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Invasive Asian Fusarium – Euwallacea ambrosia beetlemutualists pose a serious threat to forests, urban landscapesand the avocado industry
Kerry O’Donnell & Ran Libeskind-Hadas & Jiri Hulcr & Craig Bateman &
Matthew T. Kasson &Randy C. Ploetz & Joshua L. Konkol & Jill N. Ploetz &Daniel Carrillo &
Alina Campbell & Rita E. Duncan & Pradeepa N. H. Liyanage & Akif Eskalen &
Shannon C. Lynch & David M. Geiser & Stanley Freeman & Zvi Mendel & Michal Sharon &
Takayuki Aoki & Allard A. Cossé & Alejandro P. Rooney
Received: 26 July 2016 /Accepted: 30 September 2016# Springer Science+Business Media Dordrecht (outside the USA) 2016
Abstract Several species of the ambrosia beetleEuwallacea (Coleoptera: Curculionidae: Scolytinae)cultivate Ambrosia Fusarium Clade (AFC) species intheir galleries as a source of food. Like all otherscolytine beetles in the tribe Xyleborini, Euwallacea
are thought to be obligate mutualists with their fungalsymbionts. Published diversification-time estimatessuggest that the Euwallacea – Fusarium symbiosisevolved once approximately 21 million years ago.Female Euwallacea possess paired oral mycangia
PhytoparasiticaDOI 10.1007/s12600-016-0543-0
K. O’Donnell (*)Mycotoxin Prevention and Applied MycologyResearch Unit, National Center for Agricultural UtilizationResearch, US Department of Agriculture,Agricultural Research Service, 1815 North University Street,Peoria, IL 61604, USAe-mail: [email protected]
R. Libeskind-HadasDepartment of Computer Science, Harvey Mudd College,Claremont, CA 91711, USAe-mail: [email protected]
J. Hulcr :C. BatemanSchool of Forest Resources and Conservation, University ofFlorida, Gainesville, FL 32611, USA
J. Hulcre-mail: [email protected]
C. Batemane-mail: [email protected]
M. T. KassonDivision of Plant and Soil Sciences, West Virginia University,Morgantown, WV 26506, USAe-mail: [email protected]
R. C. Ploetz : J. L. Konkol : J. N. Ploetz :D. Carrillo :A. Campbell :R. E. DuncanTropical Research and Education Center, University of Florida,Homestead, FL 33031, USA
R. C. Ploetze-mail: [email protected]
J. L. Konkole-mail: [email protected]
D. Carrilloe-mail: [email protected]
P. N. H. LiyanageTea Research Institute of Sri Lanka, St Coombs, Talawakelle, SriLankae-mail: [email protected]
A. Eskalen : S. C. LynchDepartment of Plant Pathology and Microbiology, University ofCalifornia, Riverside, CA 92521, USA
A. Eskalene-mail: [email protected]
S. C. Lynche-mail: [email protected]
within which foundresses transport their Fusarium sym-biont vertically from their natal gallery to new woodyhosts. During the past two decades, exotic AsianEuwallacea – Fusarium mutualists have been intro-duced into the United States, Israel and Australia.Because these invasive pests attack and can reproduceon living woody hosts, they pose a serious threat tonative forests, urban landscapes and the avocadoindustry.
Keywords Ambrosia FusariumClade . Fungiculture .
Mutualism . Phylogenetics . Symbiosis . Xyleborini
Introduction
This review is intended to provide basic and appliedagricultural scientists with a brief introduction to thephylogenetic diversity of exotic Asian Euwallacea
ambrosia beetles (Coleoptera: Curculionidae:Scolytinae) and the fungi in the Ambrosia FusariumClade (AFC; Hypocreales: Nectriaceae) that they culti-vate as a source of food. Diversification time estimatesplace the evolutionary origin of the Euwallacea –Fusarium mutualistic symbiosis in the early Mioceneapproximately 21million years ago (Jordal and Cognato2012; Kasson et al. 2013). Of the 11 independent evo-lutionary origins of fungus-farming by arthropods, thisis the only known one in which fusaria are cultivated byambrosia beetles for nutrition. Fungiculture by the am-brosia beetles is thought to be obligate because there areno known reversals to phloem-feeding (Farrell et al.2001). In contrast to males that are haploid, lackmycangia and are flightless, female Euwallacea arediploid, possess paired oral mycangia within which theytransport fusaria, and sometimes other fungal associatesor commensals when they fly from their natal gallery toa suitable woody host where they establish a new gal-lery. See Fig. 1 for salient features of the Euwallacea lifecycle. Because Fusarium species, and the highly inbredhaplo-diploid Euwallacea ambrosia beetles that farmthem are notoriously difficult, if not impossible, to dis-tinguish morphologically, genealogical concordancephylogenetic species recognition-based analyses(Taylor et al. 2000) of multilocus DNA sequence data(Kasson et al. 2013; O’Donnell et al. 2015) were used toinfer species limits within the paired mutualists.
The economically destructive shot-hole borer ofChinese tea (Camelia sinensis (L) Kuntze) in SriLanka was the first Euwallacea – Fusarium symbiosisto be studied in any detail, although these mutualistswere originally reported as Xyleborus fornicatus(Eichhoff) and Monacrosporium ambrosium Gadd &Loos, respectively (Gadd and Loos 1947). Unaware ofthe aforementioned publication, Brayford (1987)redescribed the same species as Fusarium bugnicourtiiBrayford from a Chinese tea plantation in Chinchona,India. After Nirenberg (1990) recognized these taxa asconspecific, M. ambrosium was recombined inFusarium as F. ambrosium (Gadd & Loos) Agnihothr.& Nirenberg and F. bugnicourtii was reduced to synon-ymy with F. ambrosium.
Euwallacea spp. attack live exotic tree species inmanaged settings, such as avocado orchards and urbanvegetation, and in invaded ranges it also colonizes nat-urally occurring hosts. As such, they pose a significantthreat to naïve forests, urban landscapes and fruit pro-duction worldwide, particularly avocado. Research
D. M. GeiserDepartment of Plant Pathology and Environmental Microbiology,Pennsylvania State University, University Park, PA 16802, USAe-mail: [email protected]
S. Freeman : Z. Mendel :M. SharonInstitute of Plant Protection, ARO, The Volcani Center, BetDagan 50250, Israel
S. Freemane-mail: [email protected]
Z. Mendele-mail: [email protected]
M. Sharone-mail: [email protected]
T. AokiGenetic Resources Center (MAFF), National Agriculture andFood Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki305-8602, Japane-mail: [email protected]
A. A. CosséOtis Laboratory, USDA-APHIS-PPQ-CPHST, 1398 W. TruckRoad, Buzzards Bay, MA 02542, USAe-mail: [email protected]
A. P. RooneyCrop Bioprotection Research Unit, National Center forAgricultural Utilization Research, US Department of Agriculture,Agricultural Research Service, 1815 North University Street,Peoria, IL 61604, USAe-mail: [email protected]
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interest in the Euwallacea – Fusarium symbionts hasincreased dramatically within the past several years dueto introductions of these Asian mutualists into Israel(Mendel et al. 2012), the United States (Thomas 2012;Atkinson 2016; Eskalen et al. 2013; Ploetz et al. 2013;O’Donnell et al. 2015), Panama and Costa Rica(Kirkendall and Ødegaard 2007) (Fig. 2). Managementstrategies for the polyphagous shot hole borer (PSHB,Euwallacea sp. #1 sensu O’Donnell et al. 2015) havebeen investigated extensively over the past few years inIsrael and California (Mendel et al., in preparation).Successful preventive measures for urban vegetationare based on intensive applications of insecticides tohealthy or newly infested trees, which results in a con-spicuous knockdown effect, combined with soil appli-cation or stem injections of neonicotinoids. While thesemeasures may serve to protect ornamental vegetation,they are unfit for avocado plantations due to hazardsposed by insecticide residues and disruption of the bio-logical control balance of other pests. Major manage-ment efforts in avocado plantations rely on selectivepruning of beetle infested branches and strict sanitation.
Molecular phylogenetic analyses have providedstrong support for a monophyletic evolutionary origin
of the Fusarium-farming Euwallacea and the AFC(Kasson et al. 2013; O’Donnell et al. 2015); the latteris nested within the species-rich F. solani species com-plex (O’Donnell et al. 2008, 2013). Because only two ofthe AFC species have been described formally, the 12genealogically exclusive species lineages were distin-guished as AF-1 through AF-12. Nine AFC species arecurrently known to be cultivated by seven differentEuwallacea spp. (O’Donnell et al. 2015). TheFusarium-farming Euwallacea clade comprises eightphylogenetically distinct species, six of which representcryptic species lineages within the morphospeciesE. fornicatus (Eichhoff). The six genealogically exclu-sive species within this morphospecies were distin-guished as E. sp. #1 through #6 (Fig. 1 in O’Donnellet al. 2015); E. sp. #4 from Chinese tea in Sri Lankamay represent E. fornicatus since this species wasoriginally described in this country (Eichhoff 1868).The finding that the morphospecies E. fornicatus rep-resents several cryptic species suggests that the adven-tive populations reported from multiple countries mayalso be different species. At least four of the six phylo-genetic species within the E. fornicatus Clade can useavocado (Persea americana Miller) as a reproductivehost (Freeman et al. 2012; Mendel et al. 2012; Eskalenet al. 2013), including E. sp. #1 – F. euwallaceae S.Freeman, Z. Mendel, T. Aoki & O’Donnell AF-2(Freeman et al. 2013) in Israel and the Los AngelesBasin in southern California, E. sp. #2 – F. spp. AF-6and AF-8 in Miami-Dade County, Florida, E. sp. #3 –F. sp. AF-7 in Queensland, Australia, and E. sp. #5 – F.sp. AF-12 in San Diego and Orange Counties,California (Fig. 2). In addition to the three aforemen-tioned infestations of E. fornicatus-like ambrosia bee-tles within the United States, the Asian E. interjectus(Blandford) is currently widespread throughout south-eastern U. S. (Cognato et al. 2015), while E. validus(Eichhoff) has spread across eastern North Americaattacking the Asian exotic tree-of-heaven (Ailanthusaltissima (Mill.) Swingle) when it is stressed byVerticillium wilt (Kasson et al. 2013) (Fig. 2). In addi-tion, Euwallacea denticulus (Motschulsky), which isattacking carob (Ceratonia siliqua L.) in the U. S. andIsrael, is currently being characterized (http://biotaxa.org/Zootaxa/article/view/zootaxa.3974.3.6;Freeman andMendel, unpubl.).
Given that several exotic pest insects have switchedor gained fungal associates after they were introducedinto nonindigenous areas (Wingfield et al. 2010;
Fig. 1 Life cycle of the polyphagous shot hole borer (PSHB,Euwallacea sp. #1 sensu O’Donnell et al. 2015). This ambrosiabeetle is endemic to Asia, but has invaded Israel and the LosAngeles Basin where it farms Fusarium euwallaceae on avocadoand diverse woody hosts (Eskalen et al. 2013; Freeman et al.2013)
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Carrillo et al. 2014), co-phylogenetic analyses wereconducted to assess symbiont fidelity within theEuwallacea – Fusarium mutualism (O’Donnell et al.2015). If this mutualism was driven by strict co-speciation (i.e., parallel cladogenesis), then opposedEuwallacea – Fusarium phylogenies should be highlyconcordant (i.e., near mirror images of one another).By contrast, if this mutualism was driven by host-shiftspeciation, then the opposed phylogenies should rep-resent a highly discordant tanglegram in which thelines connecting paired mutualists crisscross (deVienne et al. 2013).
Overlapping of galleries provides the opportunityfor intraspecific horizontal transmission of symbionts;therefore, host-shift speciation is possible on an evo-lutionary time scale. That is, a mixed vertical –horizontal mode of symbiont transmission might oc-cur occasionally in which Fusarium symbionts weretransmitted vertically in mycangia of adult femalesaccompanied by a horizontal switch at the larval-
pupal stage to another AFC species (Bright andBulgheresi 2010). The available data indicated thatmutualism co-biogeography abounds with horizontalswitches and multi-partner associations (Fig. 3). Forexample, two of the seven Euwallacea spp. analyzedcultivate two closely related AFC species: E. sp. #4(probably E. fornicatus) farms F. ambrosium AF-1and F. sp. AF-11 on Chinese tea in Sri Lanka andE. sp. #2 cultivates F. spp. AF-6 and AF-8 on avo-cado in Miami-Dade County, Florida (O’Donnellet al. 2015). In addition, maximum parsimony-basedco-phylogenetic analyses (Conow et al. 2010; Merkleet al. 2010) suggest that Euwallacea spp. haveswitched fusarial symbionts at least five times overthe evolutionary history of this mutualism. However,obligate feed requirement was observed forF. euwallaceae and its Euwallacea sp. #1 beetle host,while F. ambrosium did not allow development andreproduction of this beetle when provided as an al-ternative food source (Freeman et al. 2012).
Fig. 2 A red star is used to identify where the different Fusarium-farming Euwallacea ambrosia beetles and Ambrosia FusariumClade (AFC) species were collected (Kasson et al. 2013;O’Donnell et al. 2015). The symbiont of E. sp. #6 on breadfruit(Artocarpus altilis (Parkinson) Fosberg) in Papua New Guinea(Cognato et al. 2011) was not identified, but we hypothesize thatit is a member of the AFC. The report of E. fornicatus in Panamaand Costa Rica (Kirkendall and Ødegaard 2007) needs to beverified using DNA sequence data. We hypothesize that the fol-lowing three AFC species are cultivated by Euwallacea spp.:
Fusarium sp. AF-5 NRRL 22231 on rubber tree (Heveabrasiliensis Müll. Arg.) in Malaysia, Fusarium sp. AF- 9 NRRL66088 on royal poinciana Delonix regia (Bojer) Raf. in Miami-Dade County, Florida, and Fusarium sp. AF-10 NRRL 62941 onan unknown host in Singapore. Avocado +, avocado and otherwoody hosts; beetle ?, not identified; E. sp. ?, Euwallacea sp. notidentified; E. fornicatus*, presumed to be authentic for this speciesbased on 15 conspecific collections from tea at various locations inSri Lanka, which is where this species was described originally;host ?, not identified
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Future directions
A comparative phylogenomic analysis of the AFC wasinitiated in collaboration with Jason Stajich at theUniversity of California-Riverside and Matthew T.
Kasson at West Virginia University. To date, draft ge-nomes have been generated in-house at the USDA inPeoria for the following seven AFC species: Fusariumambrosium AF-1, F. euwallaceae AF-2, Fusarium sp.AF-3, Fusarium sp. AF-4, Fusarium sp. AF-6,
Fig. 3 Opposed most-parsimonious trees (MPTs) inferred frommultilocus data for seven Ambrosia Fusarium Clade (AFC) spe-cies and five fungus-farming Euwallacea ambrosia beetles cur-rently within the U.S. The auxiliary lines that are used to identifythe paired mutualists crisscross, which is consistent with repeatedhost shifts. Note that Euwallacea sp. #2 cultivates two differentAFC species in Miami-Dade County, Florida. Also note that it is
unknown whether Fusarium sp. AF-9 from Costa Rica andMiami-Dade County, Florida is farmed by Euwallacea. Maximumparsimony bootstrap values based on 2000 pseudoreplicates of thedata are indicated above internodes. Outgroups chosen to root thephylogenies were based onmore inclusive analyses (Cognato et al.2011; O’Donnell et al. 2015). CI, consistency index; PIC, parsi-mony informative characters; RI, retention index
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Fusarium sp. AF-8, and Fusarium sp. AF-12. RNA-seqdata were also generated for F. euwallaceae AF-2,which should help improve annotation of the genome.By sampling across the phylogenetic breadth of theAFC, and related non-ambrosia fusaria, we hope toaddress several questions concerning their populationbiology and whether the 21-million-year-old mutualismhas shaped their genomes and gene content. For exam-ple, does the striking morphological transition fromproduction of iconic fusiform to clavate macroconidiarepresent an adaptation for the symbiosis (Fig. 4; alsosee Fig. 3 in Kasson et al. 2013), analogous togongylidia produced by agarics cultivated by the leaf-cutter ants (Schultz and Brady 2008) or the swollenhyphae and conidia in ambrosial fungi such asGeosmithia (Kolařík and Kirkendall 2010) orRaffaelea (Seifert et al. 2013)? Then, what is the under-lying genetic basis of this morphological transition?Also, although the AFC species are thought to be prop-agated asexually, population genetic analyses are need-ed to assess whether there is evidence of a cryptic sexualor parasexual cycle. If a sexual cycle appears to beabsent, then how do they avoid the mutational melt-down known as Muller’s ratchet (Muller 1932, 1964;Moran 1996)? Preliminary evidence suggests that thefusaria (Kasson et al. 2013) and the highly inbredEuwallacea (O’Donnell et al. 2015) may generate novel
genetic variation via interspecific hybridization. Thoughtechnically challenging, transcriptomic analyses of AFCwithin mycangia are needed to understand what specificgenes are induced by the symbiosis and what signalingpathways are involved in communication betweenFusarium and Euwallacea. This basic informationmay help develop tools to prevent establishment of thesymbiosis or enable the development of methods toimpair or disrupt communication among these econom-ically destructive mutualists. Now that techniques areavailable to mass rear Euwallacea spp. that farmFusarium in the laboratory (Cooperband et al. 2016),experiments can be conducted to assess whether thesymbiotic pairs exhibit strict specificity (Freeman et al.2012), or whether the beetles can complete their lifecycles when reared on other AFC species. In additionto elucidating symbiont fidelity, these studies shouldgreatly increase our understanding of Euwallacea repro-ductive biology, including their phenology, fecundityand female-biased sex ratios. These basic and appliedstudies are urgently needed given the serious threat theseexotic mutualists pose to urban landscapes, forests andthe avocado industry.
Acknowledgments Thanks are due to Stacy Sink for excellenttechnical assistance, and Nathane Orwig and Amy McGovern forrunning the Sanger and IlluminaMiSeq sequence data at NCAUR.
Fig. 4 a-c The morphological transition from production of strict-ly fusiform conidia (Fig. 4a. Fusarium sp. AF-6 NRRL 62591), tomixed production of fusiform and clavate conida (Fig. 4b. Fusar-ium sp. AF-8 NRRL 62586), to fixed production of clavate conidia
by derived species lineages within the AFC (Fig. 4c. F. ambrosiumAF-1 NRRL 46583; also see Fig. 3 in Kasson et al. 2013) mayrepresent an adaptation for symbiosis
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Mention of trade names or commercial products in this publicationis solely for the purpose of providing specific information and doesnot imply recommendation or endorsement by the U.S. Depart-ment of Agriculture. USDA is an equal opportunity provider andemployer. JH and CCBwere partially funded by the USDA ForestService agreement 12-CA-11420004-042, USDA FarmBill agree-ment 12-8130-0377-CA, and the National Science FoundationDEB 1256968.
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