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Biology subjects

Henry, L. P.

Publications and source records attributed to Henry, L. P..

6 recordsLinked to original sources

Seasonality, land use, and diversity shape microbiome-pathogen interactions in wild populations of Arabidopsis thaliana

The microbiome often protects plants against pathogens, but most findings are limited to controlled experiments in the lab. In the context of wild populations, one key challenge is to understand sources of variation that impact the commensal microbiome, which in turn shapes the degree of protection. Here, we surveyed both disease symptoms and microbiomes from wild populations of Arabidopsis thaliana over four consecutive seasons (fall/spring) across three different land use types. Land use types varied in the extent of anthropogenic influences and included forest meadows, human-impacted fields adjacent to agriculture or municipal parks, and highly disturbed habitats near railroad tracks. By building an integrative map of abiotic and biotic variables, we find that a key predictor of disease was biodiversity across ecological scales. Plant communities with higher diversity were associated with reduced disease burden in A. thaliana populations but also increased diversity within the microbiome of A. thaliana. This increased microbial diversity was additionally associated with less disease in A. thaliana. However, the diversity-microbiome-disease relationships were all sensitive to season and further modulated by land use. Taken together, our work highlights the importance of anthropogenic change reshaping species interactions across ecological scales to impact disease risk in wild plant populations.

ecology↗

Wolbachia interacts with the microbiome to shape fitness-associated traits during seasonal adaptation in Drosophila melanogaster

The microbiome contributes to many different host traits, but its role in host adaptation remains enigmatic. The fitness benefits of the microbiome often depend on ecological conditions, but fluctuations in both the microbiome and environment modulate these fitness benefits. Moreover, vertically transmitted bacteria might constrain the ability of both the microbiome and host to respond to changing environments. Drosophila melanogaster provides an excellent system to investigate the evolutionary effects of interactions between the microbiome and the environment. To address this question, we created field mesocosms of D. melanogaster undergoing seasonal adaptation with and without the vertically transmitted bacteria, Wolbachia pipientis. Sampling temporal patterns in the microbiome revealed that Wolbachia constrained microbial diversity. Furthermore, interactions between Wolbachia and the microbiome contributed to fitness-associated traits. Wolbachia often exerted negative fitness effects on hosts, and the microbiome modulated these effects. Our work supports recent theoretical advances suggesting that hosts in temporally fluctuating environments benefit from flexible microbial associations with low transmission fidelity--specifically when changes in the microbiome can better enable host phenotypes to match environment change. We conclude by exploring the consequences of complex interactions between Wolbachia and the microbiome for our understanding of eco-evolutionary processes and the utility of Wolbachia in combating vector-borne disease.

evolutionary biology↗

Relative abundance data can misrepresent heritability of the microbiome

Host genetics can shape microbiome composition, but to what extent it does, remains unclear. Like any other complex trait, this question can be addressed by estimating the heritability (h2) of the microbiome - the proportion of variance in the abundance of each taxon that is attributable to host genetic variation. However, unlike most complex traits, microbiome heritability is typically based on relative abundance data, where taxon-specific abundances are expressed as the proportion of the total microbial abundance in a sample. We derived an analytical approximation for the heritability that one obtains when using such relative abundances and we uncovered three problems: 1) The interdependency between taxa leads to imprecise heritability estimates. 2) Large sample size leads to high false discovery rates, overestimating the number of heritable taxa. 3) Microbial co-abundances lead to biased heritability estimates. We conclude that caution must be taken when interpreting heritability estimates and comparing values across studies.

evolutionary biology↗

When the microbiome defines the host phenotype: selection on vertical transmission in varying environments

The microbiome can contribute to variation in fitness-related traits of their hosts, and thus to host evolution. Hosts are therefore expected to be under selection to control their microbiome, for instance through controlling microbe transmission from parents to offspring. Current models have mostly focused on microbes that either increase or decrease fitness. In that case, host-level selection is relatively straightforward, favouring either complete or no inheritance. In natural systems, however, vertical transmission fidelity varies widely, and microbiome composition is often shaped by a combination of vertical and horizontal transmission modes. We propose that such mixed transmission could optimize host fitness under fluctuating environments. Using a general model, we illustrate that decreasing vertical transmission fidelity increases the amount of microbiome variation, and thus potentially phenotypic variation, across hosts. Whether or not this is advantageous depends on environmental conditions, how much the microbiome changes during host development, and the contribution of other factors to trait variation. We discuss how environmentally-dependent microbial effects can favor intermediate transmission, review examples from natural systems, and suggest research avenues to empirically test our predictions. Overall, we show that imperfect transmission may be adaptive by allowing individuals to ensure phenotypic variability in their offspring in contexts where varying environments mean that this strategy increases long-term fitness.

evolutionary biology↗

The microbiome responds to Evolve and Resequence experiments in Drosophila melanogaster

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 evolve. 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) experiment in Drosophila melanogaster to 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. Additionally, we find that excluding reads from a facultative symbiont, Wolbachia, in the analysis of bacterial diversity changes the inference, raising important questions for future E&R experiments in the D. melanogaster microbiome. ConclusionsOur genomic re-analysis suggests the microbiome often responds to host selection; thus, the microbiome may contribute to the response of Drosophila in 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.

evolutionary biology↗

Why evolve reliance on the microbiome for timing of ontogeny?

The timing of life history events has important fitness consequences. Since the 1950s, researchers have combined first principles and data to predict the optimal timing of life history transitions. Recently, a striking mystery has emerged. Such transitions can be shaped by a completely different branch of the tree of life: bacterial species in the microbiome. Probing these interactions using testable predictions from evolutionary theory could illuminate whether and how host-microbiome integrated life histories can evolve and be maintained. Beyond advancing fundamental science, this research program could yield important applications. In an age of microbiome engineering, understanding the contexts that lead to microbiota signaling shaping ontogeny could offer novel mechanisms for manipulations to increase yield in agriculture, or reduce pathogen transmission by affecting vector efficiency. We combine theory and evidence to illuminate the essential questions underlying the existence of Microbiome Dependent Ontogenetic Timing (MiDOT) to fuel research on this emerging topic.

evolutionary biology↗