A selective fungal transport organ (mycangium) maintains coarse phylogenetic congruence between fungus-farming ambrosia beetles and their symbionts

Skelton, James; Johnson, Andrew J.; Jusino, Michelle A.; Bateman, Craig; Li, You; Hulcr, Jiří

doi:10.1098/rspb.2018.2127

Cited by 56 publications

(79 citation statements)

References 58 publications

(80 reference statements)

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“…Vertical transmission may support cospeciation, in which a symbiont is fixed into a mutualistic relationship after selection based on desirable characteristics (7). However, host switches are also common, especially between closely related mutualists and congener beetles (15), which could result in X. volvulus acting as a secondary vector of R. lauricola.…”

Section: Discussionmentioning

confidence: 99%

“…Most of these symbioses are multipartite, with a beetle associated with two or more permanent partners (7). It is thought that the mycangia play a critical role in conferring symbiont specificity (14,15). Fungal symbiont transfer occurs vertically from the natal galleries to the offspring, and thereafter the symbionts are transmitted by the new generation of females when they colonize other trees (7).…”

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confidence: 99%

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Xyleborus volvulus (Coleoptera: Curculionidae): Biology and Fungal Associates

Cruz

Menocal

Mantilla

et al. 2019

Appl Environ Microbiol

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The ambrosia beetle Xyleborus volvulus Fabricius has been reported as a potential vector of the plant pathogen Raffaelea lauricola T.C. Harr., Fraedrich & Aghayeva that is affecting avocado orchards in South Florida. In this study, we examined its life cycle, process of gallery formation, gallery structure, and fungal associates by rearing one generation on avocado sawdust medium under control conditions. The adult foundress excavated a vertical tunnel that constituted the main gallery with a length of 2.5 cm, followed by the construction of up to six secondary galleries with a total length of 4.4 cm. The time period for one generation (egg to adult) was 28 days. Teneral males emerged 3 days after the emergence of the first females. The F1 generation did not significantly contribute to gallery expansion. Four species of Raffaelea and nine yeast species were recovered from galleries and beetles. Raffaelea arxii and Candida berthetii were the most frequent symbionts recovered from new adults and galleries. Candida berthetii dominated during the early stages of the gallery development, whereas R. arxii was most frequent in later stages. Other Raffaelea species were inconsistently isolated from galleries, which suggests a strong association between Xyleborus volvulus and both R. arxii and C. berthetii. These results suggest that R. arxii is the primary nutritional symbiont of X. volvulus and that yeast species may be pioneer colonizers that assist with the growth of fungal symbionts. IMPORTANCE Ambrosia beetles cultivate fungi in tunnels bored into weakened host trees. This obligate interaction is required for their survival as beetles feed on these symbiotic fungi, and the fungi benefit from transportation by the beetles. Xyleborus volvulus carries many nonpathogenic symbionts; however, recently the acquisition of Raffaelea lauricola (the causal agent of a lethal vascular disease of lauraceous trees) by this beetle has altered its status from wood degrader to potential pest in avocado. We conducted a study to understand the relationship of this beetle and its fungal associates. Our results show that X. volvulus has a multipartite flexible association with different Raffaelea species. The lack of fidelity in the mutualistic association may explain the acquisition of R. lauricola. Knowing the beetle biology and its mutualistic interactions furthers an understanding of the beetle’s role as a potential vector and in disease transmission.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Xyleborus volvulus (Coleoptera: Curculionidae): Biology and Fungal Associates

Cruz

Menocal

Mantilla

et al. 2019

Appl Environ Microbiol

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“…They are attracted en masse to tree‐stress‐related chemicals such as ethanol and terpenes, as well as aggregation pheromones released by other beetles and volatile organic compounds released by their symbiotic fungi (Hulcr, Mann, & Stelinski, ; Kandasamy, Gershenzon, Andersson, & Hammerbacher, ; Wood, ). The beetles have relationships with fungi that range from incidental commensalism to co‐evolved, reciprocally obligate nutritional mutualisms (Skelton, Johnson, et al, ). Bark and ambrosia beetles differ by their feeding ecology.…”

Section: Introductionmentioning

confidence: 99%

Relationships among wood‐boring beetles, fungi, and the decomposition of forest biomass

et al. 2019

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A prevailing paradigm in forest ecology is that wood‐boring beetles facilitate wood decay and carbon cycling, but empirical tests have yielded mixed results. We experimentally determined the effects of wood borers on fungal community assembly and wood decay within pine trunks in the southeastern United States. Pine trunks were made either beetle‐accessible or inaccessible. Fungal communities were compared using culturing and high‐throughput amplicon sequencing (HTAS) of DNA and RNA. Prior to beetle infestation, living pines had diverse fungal endophyte communities. Endophytes were displaced by beetle‐associated fungi in beetle‐accessible trees, whereas some endophytes persisted as saprotrophs in beetle‐excluded trees. Beetles increased fungal diversity several fold. Over forty taxa of Ascomycota were significantly associated with beetles, but beetles were not consistently associated with any known wood‐decaying fungi. Instead, increasing ambrosia beetle infestations caused reduced decay, consistent with previous in vitro experiments that showed beetle‐associated fungi reduce decay rates by competing with decay fungi. No effect of bark‐inhabiting beetles on decay was detected. Platypodines carried significantly more fungal taxa than scolytines. Molecular results were validated by synthetic and biological mock communities and were consistent across methodologies. RNA sequencing confirmed that beetle‐associated fungi were biologically active in the wood. Metabarcode sequencing of the LSU/28S marker recovered important fungal symbionts that were missed by ITS2, though community‐level effects were similar between markers. In contrast to the current paradigm, our results indicate ambrosia beetles introduce diverse fungal communities that do not extensively decay wood, but instead reduce decay rates by competing with wood decay fungi.

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“…Along with the depletion of the original mycobiome, we speculate that an exotic species may be prone to acquire new microorganisms due to the potential mismatch of the mechanisms maintaining symbioses with the invaded ecosystems. Symbioses are the result of a long co-evolution, and both the host and the symbionts present a series of chemical, structural, and genomic coadaptations (Blaz et al, 2018;Mayers et al, 2019;Skelton et al, 2019;Biedermann, De Fine Licht & Rohlfs, 2019;Veselská et al, 2019). The mechanisms that serve to maintain existing symbiosis may be challenged by the newly encountered microbiomes and might not work properly, leading to the establishment of new associations.…”

Section: Discussionmentioning

confidence: 99%

“…Manuscript to be reviewed investigate in future studies as a switch in the fungal symbionts in the mycentangium may lead to important consequences for the beetle fitness (Skelton et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Peer Review #2 of "Acquisition of fungi from the environment modifies ambrosia beetle mycobiome during invasion (v0.1)"

2019

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Microbial symbionts can play critical roles when their host attempts to colonize a new habitat. The lack of symbiont adaptation can in fact hinder the invasion process of their host. This scenario could change if the exotic species are able to acquire microorganisms from the invaded environment. Understanding the ecological factors that influence the take-up of new microorganisms is thus essential to clarify the mechanisms behind biological invasions. In this study, we tested whether different habitats influence the structure of the fungal communities associated with ambrosia beetles. To do so, we collected individuals of the most widespread exotic (Xylosandrus germanus) and native (Xyleborinus saxesenii) ambrosia beetles species in Europe in several old-growth and restored forests. We characterized the fungal communities associated with both species via metabarcoding. We showed that forest habitat shaped the community of fungi associated with both beetles, but the effect was stronger for the exotic X. germanus. Our results support the hypothesis that the direct contact with the mycobiome of the invaded environment can lead an exotic species to acquire native fungi. This mechanisms is likely favored by the occurrence of a bottleneck effect at the mycobiome level and/or the disruption of the mechanisms sustaining co-evolved insect-fungi symbiosis. Our study contributes to the understanding of the factors affecting insect-microbes interactions, helping to clarify the mechanisms behind biological invasions.

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A selective fungal transport organ (mycangium) maintains coarse phylogenetic congruence between fungus-farming ambrosia beetles and their symbionts

Cited by 56 publications

References 58 publications

Xyleborus volvulus (Coleoptera: Curculionidae): Biology and Fungal Associates

Xyleborus volvulus (Coleoptera: Curculionidae): Biology and Fungal Associates

Relationships among wood‐boring beetles, fungi, and the decomposition of forest biomass

Peer Review #2 of "Acquisition of fungi from the environment modifies ambrosia beetle mycobiome during invasion (v0.1)"

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