statistical power of such approaches. We develop two indices, the cross species association (CSA) and the cross species prevalence (CSP), the latter additionally incorporating genomic data from uninfected hosts. For both indices, we derive genome-wide significance thresholds by computing their expected distribution over unlinked neutral loci, i.e. those not involved in determining the outcome of interaction. Using a population genetics and an epidemiological coevolutionary model, we demonstrate that the statistical power of these indices to pinpoint the interacting loci in full genome data varies over time. This is due to the underlying GxG interactions and the coevolutionary dynamics. Under trench-warfare dynamics, CSA and CSP are very accurate in finding out the loci under coevolution, while under arms-race dynamics the power is limited especially under a gene-for-gene interaction. Furthermore, we reveal that the combination of both indices across time samples can be used to estimate the asymmetry of the underlying infection matrix. Our results provide novel insights into the power and biological interpretation of cross-species association studies using samples from natural populations or controlled experiments.

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