High diversity and low host-specificity of Termitomyces symbionts cultivated by Microtermes spp. indicate frequent symbiont exchange

Peppel, Lennart J.J. van de; Aanen, Duur K.

doi:10.1016/j.funeco.2020.100917

Cited by 15 publications

(26 citation statements)

References 37 publications

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“…All samples contained ASVs that most closely resembled Pseudoxylaria, ranging from 1 to 4 (average = 2.2) different ASVs per foraging site. It is still unknown how Pseudoxylaria spreads from colony to colony, but this raises the possibility that spreading could take place through sharing of foraging tunnels, which is conceivable as larger termite mounds often host multiple farming termite species and even genera ([ 40 , 41 ]; personal observations). Termitomyces was also present in some foraging sites (Additional file 1 : Table S2, Additional file 2 : Figure S2).…”

Section: Discussionmentioning

confidence: 99%

You don’t have the guts: a diverse set of fungi survive passage through Macrotermes bellicosus termite guts

et al. 2020

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Background Monoculture farming poses significant disease challenges, but fungus-farming termites are able to successfully keep their monoculture crop free from contamination by other fungi. It has been hypothesised that obligate gut passage of all plant substrate used to manure the fungal symbiont is key to accomplish this. Here we refute this hypothesis in the fungus-farming termite species Macrotermes bellicosus. Results We first used ITS amplicon sequencing to show that plant substrate foraged on by termite workers harbour diverse fungal communities, which potentially could challenge the farming symbiosis. Subsequently, we cultivated fungi from dissected sections of termite guts to show that fungal diversity does not decrease during gut passage. Therefore, we investigated if healthy combs harboured these undesirable fungal genera, and whether the presence of workers affected fungal diversity within combs. Removal of workers led to a surge in fungal diversity in combs, implying that termite defences must be responsible for the near-complete absence of other fungi in functioning termite gardens. Conclusions The rapid proliferation of some of these fungi when colonies are compromised indicates that some antagonists successfully employ a sit-and-wait strategy that allows them to remain dormant until conditions are favourable. Although this strategy requires potentially many years of waiting, it prevents these fungi from engaging in an evolutionary arms race with the termite host, which employs a series of complementary behavioural and chemical defences that may prove insurmountable.

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Section: Discussionmentioning

confidence: 99%

You don’t have the guts: a diverse set of fungi survive passage through Macrotermes bellicosus termite guts

et al. 2020

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“…Seldom addressed in symbiosis theory are mutualisms that involve both modes of transmission or that commonly involve intra-specific and inter-specific host-switching. For example, Microtermes termites primarily transmit their fungal symbionts vertically yet frequent horizontal exchange occurs between colonies of the same species and even different species ( van de Peppel and Aanen, 2020 ). Likewise, while some ambrosia beetles exhibit strong partner fidelity with, and vertical transmission of, particular ambrosia fungi, some may acquire fungi directly from their environment and possess different symbionts in different locations ( Kostovcik et al, 2015 ; Rassati et al, 2019 ).…”

Section: What Is Context Dependency In Mutualism?mentioning

confidence: 99%

Context Dependency in Bark Beetle-Fungus Mutualisms Revisited: Assessing Potential Shifts in Interaction Outcomes Against Varied Genetic, Ecological, and Evolutionary Backgrounds

Six

Klepzig

2021

Front. Microbiol.

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Context dependency occurs when biological interactions shift in sign or magnitude depending upon genetic, abiotic, and biotic context. Most models of mutualism address systems where interaction outcomes slide along a mutualism-antagonism continuum as environmental conditions vary altering cost-benefit relationships. However, these models do not apply to the many mutualisms that involve by-product benefits and others that do not have antagonistic alternate states. The ubiquity of such mutualisms indicates a need for different approaches and models to understand how environmental variability influences their strength, stability, and ecological roles. In this paper, we apply the concept of context dependency to mutualisms among bark beetles and fungi that span a variety of life strategies and exposures to environmental variability. Bark beetles and their mutualist fungi co-construct a niche based on by-product benefits that allows them to exist in a resource that is otherwise intractable or inaccessible. For the closest of these partnerships, this has resulted in some of the most influential agents of forest mortality in conifer forests worldwide. Understanding these symbioses is key to understanding their influence on forest structure and dynamics and responses to change. We found no evidence that bark beetle mutualisms change in sign as conditions vary, only in magnitude, and that the “closest” (and most environmentally influential) of these partnerships have evolved behaviors and mechanisms to reduce context-dependency and stabilize benefit delivery. The bark beetle-fungus symbioses most likely to slide along a mutualism-antagonism continuum are those involving loosely associated facultative symbionts that may provide benefits under some circumstances and that are horizontally transmitted by the beetle host. Additionally, some symbiotic fungi are never mutualists – these “third party” fungi are exploiters and may shift from commensalism to antagonism depending on environmental context. Our assessment indicates that a careful differentiation between bark beetle-fungus partnerships is crucial to understanding how they influence forests and respond to environmental variability.

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“…In some species, it grows out into a mound that is a large, intricate structure with tunnels and chambers in which the conditions are tightly regulated (Korb 2003). Other species form below-ground colonies that also can reach large sizes, but do not form conspicuous above-ground structures (van de Peppel and Aanen 2020). Each colony houses thousands of termites and can persist for decades (Aanen et al 2002).…”

Section: Life Cycle Of the Termite-fungus Symbiosismentioning

confidence: 99%

“…In the termite-fungus symbiosis, however, transmission mode does not seem to reflect the interaction specificity that is observed between termites and their fungi , Nobre and Aanen 2012, van de Peppel and Aanen 2020. There are species with vertical transmission that have fungal symbionts that are not monophyletic (Aanen et al 2002, Nobre et al 2011a, Nobre et al 2011b, van de Peppel and Aanen 2020, and vice versa there are species with horizontal transmission that are specialised on one fungal symbiont (De Fine Licht et al 2006. The latter especially implies that a mechanism exists that ensures a high interaction specificity despite horizontal symbiont transmission.…”

Section: Known Stabilising Mechanism In the Termite-fungus Symbiosismentioning

confidence: 99%

“…In fungus-growing termites large differences in interaction specificity are observed that do not necessarily correlate with the mode of transmission (Aanen et al 2002, Nobre et al 2011b, Nobre and Aanen 2012, van de Peppel and Aanen 2020. For example, the termite species Macrotermes natalensis, which employs a horizontal mode of transmission is only found to cultivate one lineage of Termitomyces (De Fine Licht et al 2006 , which has been found to represent a single biological species (Nobre et al, 2014).…”

Section: How Is the Right Fungus Selected?mentioning

confidence: 99%

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On conflict and resolution in the termite-fungus symbiosis

Vreeburg¹

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The asexual spore balls formed by Termitomyces are not the primordia of mushrooms (this thesis). 2. There is no such thing as a standard life cycle for basidiomycete fungi (this thesis) 3. If the outcome of a student's project is vital to her or his supervisor, a conflict of interest is inevitable. 4. Society is the customer of science. 5. Selection for soundbites and catchy headlines in science communication is in conflict with the credibility of science as a whole. 6. The core issue for the acceptance of evolutionary theory is the question whether evolutionary theory applies to humans. 7. Differences in payed parental-leave drive the observed patterns of paternal and maternal childcare. 8. Men in top positions are often not hired for their qualities, but rather because they are men.

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High diversity and low host-specificity of Termitomyces symbionts cultivated by Microtermes spp. indicate frequent symbiont exchange

Cited by 15 publications

References 37 publications

You don’t have the guts: a diverse set of fungi survive passage through Macrotermes bellicosus termite guts

You don’t have the guts: a diverse set of fungi survive passage through Macrotermes bellicosus termite guts

Context Dependency in Bark Beetle-Fungus Mutualisms Revisited: Assessing Potential Shifts in Interaction Outcomes Against Varied Genetic, Ecological, and Evolutionary Backgrounds

On conflict and resolution in the termite-fungus symbiosis

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