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Partnerships Between Ambrosia Beetles and Fungi: Lineage-Specific Promiscuity Among Vectors of the Laurel Wilt Pathogen, Raffaelea Lauricola

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Partnerships Between Ambrosia Beetles and Fungi: Lineage-Specific Promiscuity Among Vectors of the Laurel Wilt Pathogen, Raffaelea Lauricola Microbial Ecology https://doi.org/10.1007/s00248-018-1188-y FUNGAL MICROBIOLOGY Partnerships Between Ambrosia Beetles and Fungi: Lineage-Specific Promiscuity Among Vectors of the Laurel Wilt Pathogen, Raffaelea lauricola J. R. Saucedo-Carabez1 & Randy C. Ploetz1 & J. L. Konkol1 & D. Carrillo1 & R. Gazis1 Received: 17 January 2018 /Accepted: 10 April 2018 # Springer Science+Business Media, LLC, part of Springer Nature 2018 Abstract Nutritional mutualisms that ambrosia beetles have with fungi are poorly understood. Although these interactions were initially thought to be specific associations with a primary symbiont, there is increasing evidence that some of these fungi are associated with, and move among, multiple beetle partners. We examined culturable fungi recovered from mycangia of ambrosia beetles associated with trees of Persea humilis (silk bay, one site) and P. americana (avocado, six commercial orchards) that were affected by laurel wilt, an invasive disease caused by a symbiont, Raffaelea lauricola, of an Asian ambrosia beetle, Xyleborus glabratus. Fungi were isolated from 20 adult females of X. glabratus from silk bay and 70 each of Xyleborus affinis, Xyleborus bispinatus, Xyleborus volvulus, Xyleborinus saxesenii,andXylosandrus crassiusculus from avocado. With partial sequences of ribosomal (LSU and SSU) and nuclear (β-tubulin) genes, one to several operational taxonomic units (OTUs) of fungi were identified in assayed individuals. Distinct populations of fungi were recovered from each of the examined beetle species. Raffaelea lauricola was present in all beetles except X. saxesenii and X. crassiusculus,andRaffaelea spp. predominated in Xyleborus spp. Raffaelea arxii, R. subalba,andR. subfusca were present in more than a single species of Xyleborus,andR. arxii was the most abundant symbiont in both X. affinis and X. volvulus. Raffaelea aguacate was detected for the first time in an ambrosia beetle (X. bispinatus). Yeasts (Ascomycota, Saccharomycotina) were found consistently in the mycangia of the examined beetles, and distinct, putatively co-adapted populations of these fungi were associated with each beetle species. Greater understandings are needed for how mycangia in ambrosia beetles interact with fungi, including yeasts which play currently underresearched roles in these insects. Keywords Avocado . Ophiostomatales . Microascales . Saccharomycetales . Curculionidae . Scolytinae Introduction Mycangia are specialized structures adapted for the trans- port and protection of fungal symbionts in ambrosia beetles Ambrosia beetles (Coleoptera: Curculionidae: Scolytinae and [64]. Diverse types of mycangia have evolved in different Platypodinae) have obligate nutritional relationships with lineages of these insects [40]. For example, in the tribe symbiotic fungi [23, 51]. These ancient, coevolved associa- Xyleborini, Xylosandrus spp. have large, complex invaginated tions represent the earliest known examples of fungus farming sacs in the elytra, mesonotal mycangia; Xyleborinus spp. have by insects [66]. Most of the nutritional mutualists are ascomy- small elytral mycangia; and Xyleborus spp. have small cavi- cetes in the Ophiostomatales, and, to lesser extents, in the ties inside the frontal portions of the head, preoral or mandib- Microascales and Hypocreales [23, 40, 51, 54, 55]. ular mycangia. Ambrosial mutualisms were originally thought to be species-specific interactions between a fungus and beetle * Randy C. Ploetz species [5, 28, 46]. Although recent studies have con- [email protected] firmed that specific associations occur in some beetle lin- eages, nonspecific interactions have been revealed in others [40, 50]. Recently, the degree of specificity in these 1 Tropical Research & Education Center, University of Florida, Homestead, FL 33031-3314, USA relationships was correlated with mycangium type [40, Saucedo-Carabez J. R. et al. 47, 50]. Using an environmental sequencing approach, unpublished). The role that alternative species of ambrosia Kostovcik et al. [47] reported that multiple fungal associ- beetles may play in the epidemiology of this disease is a topic ates with similar abundances were detected in mycangia of current research [15]. Previously, R. lauricola was recovered of Xyleborus affinis (Eichhoff) and Xyleborus ferrugineus from 6% (58 of 928) of the individuals of eight ambrosia beetle (Fabricius) (each with preoral mycangia), whereas com- species associated with avocado; 35% (n = 79) of one of these munities in Xylosandrus crassiusculus (Motschulsky) species, X. bispinatus, carried the pathogen [58]. (mesonotal mycangium) were dominated by a single sym- Recent results support the hypothesis that X. bispinatus biont, Ambrosiella sp. Similarly, Mayers et al. [50]found plays an important role in the epidemiology of laurel wilt on that single symbionts predominated in ambrosia beetle avocado. Artificial inoculations of avocado plants in no- species with large, complex mycangia. Although the choice conditions demonstrated its role as a vector of available data indicate that large, complex mycangia are R. lauricola [Carrillo et al., unpublished]. Furthermore, more selective environments than preoral mycangia, fur- laboratory-rearing experiments demonstrated that the beetle ther study is needed. could complete its life cycle when fed solely on a R. lauricola- Relatively little is known about the specific roles many fun- based artificial medium [61]. gal symbionts play in the life cycles of their beetle associates. In The present research had two main objectives. First, to discussing the fungal nutrition of Xyleborinus saxesenii improve understandings of the epidemiology of laurel wilt in Ratzeburg, De Fine Licht and Biedermann [17] suggested that avocado, we evaluated the presence of R. lauricola in X. different fungi might serve as food sources for adults and larvae affinis, X. bispinatus, X. volvulus, X. crassiusculus, and X. of X. saxesenii. Similarly, Biedermann et al. [9] proposed that saxesenii, each of which was prevalent in commercial or- auxiliary fungi might provide nutrients for the ambrosia beetle chards affected by the disease. Second, to shed light on the partners that supplement those provided by the primary nutri- biology of these interactions, we determined the identity and tional symbiont. abundance of other fungi inhabiting the mycangia of the Xyleborus glabratus Eichhoff (Coleoptera: Curculionidae: targeted beetle species. For the first time, we report associa- Scolytinae) originated in Southeast Asia; it was detected in the tions of several described and undescribed fungi with the am- Western Hemisphere in 2002 in Port Wentworth, Georgia, brosia beetles that were targeted in this study. For the first USA [31, 59]. Shortly afterwards, laurel wilt, a destructive time, we also report distinct internal communities of yeasts disease caused by the primary nutritional symbiont of (Ascomycota, Saccharomycotina) in ambrosia beetles. We X. glabratus, Raffaelea lauricola T.C. Harrington, Fraedrich propose that these are adapted relationships that coevolved & Aghayeva (Ophiostomatales), began killing trees of native with the different beetle species. This study provides new redbay (Persea borbonia Spreng) in the surrounding area insights into associations between mycangial fungi and mem- [24]. At least 14 tree species in the Lauraceae plant family bers of the Xyleborini, in particular those in the tribe’smost are now known to be susceptible to the disease, including an specious genus, Xyleborus. important commercial fruit crop, avocado (P. a m e ric an a Miller) [39]. Anthropogenic movement of infested wood has facilitated the long-distance spread of laurel wilt, but X. glabratus- Materials and Methods assisted spread has played a more important role in its local and mid-range movement [39]. Primary factors involved in Beetle Sampling the spread of the disease within and among avocado orchards are less clear [56, 57]. Although root-graft transmission of Ambrosia beetles were reared from trees affected by laurel R. lauricola apparently plays a major role in tree-to-tree wilt. Bolts were taken from six avocado orchards (three to spread, the vectors that initiate laurel wilt outbreaks in avoca- four trees from each orchard) in Miami-Dade County, do orchards are unclear [57]. Florida, and three trees of silk bay (Persea humilis Nash) Based on a study of the life cycle of X. glabratus,Braretal. from Highlands County, Florida (Table 1,Fig.1), and [12] indicated that avocado was not a good reproductive host placed in opaque plastic containers affixed with transpar- for the beetle. This may explain the uncommon association of ent glass jars lined with moist paper towels, as described X. glabratus with avocado in Florida. In 2012, X. glabratus previously [14]. Beetles that emerged from bolts were was not trapped or reared from field-collected bolts of avocado attracted to light,7 collected in the jars, and assayed while in Miami-Dade County (0 of 79,000 individuals of ambrosia still active. A total of 70 adult females each of X. affinis, X. beetles) and was identified only 11 times among 4181 individ- bispinatus, X. volvulus, X. crassiusculus,andX. saxesenii uals from Brevard County (Carrillo et al., unpublished). In were recovered from avocado, and 20 females of X. 2015, X. glabratus was not recovered among 176,252 individ- glabratus were reared from silk bay. Beetles were identi- uals collected in Miami-Dade County (Carrillo et al., fied by their morphological characteristics. Partnerships Between
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