An agent-based model of adaptation of holobionts with different microbial symbiont transmission modes

ABSTRACTThe hologenome theory suggests that holobionts (host plus symbiont) with hosts that are only able to adapt slowly may be able to persist in deteriorating environmental conditions via rapid adaptation of their microbial symbionts. The effectiveness of such symbiont adaptation may vary depending on whether symbionts are passed directly to offspring (vertical transmission) or acquired from the environment (horizontal transmission). However, it has been suggested that holobionts with horizontal transmission cannot pass down their symbionts faithfully, preventing adaptation at the holobiont level because of host-symbiont disassociation between generations. Here we used an agent-based model to investigate whether holobionts with horizontal microbial symbiont transmission can adapt to increasing stress solely through symbiont adaptation and compared their adaptation to holobionts with vertical transmission. We found that holobionts with either transmission mode were able to adapt to increasing abiotic stress solely via symbiont adaptation. Moreover, those with horizontal transmission were more competitive than those with vertical transmission when hosts were able to selectively associate with the most suitable symbionts. However, those with horizontal transmission were less competitive than those with vertical transmission when symbiont establishment was random. Our results support the hologenome theory and demonstrate that holobionts with horizontal microbial symbiont transmission could adapt to increasing abiotic stress via their symbionts. We also showed that whether holobionts with horizontal or vertical symbiont transmission are favored in increasingly stressful conditions depends on the ability of hosts to recognize and foster microbial symbionts that confer stress tolerance.IMPORTANCESymbiotic organisms such as reef building corals are sensitive to environmental perturbations due to anthropogenic disturbances or climate change, and it is critical to understand whether they are able to adapt to previously unfavorable conditions. To date, studies have focused on the impacts of existing microbial symbiont variation on holobiont stress tolerance but here we use agent-based models to explore holobiont adaptation via symbiont adaptation. We studied both deterministic and stochastic processes in holobiont adaptation by investigating the following four factors: holobiont transmission modes, a host’s ability to recognize tolerance-conferring symbionts, a symbiont’s mutational variance, and rate of stress increase. Our simulation provides a comprehensive understanding of holobiont adaptation under stress, which not only has implications for future endangered symbiotic species management, but also provides fresh insight into species evolution as proposed by the hologenome theory.

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Transmission mode is associated with environment type and taxa across bacteria-eukaryote symbioses

10.1101/412882 ◽

2018 ◽

Cited By ~ 2

Author(s):

Shelbi L Russell

Keyword(s):

Vertical Transmission ◽

Horizontal Transmission ◽

Transmission Mode ◽

Symbiotic Associations ◽

Transmission Modes ◽

Symbiont Transmission ◽

Environment Type ◽

Full Separation ◽

Host Evolution ◽

Host Tissues

AbstractSymbiotic associations between bacteria and eukaryotes exhibit a range of transmission strategies. Anecdotal observations suggest that symbionts of terrestrial hosts tend to be strictly vertically inherited through host tissues, whereas symbionts of marine hosts tend towards horizontal transmission. Aside from a few cursory investigations, the rates and distributions of transmission modes have not been investigated in depth across associations, despite the consequences for symbiont and host evolution. To address this empirically and estimate the rate of each mode, I compiled data from the literature and for associations between transmission mode and the environment, transmission route, symbiont function, and taxa involved in the symbiosis. Of the 441 analyzed symbioses, 50.1% were strictly vertically transmitted, 34.0% exhibited some form of mixed mode transmission, and 15.9% were strictly horizontally transmitted. Binning symbioses by their environment revealed a significant skew towards vertical transmission on land and horizontal transmission in aquatic environments, with mixed modes abundant in both. However, host and symbiont taxa were not randomly distributed, which prevented the full separation of these variables. Overall, the data suggest that many symbiotic taxa are capable of horizontal transmission and barriers exist that reduce the rate of these events. Thus, both the environment type and host/symbiont taxa combined influence symbiont transmission mode evolution.One sentence summaryThrough an intensive analysis of the literature on symbiosis transmission modes, estimated rates for each transmission mode were calculated, revealing bias for horizontal transmission in the ocean and vertical transmission on land.

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Simulated folivory increases vertical transmission of fungal endophytes that deter herbivores and alter tolerance to herbivory in Poa autumnalis

Annals of Botany ◽

10.1093/aob/mcaa021 ◽

2020 ◽

Vol 125 (6) ◽

pp. 981-991 ◽

Cited By ~ 2

Author(s):

Pedro E Gundel ◽

Prudence Sun ◽

Nikki D Charlton ◽

Carolyn A Young ◽

Tom E X Miller ◽

...

Keyword(s):

Vertical Transmission ◽

Transmission Rate ◽

Horizontal Transmission ◽

Fungal Endophytes ◽

Natural Populations ◽

Plant Tolerance ◽

Hyphal Density ◽

Symbiotic Fungi ◽

Symbiont Transmission ◽

Fitness Benefits

Abstract Background and Aims The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission? Methods We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission. Key Results Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission. Conclusions Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.

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Can Differences in Symbiont Transmission Mode Explain the Abundance and Distribution of Fungus-Growing Termites in West Africa?

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2020.600318 ◽

2020 ◽

Vol 8 ◽

Author(s):

Judith Korb ◽

Simon Kolotchèlèma Silué ◽

N'golo Abdoulaye Koné

Keyword(s):

Vertical Transmission ◽

National Parks ◽

Horizontal Transmission ◽

Species Abundance ◽

Transmission Mode ◽

Termite Species ◽

Symbiont Transmission ◽

Ecological Dominance ◽

Study Sites ◽

Abundance And Distribution

Fungus-growing termites (Isoptera: Macrotermitinae) dominate African savannah ecosystems where they play important roles in ecosystem functioning. Their ecological dominance in these ecosystems has been attributed to living in an ectosymbiosis with fungi of the genus Termitomyces (Lyophyllaceae). Evolutionary theory predicts that the transmission mode of a symbiont determines cooperation and conflict between host and symbiont with vertical transmission (co-transmission of host and symbiont offspring to the next generation) leading to less conflict than horizontal transmission (symbionts are acquired by the host from the environment). Thus, one can hypothesize associations with vertical transmission to be ecological more successful than those with horizontal transmission. We tested this by analyzing whether there is an association between transmission mode and fungus-growing termite species abundance and distribution in West-African savannah and forest ecosystems. We used data from a total of 78 study sites comprising protected National Parks as well as anthropogenically disturbed ecosystems, covering Benin, Côte d'Ivoire, and Togo. Our results showed that, in contrast to expectation, species with horizontal symbiont transmission were more common. We encountered more often species with horizontal than vertical transmission. This result might be due to the fact that only five out of the 25 identified fungus-growing termite species had vertical transmission. Yet, species with horizontal transmission also had higher relative abundances within study sites than those with vertical transmission. Thus, transmission mode is unlikely to explain abundance differences between fungus-growing termite species.

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Evolution of symbiont transmission in conditional mutualisms in spatially and temporally variable environments

10.1101/2020.05.05.079103 ◽

2020 ◽

Author(s):

Alexandra Brown ◽

Erol Akçay

Keyword(s):

Vertical Transmission ◽

Horizontal Transmission ◽

Environmental Variation ◽

Transmission Mode ◽

Trade Off ◽

Symbiotic Relationships ◽

Physiological Constraints ◽

Fitness Effects ◽

Variable Environments ◽

Symbiont Transmission

AbstractSymbiotic relationships affect the fitness and organismal function of virtually all organisms. In many cases, the fitness effects of symbiosis may be beneficial or harmful depending on the environment. The hosts of such symbionts are favored to acquire them only when the symbiont is beneficial. However, it is not clear whether such selection favors vertical or horizontal transmission, both, or neither. To address this question, we model the evolution of transmission mode in a conditional mutualism experiencing spatial and temporal environmental variation. We find that when symbionts affect host lifespan, but not fecundity, horizontal transmission can contain them to beneficial environments. Vertical transmission can produce symbiont containment when the environmental state is synchronized across locations. We also find an emergent trade-off between horizontal and vertical transmission, suggesting that physiological constraints are not required for the evolution of limits on the total amount of transmission.

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

10.1101/2020.09.02.280040 ◽

2020 ◽

Author(s):

Marjolein Bruijning ◽

Lucas P. Henry ◽

Simon K.G. Forsberg ◽

C. Jessica E. Metcalf ◽

Julien F. Ayroles

Keyword(s):

Vertical Transmission ◽

Phenotypic Variability ◽

Horizontal Transmission ◽

Microbiome Composition ◽

Natural Systems ◽

Transmission Modes ◽

Varying Environments ◽

Phenotype Selection ◽

Host Evolution

AbstractThe 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.

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