Host evolutionary history and ecological context modulate the adaptive potential of the microbiome

Henry, Lucas P.; Fernández, Michael; Ayroles, Julien F.

doi:10.1101/2020.09.21.306779

Cited by 3 publications

(3 citation statements)

References 114 publications

(233 reference statements)

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“…Certain combinations of mutualists can also appear maladapted to their environment (Rúa et al, 2016). This could be due to coevolution between mutualists slowing the approach to a stable environmentally matched equilibrium (Thompson et al, 2002); however, our model suggests that this scenario could also be a stable reverse migration-selection balance equilibrium if GXE interactions are relatively weak and dispersal is low (e.g., as in the Drosophila melanagoster microbiome experiment, Henry et al, 2020). Finally, our model suggests that asymmetric rates of dispersal between partners increases the scope for local polymorphism in mutualisms.…”

Section: Implications For Empirical Studiesmentioning

confidence: 84%

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How genotype-by-environment interactions can maintain variation in mutualisms

Carlson,

Frederickson,

Osmond

2024

Preprint

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Coevolution requires reciprocal genotype-by-genotype (GXG) interactions for fitness, which occur when the fitnesses of interacting species depend on the match between their genotypes. However, in mutualisms, when GXG interactions are mutually beneficial, simple models predict that positive feedbacks will erode genetic variation, weakening or eliminating the GXG interactions that fuel ongoing coevolution. This is inconsistent with the ample trait and fitness variation observed within real-world mutualisms. Here, we explore how genotype-by-environment (GXE) interactions, which occur when different genotypes respond differently to different environments, maintain variation in mutualisms. We employ a game theoretic model in which the fitnesses of two partners depend on mutually beneficial GXG and GXE interactions. Variation is maintained via migration-selection balance when GXE interactions are slightly stronger than GXG interactions or when they are much stronger than GXG interactions for just one partner. However, unexpectedly, when GXE interactions are much stronger than GXG interactions for both partners and dispersal is high, genotypically mismatched partners can fix, eroding variation and leading to apparent maladaptation between partners. We parameterize our model using data from three published reciprocal transplant experiments and find that the observed strengths of GXE interactions can maintain or erode variation in mutualisms via these mechanisms.

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Section: Implications For Empirical Studiesmentioning

confidence: 84%

“…Henry et al (2020) conducted a microbiome reciprocal transplant experiment that we use to parameterize our fitness payoffs. They experimentally evolved one population of Drosophila melanogaster together with its microbiome (composed of Acetobacter spp.)…”

mentioning

confidence: 99%

How genotype-by-environment interactions can maintain variation in mutualisms

Carlson,

Frederickson,

Osmond

2024

Preprint

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“…System complexity emerges from the linking and co-localization of biotic and shared abiotic niches in space and time. From the point of view of population genetics, this leads to a genotype × genotype × environment (G×G×E) interaction that can co-evolve (Thompson 2005(Thompson , 2009(Thompson , 2013(Thompson , 2014Morris 2018;Henry et al 2020).…”

Section: On the Evolution Of Symbiosismentioning

confidence: 99%

Symbiosis and the Anthropocene

Hom

Penn

2021

Symbiosis

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Recent human activity has profoundly transformed Earth biomes on a scale and at rates that are unprecedented. Given the central role of symbioses in ecosystem processes, functions, and services throughout the Earth biosphere, the impacts of human-driven change on symbioses are critical to understand. Symbioses are not merely collections of organisms, but co-evolved partners that arise from the synergistic combination and action of different genetic programs. They function with varying degrees of permanence and selection as emergent units with substantial potential for combinatorial and evolutionary innovation in both structure and function. Following an articulation of operational definitions of symbiosis and related concepts and characteristics of the Anthropocene, we outline a basic typology of anthropogenic change (AC) and a conceptual framework for how AC might mechanistically impact symbioses with select case examples to highlight our perspective. We discuss surprising connections between symbiosis and the Anthropocene, suggesting ways in which new symbioses could arise due to AC, how symbioses could be agents of ecosystem change, and how symbioses, broadly defined, of humans and “farmed” organisms may have launched the Anthropocene. We conclude with reflections on the robustness of symbioses to AC and our perspective on the importance of symbioses as ecosystem keystones and the need to tackle anthropogenic challenges as wise and humble stewards embedded within the system.

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Blue light toxicity drives the gut microbiota-mediated lipid accumulation inDrosophila

Takada,

Ichinose,

Fuse

et al. 2024

Preprint

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Blue light (BL), abundant in sunlight, is highly toxic to many insect species when exposure is excessive. While the physiological mechanisms of BL toxicity are being revealed, the evolutionary responses remain less explored. In this study, using Drosophila melanogaster as a model system, we conducted laboratory selection for over 60 generations under excessive BL exposure. The selected line (SL) flies exhibited enhanced BL-tolerance, and also increased body weight and lipid accumulation. Interestingly, we found elongated midgut in the SL flies, and increased microbiota, which was dominated by Acetobacter persici. The BL-tolerance and the lipid accumulation were dependent on the increment of gut microbiota. Genomic analysis identified mutations in the Hippo signaling pathway linked to midgut elongation, while transcriptome analysis showed downregulation of Tachykinin (Tk), a key suppressor of intestinal lipogenesis. Genetically induced lipid accumulation through manipulation of Tk or related lipogenic genes was sufficient to confer BL-tolerance. Moreover, our findings indicate that parental BL irradiation, along with accumulated mutations from laboratory selection, played a crucial role in midgut elongation and increased bacterial abundance. These findings reveal evolutionary responses to excessive BL exposure that shape host traits to maximize the benefits provided by gut microbiota.

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Host evolutionary history and ecological context modulate the adaptive potential of the microbiome

Cited by 3 publications

References 114 publications

How genotype-by-environment interactions can maintain variation in mutualisms

How genotype-by-environment interactions can maintain variation in mutualisms

Symbiosis and the Anthropocene

Blue light toxicity drives the gut microbiota-mediated lipid accumulation inDrosophila

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