Natural selection for imprecise vertical transmission in host–microbiota systems

Bruijning, Marjolein; Henry, Lucas P.; Forsberg, Simon K. G.; Metcalf, C. Jessica E.; Ayroles, Julien F.

doi:10.1038/s41559-021-01593-y

Cited by 46 publications

(59 citation statements)

References 96 publications

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“…One plausible ecological explanation for how mycorrhizas facilitate the evolutionary processes of drought adaptation might be related to the imperfect vertical transmission of fidelity, recently modeled for host-microbiome associations (Bruijning et al ., 2022). Although mycorrhizal fungi are not vertically transmitted, as are other microbes in other systems (Bruijning et al ., 2022 and references therein), and plants have to reacquire fungi from soil every generation (Smith & Read, 2008), plant genomes harbor (or have lost) symbiosis-related genes that function as transgenerational transmission mechanisms of plant mycorrhizal strategy (Cope et al ., 2019; Fernández et al ., 2019; Radhakrishnan et al ., 2020; Cosme et al ., 2021; Venice et al ., 2021). Moreover, it seems safe to assume that mycorrhizal fungal guilds are relatively stable entities at an evolutionary time scale based on fossil, chemistry, and genome observations (Remy et al ., 1994; Redecker et al ., 2000; Miyauchi et al ., 2020; Huang et al ., 2022).…”

Section: Discussionmentioning

confidence: 99%

Mycorrhizas shape the evolution of plant adaptation to drought

Cosme

2022

Preprint

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SummaryPlant adaptation to drought facilitates major ecological transitions, and is likely to play a vital role under looming climate change. Mycorrhizas can influence the physiological capacity of plants to tolerate drought. Here, I show how mycorrhizal strategy and drought adaptation shape one another throughout the course of plant evolution.To characterize the evolutions of both plant characters, I applied a phylogenetic comparative method using data of 1,638 extant species globally distributed.The detected correlated evolution unveiled gains and losses of drought tolerance occurring at faster rates in lineages with an ecto- or ericoid mycorrhizal strategy, which were on average about 15 and 300 times quicker than that in lineages with the arbuscular mycorrhizal and naked root (non-mycorrhiza or facultatively arbuscular mycorrhiza) strategy, respectively. Among mycorrhiza shifts, the arbuscular mycorrhiza losses in drought sensitive lineages were more frequent than any symbiont switching or other mutualism breakdown.My study suggests that mycorrhizas play a key facilitator role in the evolutionary process of plant adaptation to critical changes in water availability across global climates.

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Section: Discussionmentioning

confidence: 99%

Mycorrhizas shape the evolution of plant adaptation to drought

Cosme

2022

Preprint

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“…Low fidelity can lead to highly variable associations, which if the host phenotype is responsive, then the microbiome can generate novel phenotypic variation [3]. Theory suggests that this novel phenotypic variation generated from low fidelity associations may also be favored when in variable environments [50]. For D. melanogaster , neutrality in the microbiome may enable flies to rapidly adapt to variable environments.…”

Section: Discussionmentioning

confidence: 99%

Latitudinal cline does not predict variation in the microbiome of wildDrosophila melanogaster

Henry

Ayroles

2022

Preprint

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Microbiomes affect many aspects of host biology, but the eco-evolutionary forces that shape their diversity in natural populations remain poorly understood. Geographic gradients, like latitudinal clines, generate predictable patterns in biodiversity at macroecological scales, but whether these macro-scale processes apply to host-microbiome interactions is an open question. To address this question, we sampled the microbiomes of 13 natural populations of Drosophila melanogaster along a latitudinal cline in eastern United States. The microbiomes were surprisingly consistent across the cline--latitude did not predict either alpha or beta diversity. Only a narrow taxonomic range of bacteria were present in all microbiomes, indicating that strict taxonomic filtering by the host and neutral ecological dynamics are the primary factors shaping the fly microbiome. Additional temporal sampling across two independent sites revealed significant differences in microbial communities over time, suggesting that local environmental differences that vary at fine spatiotemporal scales are more likely to shape the microbiome. Our findings reveal the complexity of eco-evolutionary interactions shaping microbial variation in D. melanogaster and highlight the need for additional sampling of the microbiomes in natural populations along environmental gradients.

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“…As Wolbachia decreases the capacity for change in the microbiome, evolution in the host genome also is likely to change, much like adaptive tracking (9,69). More work is necessary to understand the linkages between host and microbiome evolution, but adaptive tracking may depend on hostmicrobe interactions (9). Adaptive tracking in Drosophila can occur during seasonal evolution (70), and potentially in the many organisms that live in temporally fluctuating environments-if and how the microbiome contributes to adaptive tracking remains an open question.…”

Section: Implications For Microbiome Interactions In Seasonally Evolv...mentioning

confidence: 99%

Wolbachiainteracts with the microbiome to shape fitness-associated traits during seasonal adaptation inDrosophila melanogaster

Henry

Fernández

Wolf

et al. 2022

Preprint

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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.

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Natural selection for imprecise vertical transmission in host–microbiota systems

Cited by 46 publications

References 96 publications

Mycorrhizas shape the evolution of plant adaptation to drought

Mycorrhizas shape the evolution of plant adaptation to drought

Latitudinal cline does not predict variation in the microbiome of wildDrosophila melanogaster

Wolbachiainteracts with the microbiome to shape fitness-associated traits during seasonal adaptation inDrosophila melanogaster

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