Ambrosia beetle Premnobius cavipennis (Scolytinae: Ipini) carries highly divergent ascomycotan ambrosia fungus, Afroraffaelea ambrosiae gen. nov. et sp. nov. (Ophiostomatales)

Bateman, Craig; Huang, Yin-Tse; Simmons, D. Rabern; Kasson, Matthew T.; Stanley, Edward L.; Hulcr, Jiří

doi:10.1016/j.funeco.2016.10.008

Cited by 30 publications

(22 citation statements)

References 45 publications

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“…With the inclusion of ~2,200 more gene regions, the analysis presented here fulfils these requirements and validates their viewpoint. Heeding this advice, we elected to exclude Afroraffaelea ambrosiae from our primary conclusions on domestication as there was no support for its correct position within the Ophiostamatales (similar to when the species was first described (Bateman et al., )). It is possible that the rapid radiation at the base of the Ophiostomatales resulted in a mis‐rooting in our supermatrix analysis, one that would unite the RA and RL clades with increased taxon sampling and a different data set.…”

Section: Discussionmentioning

confidence: 99%

“…Past efforts to definitively reconstruct evolutionary relationships among Ophiostomatales genera have been inconclusive. The inferred phylogenies were often poorly supported, or the relationships among taxa were unstable across studies, with results varying depending on the taxa or loci sampled, and on the phylogenetic methods employed (Bateman et al., ; Dreaden et al., ; Massoumi Alamouti, Tsui, & Breuil, ; Musvuugwa et al., ; Taerum et al., ). Phylogenetic uncertainty makes it difficult to address long‐standing questions regarding the timing and number of domestication events for ambrosial cultivars in the Ophiostomatales (Dreaden et al., ).…”

Section: Introductionmentioning

confidence: 99%

“…Past efforts to definitively reconstruct evolutionary relationships among Ophiostomatales genera have been inconclusive. The inferred phylogenies were often poorly supported, or the relationships among taxa were unstable across studies, with results varying depending on the taxa or loci sampled, and on the phylogenetic methods employed (Bateman et al, 2017;Dreaden et al, 2014;Massoumi Alamouti, Tsui, & Breuil, 2009;Musvuugwa et al, 2015;Taerum et al, 2013).…”

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Know your farmer: Ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars

2017

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Bark and ambrosia beetles are highly specialized weevils (Curculionidae) that have established diverse symbioses with fungi, most often from the order Ophiostomatales (Ascomycota, Sordariomycetes). The two types of beetles are distinguished by their feeding habits and intimacy of interactions with their symbiotic fungi. The tree tissue diet of bark beetles is facilitated by fungi, while ambrosia beetles feed solely on fungi that they farm. The farming life history strategy requires domestication of a fungus, which the beetles consume as their sole food source. Ambrosia beetles in the subfamily Platypodinae originated in the mid-Cretaceous (119-88 Ma) and are the oldest known group of farming insects. However, attempts to resolve phylogenetic relationships and the timing of domestication events for fungal cultivars have been largely inconclusive. We sequenced the genomes of 12 ambrosia beetle fungal cultivars and bark beetle associates, including the devastating laurel wilt pathogen, Raffaelea lauricola, to estimate a robust phylogeny of the Ophiostomatales. We find evidence for contemporaneous diversification of the beetles and their associated fungi, followed by three independent domestication events of the ambrosia fungi genus Raffaelea. We estimate the first domestication of an Ophiostomatales fungus occurred ~86 Ma, 25 million years earlier than prior estimates and in close agreement with the estimated age of farming in the Platypodinae (96 Ma). Comparisons of the timing of fungal domestication events with the timing of beetle radiations support the hypothesis that the first large beetle radiations may have spread domesticated "ambrosia" fungi to other fungi-associated beetle groups, perhaps facilitating the evolution of new farming lineages.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…Past efforts to definitively reconstruct evolutionary relationships among Ophiostomatales genera have been inconclusive. The inferred phylogenies were often poorly supported, or the relationships among taxa were unstable across studies, with results varying depending on the taxa or loci sampled, and on the phylogenetic methods employed (Bateman et al, 2017;Dreaden et al, 2014;Massoumi Alamouti, Tsui, & Breuil, 2009;Musvuugwa et al, 2015;Taerum et al, 2013).…”

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Know your farmer: Ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars

2017

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“…Other clades of ambrosia beetles and fungus-feeding bark beetles (Curculionidae: Scolytinae) have evolved different types of mycangia (Schedl, 1962;Francke-Grosmann, 1967;Bateman et al, 2017;Hulcr & Stelinski, 2017). In some cases, the mycangia are rigid chitinous structures and not flexible, in which case developmental plasticity is unlikely (such as Dendroctonus spp.…”

Section: Discussionmentioning

confidence: 99%

Plasticity of mycangia in Xylosandrus ambrosia beetles

Ruan

Stanley

et al. 2018

Insect Science

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Insects that depend on microbial mutualists evolved a variety of organs to transport the microsymbionts while dispersing. The ontogeny and variability of such organs is rarely studied, and the microsymbiont's effects on the animal tissue development remain unknown in most cases. Ambrosia beetles (Coleoptera: Curculionidae: Scolytinae or Platypodinae) and their mutualistic fungi are an ideal system to study the animal-fungus interactions. While the interspecific diversity of their fungus transport organ-mycangia-is well-known, their developmental plasticity has been poorly described. To determine the ontogeny of the mycangium and the influence of the symbiotic fungus on the tissue development, we dissected by hand or scanned with micro-CT the mycangia in various developmental stages in five Xylosandrus ambrosia beetle species that possess a large, mesonotal mycangium: Xylosandrus amputatus, Xylosandrus compactus, Xylosandrus crassiusculus, Xylosandrus discolor, and Xylosandrus germanus. We processed 181 beetle samples from the United States and China. All five species displayed three stages of the mycangium development: (1) young teneral adults had an empty, deflated and cryptic mycangium without fungal mass; (2) in fully mature adults during dispersal, the pro-mesonotal membrane was inflated, and most individuals developed a mycangium mostly filled with the symbiont, though size and symmetry varied; and (3) after successful establishment of their new galleries, most females discharged the bulk of the fungal inoculum and deflated the mycangium. Experimental aposymbiotic individuals demonstrated that the pronotal membrane invaginated independently of the presence of the fungus, but the fungus was required for inflation. Mycangia are more dynamic than previously thought, and their morphological changes correspond to the phases of the symbiosis. Importantly, studies of the fungal symbionts or plant pathogen transmission in ambrosia beetles need to consider which developmental stage to sample. We provide illustrations of the different stages, including microphotography of dissections and micro-CT scans.

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“…Indeed, Bateman et al (2016) described a new genus in Ophiostomatales from Premnobius cavipennis ( Scolytinae ; Ipini ), an independently evolved ambrosia beetle lineage largely confined to Africa. Furthermore, ambrosia beetles’ mycosymbionts are not limited to the ascomycetous Ophiostomatales .…”

Section: Discussionmentioning

confidence: 99%

New Raffaelea species (Ophiostomatales) from the USA and Taiwan associated with ambrosia beetles and plant hosts

et al. 2016

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Raffaelea (Ophiostomatales) is a genus of more than 20 ophiostomatoid fungi commonly occurring in symbioses with wood-boring ambrosia beetles. We examined ambrosia beetles and plant hosts in the USA and Taiwan for the presence of these mycosymbionts and found 22 isolates representing known and undescribed lineages in Raffaelea. From 28S rDNA and β-tubulin sequences, we generated a molecular phylogeny of Ophiostomatales and observed morphological features of seven cultures representing undescribed lineages in Raffaelea s. lat. From these analyses, we describe five new species in Raffaelea s. lat.: R. aguacate, R. campbellii, R. crossotarsa, R. cyclorhipidia, and R. xyleborina spp. nov. Our analyses also identified two plant-pathogenic species of Raffaelea associated with previously undocumented beetle hosts: (1) R. quercivora, the causative agent of Japanese oak wilt, from Cyclorhipidion ohnoi and Crossotarsus emancipatus in Taiwan, and (2) R. lauricola, the pathogen responsible for laurel wilt, from Ambrosiodmus lecontei in Florida. The results of this study show that Raffaelea and associated ophiostomatoid fungi have been poorly sampled and that future investigations on ambrosia beetle mycosymbionts should reveal a substantially increased diversity.

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Ambrosia beetle Premnobius cavipennis (Scolytinae: Ipini) carries highly divergent ascomycotan ambrosia fungus, Afroraffaelea ambrosiae gen. nov. et sp. nov. (Ophiostomatales)

Abstract: 2016-12-23T18:37:48

Cited by 30 publications

References 45 publications

Know your farmer: Ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars

Know your farmer: Ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars

Plasticity of mycangia in Xylosandrus ambrosia beetles

New Raffaelea species (Ophiostomatales) from the USA and Taiwan associated with ambrosia beetles and plant hosts

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