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Three Genera in the Ceratocystidaceae Are the Respective Symbionts of Three Independent Lineages of Ambrosia Beetles with Large, Complex Mycangia

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Three Genera in the Ceratocystidaceae Are the Respective Symbionts of Three Independent Lineages of Ambrosia Beetles with Large, Complex Mycangia fungal biology 119 (2015) 1075e1092 journal homepage: www.elsevier.com/locate/funbio Three genera in the Ceratocystidaceae are the respective symbionts of three independent lineages of ambrosia beetles with large, complex mycangia Chase G. MAYERSa, Douglas L. MCNEWa, Thomas C. HARRINGTONa,*, Richard A. ROEPERb, Stephen W. FRAEDRICHc, Peter H. W. BIEDERMANNd, Louela A. CASTRILLOe, Sharon E. REEDf aDepartment of Plant Pathology and Microbiology, Iowa State University, 351 Bessey Hall, Ames, IA 50011, USA bDepartment of Biology, Alma College, Alma, MI 48801, USA cSouthern Research Station, USDA Forest Service, Athens, GA 30602, USA dResearch Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans-Knoll-Str.€ 8, 07745 Jena, Germany eDepartment of Entomology, Cornell University, R.W. Holley Center for Agriculture and Health, Ithaca, NY 14853, USA fDivision of Plant Sciences, University of Missouri, 52 Agriculture Lab, Columbia, MO 65211, USA article info abstract Article history: The genus Ambrosiella accommodates species of Ceratocystidaceae (Microascales) that are ob- Received 23 May 2015 ligate, mutualistic symbionts of ambrosia beetles, but the genus appears to be polyphyletic Received in revised form and more diverse than previously recognized. In addition to Ambrosiella xylebori, Ambrosiella 28 July 2015 hartigii, Ambrosiella beaveri, and Ambrosiella roeperi, three new species of Ambrosiella are de- Accepted 3 August 2015 scribed from the ambrosia beetle tribe Xyleborini: Ambrosiella nakashimae sp. nov. from Xy- Available online 19 August 2015 losandrus amputatus, Ambrosiella batrae sp. nov. from Anisandrus sayi, and Ambrosiella Corresponding Editor: grosmanniae sp. nov. from Xylosandrus germanus. The genus Meredithiella gen. nov. is created Stephen W. Peterson for symbionts of the tribe Corthylini, based on Meredithiella norrisii sp. nov. from Corthylus punctatissimus. The genus Phialophoropsis is resurrected to accommodate associates of the Keywords: Xyloterini, including Phialophoropsis trypodendri from Trypodendron scabricollis and Phialophor- Ambrosia fungi opsis ferruginea comb. nov. from Trypodendron lineatum. Each of the ten named species was Scolytinae distinguished by ITS rDNA barcoding and morphology, and the ITS rDNA sequences of four Symbiosis other putative species were obtained with Ceratocystidaceae-specific primers and template DNA extracted from beetles or galleries. These results support the hypothesis that each ambrosia beetle species with large, complex mycangia carries its own fungal symbiont. Co- nidiophore morphology and phylogenetic analyses using 18S (SSU) rDNA and TEF1a DNA sequences suggest that these three fungal genera within the Ceratocystidaceae indepen- dently adapted to symbiosis with the three respective beetle tribes. In turn, the beetle gen- era with large, complex mycangia appear to have evolved from other genera in their * Corresponding author. Tel.: þ1 515 294 0582. E-mail address: [email protected] (T. C. Harrington). http://dx.doi.org/10.1016/j.funbio.2015.08.002 1878-6146/ª 2015 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. 1076 C. G. Mayers et al. respective tribes that have smaller, less selective mycangia and are associated with Raffae- lea spp. (Ophiostomatales). ª 2015 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. Introduction Ambrosiella spp. have so far been recovered or reported from five beetle genera (Harrington et al. 2014), and each of The six recognized species of Ambrosiella Brader ex Arx & Hen- these genera appear to have relatively large and complex nebert 1965 (Sordariomycetes: Microascales: Ceratocystidaceae)are mycangia with secretions directly through reticulated mycan- obligate, mutualistic symbionts of ambrosia beetles. Ambrosia gial walls. Within the tribe Xyleborini, species of Xylosandrus, beetles are an ecological group of more than 3400 species of my- Anisandrus, and Cnestus have large, internal mesonotal cophagous sapwood-boring beetles in the subfamilies Platypo- mycangia in female adults (Francke-Grosmann 1956, 1967; dinae and Scolytinae (Coleoptera: Curculionidae). Whereas Beaver 1989; Kinuura 1995; Hulcr et al. 2007; Stone et al. 2007; their bark beetle relatives generally feed on the nutritious inner Hulcr & Cognato 2010; Cognato et al. 2011a). In the Corthylini, bark (secondary phloem) of trees, ambrosia beetles tunnel in the Corthylus spp. have long, folded tubes that open into the pro- nutrient-poor sapwood and depend on mutualistic fungi for coxae of adult males (Finnegan 1963; Giese 1967). In the Xylo- their nutrition (Harrington 2005). The beetles generally do not terini, female Trypodendron spp. have large, tubular, pleural- eat wood while boring (Beaver 1989), though the larvae of prothoracic mycangia (Francke-Grosmann 1956, 1967; some ambrosia beetles ingest fungus-colonized wood (xylomy- Schneider & Rudinsky 1969b). cetophagy) (Roeper 1995; De Fine Licht & Biedermann 2012). The Ambrosiella initially included ambrosia beetle symbionts major food of both larvae and adults is ambrosial growth of with percurrent proliferation of conidiogenous cells vs. sympo- fungi within the sapwood tunnels. A diverse fungal flora grows dial proliferation by Raffaelea spp. (Brader 1964; von Arx & in ambrosia beetle galleries, but the dominant fungi are obligate Hennebert 1965; Batra 1967). Gebhardt et al. (2005) demon- symbionts of ambrosia beetles and have not been found as free- strated that some Raffaelea spp. have percurrent and sympodial living species (Harrington et al. 2010). proliferation, but Ambrosiella xylebori Brader ex Arx & Henne- The fungal symbionts rely on the beetles for dispersal and bert 1965, Ambrosiella hartigii L.R. Batra 1968, and Ambrosiella fer- are primarily carried by adult beetles in special sacs called ruginea (Math.-Ka€arik)€ L.R. Batra 1968 produced conidia from mycangia, in which the fungi grow in a budding yeast-like or phialides. Harrington et al. (2010) limited Ambrosiella spp. to arthrospore-like phase (Fraedrich et al. 2008; Harrington et al. the phialidic ambrosia fungi within the Ceratocystidaceae and 2014). In the studied cases of ambrosia beetle mycangia, gland Raffaelea spp. to symbionts within the Ophiostomatales.All cells secrete material into or near the mycangium to support known Ambrosiella spp. produce a fruity aroma (Harrington growth of the fungal symbionts (Schneider & Rudinsky 2009), and these volatiles may play a role in attracting ambrosia 1969a, 1969b), and the overflow of spores from the mycangium beetles within the galleries (Hulcr et al. 2011). inoculates the galleries during construction. Of the two weevil As now recognized, most Ambrosiella spp. produce large, subfamilies, the Platypodinae consist entirely of ambrosia bee- thick-walled, ovoid, terminal aleurioconidia with inconspicu- tles and have relatively small and simple mycangia ous collarettes and/or basipetal chains of cylindrical to barrel- (Nakashima 1975; Cassier et al. 1996; Marvaldi et al. 2002). In shaped phialoconidia via ring-wall building (Minter et al. 1983; contrast, ambrosia beetles arose at least 10 separate times Nag Raj & Kendrick 1993; Riggs & Mims 2000). The presence of from bark beetle lineages within the Scolytinae (Farrell et al. deep-seated phialides in the symbiont of Trypodendron scabri- 2001; Jordal & Cognato 2012; Kirkendall et al. 2015), each event collis (tribe Xyloterini), Ambrosiella trypodendri (L.R. Batra) apparently marked by the development of novel mycangia. T.C. Harr. 2010, was used to erect the monotypic genus Phialo- Generally, the Scolytinae mycangia are relatively small and phoropsis L.R. Batra 1968, but Harrington et al. (2010) placed harbor one or more species of Raffaelea Arx & Hennebert Phialophoropsis in synonomy with Ambrosiella. However, phy- 1965 (Ophiostomatales)(Cassar & Blackwell 1996; Harrington logenetic analyses have generally suggested that the two gen- & Fraedrich 2010; Harrington et al. 2010, 2014). These small era are distinct (Alamouti et al. 2009; Harrington 2009; Six et al. mycangia include oral pouches, pronotal pits, elytral pouches, 2009; Harrington et al. 2010; de Beer et al. 2014). and coxal enlargements, each of which are simple modifica- At present, there are six named species of Ambrosiella: A. tions of the adult beetle’s exoskeleton, with secreting gland trypodendri from T. scabricollis (Batra 1967); A. ferruginea from cells near the opening of the mycangium (Francke- Trypodendron lineatum (Batra 1967); Ambrosiella xylebori from Grosmann 1967; Beaver 1989). In contrast, certain genera of Xylosandrus compactus (Brader 1964); A. hartigii from Anisandrus Scolytinae exhibit markedly larger and more elaborate mycan- dispar (Batra 1967); Ambrosiella beaveri Six, de Beer & W.D. gia that are set entirely within the body and are composed of Stone from Cnestus mutilatus (Six et al. 2009); and Ambrosiella a reticular structure punctuated by gland cells secreting di- roeperi T.C. Harr. & McNew from Xylosandrus crassiusculus rectly into the mycangium (Francke-Grosmann 1956; (Harrington et al. 2014). In addition to X. compactus, A. xylebori Finnegan 1963; Schneider & Rudinsky 1969b; Stone et al. has been reported from Corthylus columbianus (Batra 1967; 2007). These larger, complex mycangia have specialized chan- Nord 1972) and Corthylus punctatissimus (Roeper 1995). Besides nels or tubes that direct the overflow of fungal growth to the An. dispar, A. hartigii has been reported from
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