Title: Meta-analysis suggests the microbiome responds to Evolve and Resequence experiments in Drosophila melanogaster
AbstractBackground
Experimental evolution has a long history of uncovering fundamental insights into evolutionary processes, but has largely neglected one underappreciated component--the microbiome. As eukaryotic hosts evolve, the microbiome may also respond to selection. However, the microbial contribution to host evolution remains poorly understood. Here, we re-analyzed genomic data to characterize the metagenomes from ten Evolve and Resequence (E&R) experiments inDrosophila melanogasterto determine how the microbiome changed in response to host selection.
Results
Bacterial diversity was significantly different in 5/10 studies, primarily in traits associated with metabolism or immunity. Duration of selection did not significantly influence bacterial diversity, highlighting the importance of associations with specific host traits.
Conclusions
Our genomic re-analysis suggests the microbiome often responds to host selection; thus, the microbiome may contribute to the response ofDrosophilain E&R experiments. We outline important considerations for incorporating the microbiome into E&R experiments. The E&R approach may provide critical insights into host-microbiome interactions and fundamental insight into the genomic basis of adaptation.
Animals form complex symbiotic associations with their gut microbes, whose evolution is determined by an intricate network of host and environmental factors. In many insects, such asDrosophila melanogaster, the microbiome is flexible, environmentally determined, and less diverse than in mammals. In contrast, mammals maintain complex multispecies consortia that are able to colonize and persist in the gastrointestinal tract. Understanding the evolutionary and ecological dynamics of gut microbes in different hosts is challenging. This requires disentangling the ecological factors of selection, determining the timescales over which evolution occurs, and elucidating the architecture of such evolutionary patterns.
Results
We employ experimental evolution to track the pace of the evolution of a common gut commensal,Lactiplantibacillus plantarum, within invertebrate (Drosophila melanogaster) and vertebrate (Mus musculus) hosts and their respective diets. We show that inDrosophila, the nutritional environment dictates microbial evolution, while the host benefitsL. plantarumgrowth only over short ecological timescales. By contrast, in a mammalian animal model,L. plantarumevolution results to be divergent between the host intestine and its diet, both phenotypically (i.e., host-evolved populations show higher adaptation to the host intestinal environment) and genomically. Here, both the emergence of hypermutators and the high persistence of mutated genes within the host’s environment strongly differed from the low variation observed in the host’s nutritional environment alone.
Conclusions
Our results demonstrate thatL. plantarumevolution diverges between insects and mammals. While the symbiosis betweenDrosophilaandL. plantarumis mainly determined by the host diet, in mammals, the host and its intrinsic factors play a critical role in selection and influence both the phenotypic and genomic evolution of its gut microbes, as well as the outcome of their symbiosis.
Stern, David B.; Anderson, Nathan W.; Diaz, Juanita A.; Lee, Carol Eunmi(
, Nature Communications)
Abstract
The role of epistasis in driving adaptation has remained an unresolved problem dating back to the Evolutionary Synthesis. In particular, whether epistatic interactions among genes could promote parallel evolution remains unexplored. To address this problem, we employ an Evolve and Resequence (E&R) experiment, using the copepodEurytemora affinis, to elucidate the evolutionary genomic response to rapid salinity decline. Rapid declines in coastal salinity at high latitudes are a predicted consequence of global climate change. Based on time-resolved pooled whole-genome sequencing, we uncover a remarkably parallel, polygenic response across ten replicate selection lines, with 79.4% of selected alleles shared between lines by the tenth generation of natural selection. Using extensive computer simulations of our experiment conditions, we find that this polygenic parallelism is consistent with positive synergistic epistasis among alleles, far more so than other mechanisms tested. Our study provides experimental and theoretical support for a novel mechanism promoting repeatable polygenic adaptation, a phenomenon that may be common for selection on complex physiological traits.
Gould, Alison L.; Zhang, Vivian; Lamberti, Lisa; Jones, Eric W.; Obadia, Benjamin; Korasidis, Nikolaos; Gavryushkin, Alex; Carlson, Jean M.; Beerenwinkel, Niko; Ludington, William B.(
, Proceedings of the National Academy of Sciences)
Gut bacteria can affect key aspects of host fitness, such as development, fecundity, and lifespan, while the host, in turn, shapes the gut microbiome. However, it is unclear to what extent individual species versus community interactions within the microbiome are linked to host fitness. Here, we combinatorially dissect the natural microbiome ofDrosophila melanogasterand reveal that interactions between bacteria shape host fitness through life history tradeoffs. Empirically, we made germ-free flies colonized with each possible combination of the five core species of fly gut bacteria. We measured the resulting bacterial community abundances and fly fitness traits, including development, reproduction, and lifespan. The fly gut promoted bacterial diversity, which, in turn, accelerated development, reproduction, and aging: Flies that reproduced more died sooner. From these measurements, we calculated the impact of bacterial interactions on fly fitness by adapting the mathematics of genetic epistasis to the microbiome. Development and fecundity converged with higher diversity, suggesting minimal dependence on interactions. However, host lifespan and microbiome abundances were highly dependent on interactions between bacterial species. Higher-order interactions (involving three, four, and five species) occurred in 13–44% of possible cases depending on the trait, with the same interactions affecting multiple traits, a reflection of the life history tradeoff. Overall, we found these interactions were frequently context-dependent and often had the same magnitude as individual species themselves, indicating that the interactions can be as important as the individual species in gut microbiomes.
Ecological theory suggests that dispersal limitation and selection by climatic factors influence bacterial community assembly at a continental scale, yet the conditions governing the relative importance of each process remains unclear. The carnivorous pitcher plantSarracenia purpureaprovides a model aquatic microecosystem to assess bacterial communities across the host plant's north–south range in North America. This study determined the relative influences of dispersal limitation and environmental selection on the assembly of bacterial communities inhabitingS. purpureapitchers at the continental scale.
Location
Eastern United States and Canada.
Time Period
2016.
Major Taxa Studied
Bacteria inhabitingS. purpureapitchers.
Methods
Pitcher morphology, fluid, inquilines and prey were measured, and pitcher fluid underwent DNA sequencing for bacterial community analysis. Null modelling of β‐diversity provided estimates for the contributions of selection and dispersal limitation to community assembly, complemented by an examination of spatial clustering of individuals. Phylogenetic and ecological associations of co‐occurrence network module bacteria was determined by assessing the phylogenetic diversity and habitat preferences of member taxa.
Results
Dispersal limitation was evident from between‐site variation and spatial aggregation of individual bacterial taxa in theS. purpureapitcher system. Selection pressure was weak across the geographic range, yet network module analysis indicated environmental selection within subgroups. A group of aquatic bacteria held traits under selection in warmer, wetter climates, and midge abundance was associated with selection for traits held by a group of saprotrophs. Processes that increased pitcher fluid volume weakened selection in one module, possibly by supporting greater bacterial dispersal.
Conclusion
Dispersal limitation governed bacterial community assembly inS. purpureapitchers at a continental scale (74% of between‐site comparisons) and was significantly greater than selection across the range. Network modules showed evidence for selection, demonstrating that multiple processes acted concurrently in bacterial community assembly at the continental scale.
De_La_Fuente, Caesar A; Lahoud, Nehme; Meyer, Justin R(
, bioRxiv)
Abstract
Bacteriophages, the most abundant and genetically diverse life forms, seemingly defy fundamental ecological theory by exhibiting greater diversity than their numerous bacterial prey. This paradox raises questions about the mechanisms underlying parasite diversity. To investigate this, we took advantage of a surprising experimental result: when bacteriophage λ is continually supplied a single host, λ repeatedly evolves multiple genotypes within the same flask that vary in their receptor use. Measurements of negative frequency-dependent selection between receptor specialists revealed that diversifying selection drove their evolution and maintenance. However, the source of environmental heterogeneity necessary to generate this type of selection was unclear, as only a single isogenic host was provided and replenished every eight hours. Our experiments showed that selection for different specialist phages oscillated over the 8-hour incubation period, mirroring oscillations in gene expression of λ’s two receptors (Escherichia coliouter membrane proteins LamB and OmpF). These receptor expression changes were attributed to both cell-to-cell variation in receptor expression and rapid bacterial evolution, which we documented using phenotypic resistance assays and population genome sequencing. Our findings suggest that cryptic phenotypic variation in hosts, arising from non-genetic phenotypic heterogeneity and rapid evolution, may play a key role in driving viral diversity.
Henry, Lucas P., and Ayroles, Julien F. Meta-analysis suggests the microbiome responds to Evolve and Resequence experiments in Drosophila melanogaster. BMC Microbiology 21.1 Web. doi:10.1186/s12866-021-02168-4.
Henry, Lucas P., & Ayroles, Julien F. Meta-analysis suggests the microbiome responds to Evolve and Resequence experiments in Drosophila melanogaster. BMC Microbiology, 21 (1). https://doi.org/10.1186/s12866-021-02168-4
Henry, Lucas P., and Ayroles, Julien F.
"Meta-analysis suggests the microbiome responds to Evolve and Resequence experiments in Drosophila melanogaster". BMC Microbiology 21 (1). Country unknown/Code not available: Springer Science + Business Media. https://doi.org/10.1186/s12866-021-02168-4.https://par.nsf.gov/biblio/10221077.
@article{osti_10221077,
place = {Country unknown/Code not available},
title = {Meta-analysis suggests the microbiome responds to Evolve and Resequence experiments in Drosophila melanogaster},
url = {https://par.nsf.gov/biblio/10221077},
DOI = {10.1186/s12866-021-02168-4},
abstractNote = {Abstract BackgroundExperimental evolution has a long history of uncovering fundamental insights into evolutionary processes, but has largely neglected one underappreciated component--the microbiome. As eukaryotic hosts evolve, the microbiome may also respond to selection. However, the microbial contribution to host evolution remains poorly understood. Here, we re-analyzed genomic data to characterize the metagenomes from ten Evolve and Resequence (E&R) experiments inDrosophila melanogasterto determine how the microbiome changed in response to host selection. ResultsBacterial diversity was significantly different in 5/10 studies, primarily in traits associated with metabolism or immunity. Duration of selection did not significantly influence bacterial diversity, highlighting the importance of associations with specific host traits. ConclusionsOur genomic re-analysis suggests the microbiome often responds to host selection; thus, the microbiome may contribute to the response ofDrosophilain E&R experiments. We outline important considerations for incorporating the microbiome into E&R experiments. The E&R approach may provide critical insights into host-microbiome interactions and fundamental insight into the genomic basis of adaptation.},
journal = {BMC Microbiology},
volume = {21},
number = {1},
publisher = {Springer Science + Business Media},
author = {Henry, Lucas P. and Ayroles, Julien F.},
}
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