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 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 Parallel changes in gut microbiome composition and function in parallel local adaptation and speciation

2019 ◽  
Author(s):  
Diana J. Rennison ◽  
Seth M. Rudman ◽  
Dolph Schluter
Keyword(s):  
Microbial Communities ◽  
Local Adaptation ◽  
Biotic Interactions ◽  
Ecological Speciation ◽  
Microbiome Composition ◽  
Interacting Species ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
And Function ◽  
Host Evolution

AbstractThe processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic interactions drive evolution comes from repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet, relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we utilize three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host-microbe interactions might play an important role in host adaptation and diversification.

scholarly journals Health and disease markers correlate with gut microbiome composition across thousands of people

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Ohad Manor ◽  
Chengzhen L. Dai ◽  
Sergey A. Kornilov ◽  
Brett Smith ◽  
Nathan D. Price ◽  
...  
Keyword(s):  
Gut Microbiome ◽  
Lifestyle Factors ◽  
Clinical Markers ◽  
Human Gut ◽  
Microbiome Composition ◽  
Targeted Interventions ◽  
Human Gut Microbiome ◽  
Host Diet ◽  
Microbe Interactions ◽  
Host Microbe Interactions

Abstract Variation in the human gut microbiome can reflect host lifestyle and behaviors and influence disease biomarker levels in the blood. Understanding the relationships between gut microbes and host phenotypes are critical for understanding wellness and disease. Here, we examine associations between the gut microbiota and ~150 host phenotypic features across ~3,400 individuals. We identify major axes of taxonomic variance in the gut and a putative diversity maximum along the Firmicutes-to-Bacteroidetes axis. Our analyses reveal both known and unknown associations between microbiome composition and host clinical markers and lifestyle factors, including host-microbe associations that are composition-specific. These results suggest potential opportunities for targeted interventions that alter the composition of the microbiome to improve host health. By uncovering the interrelationships between host diet and lifestyle factors, clinical blood markers, and the human gut microbiome at the population-scale, our results serve as a roadmap for future studies on host-microbe interactions and interventions.

scholarly journals Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome

2021 ◽  
Vol 288 (1957) ◽  
pp. 20210552
Author(s):  
Xavier A. Harrison ◽  
Allan D. McDevitt ◽  
Jenny C. Dunn ◽  
Sarah M. Griffiths ◽  
Chiara Benvenuto ◽  
...  
Keyword(s):  
Bacterial Communities ◽  
Natural Populations ◽  
Sample Type ◽  
Fungal Community Composition ◽  
Tissue Storage ◽  
Bacterial Microbiome ◽  
Host Phylogeny ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Using Data

Interactions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Though recent research has highlighted the importance of interactions between animals and their bacterial communities, comparative evidence for fungi is lacking, especially in natural populations. Using data from 49 species, we present novel evidence of strong covariation between fungal and bacterial communities across the host phylogeny, indicative of recruitment by hosts for specific suites of microbes. Using co-occurrence networks, we demonstrate marked variation across host taxonomy in patterns of covariation between bacterial and fungal abundances. Host phylogeny drives differences in the overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in the mammalian gut microbiome. Sample type, tissue storage and DNA extraction method also affected bacterial and fungal community composition, and future studies would benefit from standardized approaches to sample processing. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host–microbe interactions.

scholarly journals The Evolution of Larger Size in High Altitude Drosophila melanogaster has a Polymorphic Genetic Architecture

2021 ◽  
Author(s):  
Quentin D Sprengelmeyer ◽  
Justin B Lack ◽  
Dylan T Braun ◽  
Matthew J Monette ◽  
John E. Pool
Keyword(s):  
Drosophila Melanogaster ◽  
Qtl Mapping ◽  
Genetic Architecture ◽  
Natural Populations ◽  
Enrichment Analysis ◽  
Thorax Length ◽  
Adaptive Trait ◽  
Polygenic Adaptation ◽  
Trait Locus ◽  
Population Genetic Analyses

Important uncertainties persist regarding the genetic architecture of adaptive trait evolution in natural populations, including the number of genetic variants involved, whether they are drawn from standing genetic variation, and whether directional selection drives them to complete fixation. Here, we take advantage of a unique natural population of Drosophila melanogaster from the Ethiopian highlands, which has evolved larger body size than any other known population of this species. We apply a bulk segregant quantitative trait locus (QTL) mapping approach to four unique crosses between highland Ethiopian and lowland Zambian populations for both thorax length and wing length. Results indicated a persistently variable genetic basis for these evolved traits (with largely distinct sets of QTLs for each cross), and at least a moderately polygenic architecture with relatively strong effects present. We complemented these mapping experiments with population genetic analyses of QTL regions and gene ontology enrichment analysis, generating strong hypotheses for specific genes and functional processes that may have contributed to these adaptive trait changes. Finally, we find that the genetic architectures our QTL mapping results for size traits mirror those from similar experiments on other recently-evolved traits in this species. Collectively, these studies suggest a recurring pattern of polygenic adaptation in this species, in which causative variants do not approach fixation and moderately strong effect loci are present.

scholarly journals The rice leaf microbiome has a conserved community structure controlled by complex host-microbe interactions

2019 ◽  
Author(s):  
Veronica Roman-Reyna ◽  
Dale Pinili ◽  
Frances Nikki Borja ◽  
Ian Lorenzo Quibod ◽  
Simon C. Groen ◽  
...  
Keyword(s):  
Stress Responses ◽  
Cropping Systems ◽  
Field Trials ◽  
The Philippines ◽  
Microbiome Composition ◽  
Relative Contribution ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Composition Structure ◽  
Genomic Regions

AbstractUnderstanding the factors that influence the outcome of crop interactions with microbes is key to managing crop diseases and improving yield. While the composition, structure and functional profile of crop microbial communities are shaped by complex interactions between the host, microbes and the environment, the relative contribution of each of these factors is mostly unknown. Here, we profiled the community composition of bacteria across leaves of 3,024 rice (Oryza sativa) accessions from field trials in China and the Philippines using metagenomics. Despite significant differences in diversity between environments, the structure and metabolic profiles of the microbiome appear to be conserved, suggesting that microbiomes converge onto core functions. Furthermore, co-occurrence analysis identified microbial hubs that regulate the network structure of the microbiome. We identified rice genomic regions controlling the abundance of these hubs, enriched for processes involved in stress responses and carbohydrate metabolism. We functionally validated the importance of these processes, finding that abundance of hub taxa was different in rice mutants with altered cellulose and salicylate accumulation, two major metabolites at the host-microbe interactions interface. By identifying key host genomic regions, host traits and hub microbes that govern microbiome composition, our study opens the door to designing future cropping systems.

scholarly journals The Evolution of Larger Size in High Altitude Drosophila melanogaster has a Variable Genetic Architecture

2022 ◽  
Author(s):  
Quentin D Sprengelmeyer ◽  
Justin B Lack ◽  
Dylan T Braun ◽  
Matthew J Monette ◽  
John E Pool
Keyword(s):  
Drosophila Melanogaster ◽  
Qtl Mapping ◽  
Genetic Architecture ◽  
Natural Populations ◽  
Enrichment Analysis ◽  
Thorax Length ◽  
Adaptive Trait ◽  
Polygenic Adaptation ◽  
Trait Locus ◽  
Population Genetic Analyses

Abstract Important uncertainties persist regarding the genetic architecture of adaptive trait evolution in natural populations, including the number of genetic variants involved, whether they are drawn from standing genetic variation, and whether directional selection drives them to complete fixation. Here, we take advantage of a unique natural population of Drosophila melanogaster from the Ethiopian highlands, which has evolved larger body size than any other known population of this species. We apply a bulk segregant quantitative trait locus (QTL) mapping approach to four unique crosses between highland Ethiopian and lowland Zambian populations for both thorax length and wing length. Results indicated a persistently variable genetic basis for these evolved traits (with largely distinct sets of QTLs for each cross), and at least a moderately polygenic architecture with relatively strong effects present. We complemented these mapping experiments with population genetic analyses of QTL regions and gene ontology enrichment analysis, generating strong hypotheses for specific genes and functional processes that may have contributed to these adaptive trait changes. Finally, we find that the genetic architectures our QTL mapping results for size traits mirror those from similar experiments on other recently-evolved traits in this species. Collectively, these studies suggest a recurring pattern of polygenic adaptation in this species, in which causative variants do not approach fixation and moderately strong effect loci are present.

scholarly journals Meta-analysis of diets used in Drosophila microbiome research and introduction of the Drosophila Dietary Composition Calculator (DDCC)

2020 ◽  
Author(s):  
Danielle N.A. Lesperance ◽  
Nichole A. Broderick
Keyword(s):  
Meta Analysis ◽  
Standard Diet ◽  
Dietary Composition ◽  
Community Resources ◽  
Nutritional Content ◽  
Web Based ◽  
Microbiome Composition ◽  
Microbiome Research ◽  
Microbe Interactions ◽  
Host Microbe Interactions

AbstractWhile the term standard diet is commonly used in studies using Drosophila melanogaster, more often than not these diets are anything but standard, making it difficult to contextualize results in the broader scope of the field. This is especially evident in microbiome studies, despite diet having a pivotal role in microbiome composition and resulting host-microbe interactions. Here, we performed a meta-analysis of diets used in fly microbiome research and provide a web-based tool for researchers to determine the nutritional content of diets of interest. Our goal is for these community resources to aid in contextualizing both past and future microbiome studies (with utility to other fields as well) to better understand how individual lab diets can contribute to observed phenotypes.

scholarly journals Host-associated fungal communities are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome

2020 ◽  
Author(s):  
Xavier A. Harrison ◽  
Allan D. McDevitt ◽  
Jenny C. Dunn ◽  
Sarah Griffiths ◽  
Chiara Benvenuto ◽  
...  
Keyword(s):  
Bacterial Communities ◽  
Natural Populations ◽  
Fungal Communities ◽  
Phylogenetic Distance ◽  
Bacterial Microbiome ◽  
Host Phylogeny ◽  
Microbe Interactions ◽  
Host Microbe Interactions ◽  
Microbial Groups ◽  
Taxonomic Groups

ABSTRACTInteractions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Despite a recent proliferation of research on interactions between animals and their associated bacterial communities, comparative evidence from fungal communities is lacking, especially in natural populations. This disparity means knowledge of host-microbe interactions is biased towards the bacterial microbiome. Using samples from 49 species from eight metazoan classes, we demonstrate that the ecological distance between both fungal and bacterial components of the microbiome shift in tandem with host phylogenetic distance. Though so-called phylosymbiosis has been shown in bacterial communities, we extend previous knowledge by demonstrating that the magnitude of shifts in fungal and bacterial community structure across host phylogeny are correlated. These data are indicative of coordinated recruitment by hosts for specific suites of microbes, and potentially selection for bacterial-fungal interactions across a broad taxonomic range of host species. Using co-occurrence networks comprising both microbial groups, we illustrate that fungi form a critical component of microbial interaction networks, and that the strength and frequency of such interactions vary across host taxonomic groups. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host-microbe interactions.

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