The Ambrosia Symbiosis: from Evolutionary Ecology to Practical Management Jiri Hulcr and Lukasz L

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ANNUAL REVIEWS Further Click here to view this article's online features: • Download ﬁgures as PPT slides • Navigate linked references • Download citations The Ambrosia Symbiosis: From • Explore related articles • Search keywords Evolutionary Ecology to Practical Management

Jiri Hulcr1,2 and Lukasz L. Stelinski2,3

1School of Forest Resources and Conservation, University of Florida, Gainesville, Florida 32611; email: hulcr@uﬂ.edu 2Entomology and Nematology Department, University of Florida, Gainesville, Florida 32611 3Citrus Research and Education Center, University of Florida, Lake Alfred, Florida 33850; email: stelinski@uﬂ.edu

Annu. Rev. Entomol. 2017. 62:285–303 Keywords First published online as a Review in Advance on agriculture, pest management, plant pathogens, social evolution, speciﬁcity November 16, 2016

The Annual Review of Entomology is online at Abstract ento.annualreviews.org The ambrosia beetle–fungus farming symbiosis is more heterogeneous than This article’s doi: previously thought. There is not one but many ambrosia symbioses. Beetle- 10.1146/annurev-ento-031616-035105 Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org fungus speciﬁcity is clade dependent and ranges from strict to promiscuous. Copyright c 2017 by Annual Reviews. Each new origin has evolved a new mycangium. The most common rela- All rights reserved tionship with host trees is colonization of freshly dead tissues, but there are

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. also parasites of living trees, vectors of pathogenic fungi, and beetles living in rotten trees with a wood-decay symbiont. Most of these strategies are driven by fungal metabolism whereas beetle ecology is evolutionarily more ﬂexible. The ambrosia lifestyle facilitated a radiation of social strategies, from fungus thieves to eusocial species to communities assembled by attraction to fungal scent. Although over 95% of the symbiotic pairs are economically harmless, there are also three types of pest damage: tree pathogen inoculation, mass accumulation on susceptible hosts, and structural damage. Beetles able to colonize live tree tissues are most likely to become invasive pests.

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INTRODUCTION Almost 200 years ago, an entomologist first watched a minute, xylem-boring beetle in its tunnel feeding on a white substance of unknown origin (88). The substance—now known to be a fungus— was termed ambrosia, the food of gods. For nearly two centuries thereafter, the ambrosia symbiosis remained a marginal curiosity studied by only a handful of academics. This is changing. Today, the study of the ambrosia system is among the most active directions in insect symbiosis research glob- ally. Interest in the beetles and fungi, unparalleled in diversity and economic impact compared to other fungus-farming symbioses, has surged, with approximately one research article published per week (see Thomson Reuters Web of Science at http://ipscience.thomsonreuters.com/product/ web-of-science/). The system is emerging as a useful model of eukaryotic symbioses for several reasons. First, it offers an opportunity to study symbiosis in a truly comparative, hypothesis-testing framework due to the many independent origins among bark beetles and weevils (Coleoptera: Cur- culionidae: Scolytinae and Platypodinae) (46, 62) and at least seven origins in fungi (five or more in Ascomycota and two or more in Basidiomycota) (1, 4, 69). Second, the ambrosia symbiosis can be studied by anyone and anywhere: Many species are as common in tropical jungles as in city suburbs and are very easy to collect or trap. Finally, the system abounds with unanswered questions that are becoming relatively easy to answer as our technological capabilities grow. Fungal symbionts have been studied in fewer than 5% of ambrosia beetle species. There remain over 3,000 ambrosia beetle species, and five independent origins of the symbiosis, in which the fungi have never been investigated. Although serving as an emerging academic topic, the wood-boring beetle–fungus consortia have also earned a more sobering reputation: Many have emerged from being inconspicuous wood-degraders to being major threats to forest health. Human-imported beetle-fungus consortia have spread across continents. Some of the fungi turned out to be pathogenic and have killed millions of naive host trees. In the 10 years since the invasion into the southeastern United States of the Asian beetle Xyleborus glabratus and its previously unknown mycobiont Raffaelea lauricola, over 500 million trees in the family Lauraceae have been killed (94). Avocado production in Florida and elsewhere is also at risk (94). This was impossible to predict because there was no information about these species before they became invasive. Similarly, California and Israel were recently invaded by the polyphagous shot hole borer, Euwallacea aff. fornicatus, and its symbiont, Fusarium euwallaceae. This pathosystem has killed thousands of trees in city streets, botanical gardens, and fruit orchards since 2012. In this case, as well, the fungal pathogen was unknown to science prior to its invasion (77).

AMBROSIA BEETLES Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org Ambrosia beetles are a polyphyletic assemblage of independently evolved clades within weevils, mostly within bark beetles, that employ fungus farming in trees as their dominant ecological

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. strategy. How many times did ambrosial fungus farming evolve? The number is still not entirely clear. One reason is that ongoing phylogenetic analyses of the beetles and fungi involved are updating the traditional classification. Among the beetles, there are 11 unambiguous origins of fungus farming (Figure 1). However, there may be as many as five additional clades that appear to be descendants of separate origins of the symbiosis (Table 1). Another reason for the uncertainty is that there are species in which fungus farming is assumed but not proven, such as within the Hypothenemus birmanus group or the large beetles in the genera Dactylipalpus and Phloeoborus.Other species grow nutritional fungi and could be classified as ambrosial, but their other traits differ from typical ambrosia beetles. That is the case with many phloem-feeding bark beetles associated with fungi, including several Dendroctonus spp., Ips spp., Pityoborus spp., and Tomicus minor (37). Their

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larvae build individual galleries, as do the larvae of other bark beetles, but feed predominantly on speciﬁc nutritional fungal symbionts. They may represent an intermediate step in the evolution from the bark beetle habit to the true ambrosia beetle symbiosis. The origins of ambrosia feeding in different bark beetle groups have occurred relatively regu- larly through time. The oldest group is the Platypodinae, and on the other end of the spectrum of evolutionary age are several recently evolved ambrosia groups with only one or a few species (54). There is no overall correlation between the number of species within a clade and the clade’s age. Similarly, a transition from phloem feeding to the ambrosia symbiosis does not automatically lead to increased species diversity. Several groups ﬁrst appeared during warmer geological periods

Oral mycangia & Flavodon RaffaeleaOral mycangia and Euwallacea

Xylosandrus group assoc. associates

Amasa Xyleborinus Premnobiina clade Xyleborini Tomicus minor Dendroctonus frontalis

Ips spp. ?

Scolytoplatypodini Scolytodes unipunctatus Xyloterini Platypodinae Hypothenemus spp. Weevil ancestor

Camptocerus Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org Sueus ?

Corthylini Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only.

Bothrosternini s. str.

Dactylipalpus Phloeoborus Hyleops Pityoborus

Xylem Phloem

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(54), but their subsequent diversiﬁcation has not been correlated with climate. There is only a single possible reversal from ambrosia feeding back to phloem feeding in the Camptocerus clade (Scolytini), accompanied by the reduction of the mycangium (93).

AMBROSIA FUNGI The best-known ambrosia fungi belong to the order Ophiostomatales, particularly the genus Raf- faelea andtoalesserextentAfroraffaelea. Raffaelea is one of the most widespread ambrosial mutualist genera, having colonized many independent beetle groups throughout its evolution. This appear- ance of evolutionary infidelity may be inflated by the fact that the genus is polyphyletic, currently containing at least two independent origins of the symbiosis in unrelated Ophiostomatales (24). Several Raffaelea species, such as R. lauricola and R. quercivora, have a significant economic and ecological impact. Ophiostomatales also contain fungi that are associated with fungus-feeding bark beetles (i.e., beetles that culture fungi in the phloem and are usually not considered to be ambrosia beetles), including Ceratocystiopsis, Ophiostoma,andGrosmannia (1, 16, 89), and their nutritional role and transmission via mycangia probably satisfy the definition of an ambrosia fungus. Distantly related to Ophiostomatales, the Microascales also include multiple groups of ambrosia fungi, of which some are important and widespread: Ambrosiella, Meredithiella,andPhialophoropsis (75). The massive fungal genus Fusarium also contains bona fide ambrosial mutualists, currently grouped in the Ambrosia Fusarium Clade (AFC), in which species are not named but numbered (56, 81). Yeasts have always been reported from galleries and mycangia of ambrosia beetles, but the only true ambrosial clade in Saccharomycetales is the genus Ambrosiozyma. These are fungi highly evolved for mutualism with beetles, are found in Corthylini and some Platypodinae, and are probably rather promiscuous. Many other, nonspecific yeasts are routinely reported, including various Candida spp. and Pichia spp. Their abundance often surpasses that of the primary mutualists in terms of colony-forming units on agar plates or marker reads in DNA sequencing studies. However, the same species are often isolated from unrelated beetle species and are probably nonspecific commensals or parasites, occurring in subcortical spaces created by any wood borer (13, 22, 34). The genus Geosmithia (Hypocreales) contains mostly commensals of bark beetles in dry mi- crohabitats, such as in branches where Ophiostomatales are absent. However, several Geosmithia species are true nutritional mutualists of ambrosia beetles (63, 64). The most intriguing aspect of ←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−

Figure 1

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org The diversity and relationships of ambrosia beetle groups. Phylogeny adapted from Reference 46. Clade breadth represents approximate species diversity. Blue-marked clades are ambrosia beetles inhabiting xylem; red-marked clades are phloeomycetophagous beetles inhabiting phloem. Solid yellow line indicates outline of the mycangium as visible externally; dashed yellow line indicates outline of the internal mycangium where Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. not visible externally. Clockwise, from the root (photos by Jiri Hulcr unless noted otherwise): Diapus quinquespinatus, Platypus sp., Ips acuminatus, Premnobius cavipennis (photo by Craig C. Bateman), Xylosandrus crassiusculus, Xyleborus pinicola, Ambrosiophilus atratus, Euwallacea fornicatus, Amasa sp., Xyleborinus andrewesi, Tomicus minor, Dendroctonus frontalis, Scolytoplatypus eutomoides, Scolytodes unipunctatus (photo by Thomas H. Atkinson), Trypodendron sp. (photo by Craig. C. Bateman), Hypothenemus curtipennis (photo by Andrew J. Johnson), Sueus niisimai (photo by Andrew J. Johnson), Corthylus papulans (photo by Andrew J. Johnson), Monarthrum fasciatum (photo by Andrew J. Johnson), Pityoborus comatus (photo by Andrew J. Johnson), Phloeoborus orinocensis (photo by Sarah M. Smith, available at http://barkbeetles.info, reprinted with permission from the Smithsonian Institution), Dactylipalpus grouvellei (photo by Andrew J. Johnson), Eupagiocerus dentipes (photo by Sarah M. Smith, available at http://barkbeetles.info, reprinted with permission from the Smithsonian Institution), Camptocerus niger (photo by Craig C. Bateman).

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Table 1 Associations between ambrosia beetles and ambrosia fungia Most inclusive taxon Associated fungi Mycangium Note Reference(s) 1 Phloeoborus Unknown Setose patch on each Association inferred from the — proepisternum presence of mycangia; ecology not known. 2 Dactylipalpus Unknown Transverse furrow on Association inferred from the 86 pronotum presence of mycangia; ecology not known, but eggs are laid in a group in a communal chamber. 3 Sueus Unknown Unknown Ambrosial habit obvious; 8 garden development slow. 4 Bothrosternini Geosmithia spp. Setose patch on each Unclear whether the separate 64, 102 (Bothrosternus, proepisternum genera represent one or two Eupagiocerus, origins; breadth of Cnesinus) Geosmithia unclear. 5 Scolytodes Raffaelea spp. Unknown The only Scolytodes species 50 unipunctatus known to be ambrosial; others feed on tree tissues. 6 Hyleops Unknown Unknown — 9 7 Camptocerus s. str. Unknown Circular depression Sister clade to Cnemonyx. 93 on pronotum 8 Camptocerus s. l. Unknown Circular depression Derived from within 93 on pronotum Cnemonyx. 9 Scolytoplatypodini Ambrosiella spp. Pronotal and/or The main symbiont grows 10, 80 (Microascales) proepisternal pits poorly on commonly used media and association with Ambrosiella was inferred only from morphology in the gallery. However, the twig-/branch-boring habit of the beetles and complex thoracic mycangia suggest that Ambrosiella is the most likely candidate. 10 Xyloterini Phialophoropsis Paired tubules inside Of the three genera, only 75 (Microascales), pronotum Trypodendron has been well Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org possibly also studied. Xyloterinus was Candida spp. studied with contradictory results (76, 97), suggesting

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. that the primary mutualist maybeseasonaland fastidious. (Continued )

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Table 1 (Continued ) Most inclusive taxon Associated fungi Mycangium Note Reference(s) 11 Xyleborini: Flavodon ambrosius Preoral The fungal mutualist is an 57, 71 Ambrosiodmus and (Polyporales) aggressive wood-rot Ambrosiophilus fungus. 12 Xyleborini: Ambrosia Fusarium Preoral Multiple species within the 56, 81 Euwallacea clade (AFC) Fusarium solani species species complex have evolved a strict ambrosial habit. 13 Xyleborini: Ambrosiella spp. Deep mesonotal Large clade with six 1, 75 Xylosandrus clade (Microascales) membranous genera, including several (Anisandrus, invagination pests; all have similar Cnestus, Diuncus, habits including boring Eccoptopterus, into twigs and branches Hadrodemius, and probably high Xylosandrus) speciﬁcity to their fungus species. 14 Xyleborini: Amasa Raffaelea “Esteya” Paired preoral Amasa was reported as 14, 24, 35, 38 group associated with Dryadomyces but that has been synonymized with Raffaelea. 15 Xyleborini: Raffaelea s. str, Paired preoral The most commonly 29, 65, 87 Xyleborus many species (sometimes studied ambrosia beetles. inaccurately called Many Xyleborus s. str. can mandibular) vector several different Raffaelea species and other fungi, representing a promiscuous relationship. 16 Xyleborini: Raffaelea “Esteya” Paired cavity at the The Raffaelea species in 14, 24, 39 Xyleborinus group base of pronotum this clade are of a adjacent to different origin than scutellum; also in those associated with the gut Xyleborus. 17 Other Xyleborini No published Mostly unknown; Preliminary observations — genera record several Old World suggest that this diverse

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org genera appear to group contains other have metanotal or unexplored symbioses. elytral mycangia For example, some (Coptodryas, Microperus may be Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. Pseudowebbia, associated with a Cryptoxyleborus) white-rot fungus similar to Ambrosiodmus. Webbia, Schedlia, and related genera are very host speciﬁc, suggesting a novel fungus. (Continued )

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Table 1 (Continued ) Most inclusive taxon Associated fungi Mycangium Note Reference(s) 18 Corthylini: Ambrosiozyma Paired procoxal The ambrosial Corthylini 87, 99 Monarthrum and (Saccharomycetales), cavity or pregular may be paraphyletic or Gnathotrichus Raffaelea pocket polyphyletic and appear (Ophiostomatales) to have evolved different symbioses. The genera Monarthrum and Gnathotrichus have been studied repeatedly but with contradictory results. Older reports of Ambrosiella refer to species that are now classiﬁed as Raffaelea. 19 Corthylini: Meredithiella Tubules in prothorax — — Corthylus (Microascales) 20 Premnobiina Afroraffaelea Preoral (probably not — 4 (Ophiostomatales) homologous to Xyleborini) 21 Hypothenemus Unknown Unknown Galleries of several other 86 concolor Hypothenemus species (e.g., Hypothenemus birmanus, Hypothenemus dissimilis) resemble the ambrosia system, but fungus is apparent. 22 Hypothenemus Unknown Setose depressions on Hypothenemus curtipennis 9 curtipennis pronotum and Hypothenemus concolor morphology and biogeography support placement in different sections of the genus, suggesting independent origins of the ambrosia habit. 23 Platypodinae Raffaelea s. str., Pronotal pits, Platypodinae are the 11, 53, 60, 66

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org Raffaelea “Esteya” furrows, and frontier of ambrosia group, Ambrosiozyma cavities; epistomal research due to poor spp. cavity in some fungus sampling, Euplatypus phylogenies being only Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. recently available, and the great diversity of mycangia.

aThe records represent independent evolutionary associations, not necessarily taxonomic groups. An independent association is deﬁned either as a new origin of the ambrosia habit in beetles within a non–ambrosial beetle clade or as a new association between an existing ambrosia beetle clade and distinct new fungal mutualists. Associations that are new only from the fungal side are not listed, because the fungal aspect is less well understood. Most ambrosia beetles carry, and probably consume, multiple fungal species, but in the majority of cases, one species or a genus is the most ecologically prevalent and nutritionally signiﬁcant.

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these discoveries is that these few beetle species represent unrelated genera from South Amer- ica, a continent where the ambrosia symbiosis has been explored much less than elsewhere. This suggests that Geosmithia may be the prevalent ambrosia fungi in the Neotropics.

THE SYMBIOSIS How many species of fungi are in a beetle mycangium, and what are they doing there? The paradigm of ambrosia symbiosis specificity has been changing as dramatically as the methodology with which the symbiosis is investigated. The traditional focus on a single, primary symbiont was a product of (a) the assumption that the symbiosis is a one-on-one relationship (5, 32, 79) and (b) the culturing approaches that typically underestimate the fungal diversity, such as plating from an entire crushed beetle or from chunks of gallery wall, which allow only one or a few competitive taxa to proliferate. The more recent view treats the fungal associates as communities, as a result of a more quantitative method of dilution culturing and because researchers have investigated beetle species that naturally carry multiple fungi (3). The community-like pattern has been lately corroborated in some cases by the introduction of high-throughput DNA-based approaches (65). Most recently, with the integration of complementary research methods and truly global sampling, investigators are seeing the emergence of a new paradigm that appreciates the differences between fungus-beetle associations (4, 71, 75): There may be as many degrees of specificity and mechanisms of maintenance as there are origins of these symbioses. Beetle clades with large and complex mycangia are typically strictly associated with individual fungal species from Microascales (75). However, no similar conclusion can yet be made with respect to other types of mycangia, particularly in beetle groups with oral mycangia (which are not necessarily homologous). For example, Xyleborini in the Xyleborus s. str. group are among the most promiscuous, typically carrying several species of Raffaelea (19, 39, 65). Euwallacea also have oral mycangia and can accommodate several species of their AFC and occasionally also Raffaelea, but any individual beetle typically carries one dominant fungus clone (56). Other clades with oral mycangia, such as Premnobius and Ambrosiodmus, are even more specific, as each individual tends to contain a virtually pure culture of a single symbiont (4, 71). Although processes in beetle mycangia seem to determine species-level specificity, the broader ecology of the association is determined by the symbiotic fungus. Raffaelea is typically associated with beetles that occupy larger and moister parts of the tree, which may reflect the ecology of the ancestral Ophiostomatales (89). In contrast, Ambrosiella s. str. (Microascales) seems to be predominantly associated with beetles that bore into smaller and drier material, such as branches (75). The three most common genera of ambrosia fungi, Raffaelea, Ambrosiella,and

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org Fusarium, belong to families of phytopathogens. This probably explains why ancestors of these fungi were recruited from moribund tree tissues by bark-dwelling ancestors of ambrosia beetles, but it also explains their nutritional niche. Like their pathogenic ancestors, most modern ambrosia

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. fungi do not degrade wood but instead rapidly assimilate nutrients that remain in the dying tree tissues. A completely different ecology is represented by Flavodon ambrosius, the only known ambrosial fungus that actually digests cellulose within wood. Flavodon belongs to Polyporales, efﬁcient white-rot basidiomycetes. Its capacity to convert rotten wood into animal nutrition over a long period of time allowed its ambrosia beetle vectors to spend multiple generations within a single tree (57). Human trade and travel have homogenized beetle-fungus biogeography, but associations between the beetles and the fungi appear to remain unchanged even in newly invaded lands. Highly speciﬁc beetles retain the same symbiont wherever they are sampled [Ambrosiodmus (71), Premno- bius (4), Xylosandrus (40)]. Beetle clades that associate with several fungi from the same genus retain

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the same mix of congeners [Euwallacea (81)]. And finally, promiscuous ambrosia beetles remain so in both native and invaded regions. Although they may retain one dominant fungus, they also absorb newly encountered species [Xyleborus spp. and Raffaelea spp.: (20)]. It is likely that part of the apparent promiscuity of invasive Xyleborus spp. is due to their association with Raffaelea,many species of which are already available in most newly invaded regions, such as North America. Other ambrosia fungus genera are rare or absent in the United States, so beetles carrying these have no other fungi to add to their mycangia and exhibit promiscuity. Ambrosia beetles are routinely accompanied by many fungi other than the coevolved mutualists, sometimes dozens of species (65, 73). Many of these fungi are well adapted for transport on the insect and sporulate profusely, easily confusing both culturing and culture-independent studies. Simple counts of colony abundance or DNA reads are typically insufficient for disentangling the commensals from the mutualists (78). Therefore, detailed examination of where the fungi occur, and how frequently, is required (4). In terms of biomass, the coevolved symbiont typically thwarts other fungi during the active stage of gallery development but is often outcompeted in later stages (14, 61). There are also nonfungal organisms in the galleries, including mites, nematodes, and the ubiquitous bacteria. Some of the bacteria display biological activity toward fungi and beetles on agar plates (36); however, most have a nonspecific pattern of occurrence typical of transient organisms from the environment (2, 45) or belong to parasitic taxa (51).

Beetle-Fungus Interactions One of the most important but also the least investigated aspects of this symbiosis is the mechanism of mutual recognition. Chemical signaling between the partners is likely to occur, especially within the mycangium, which facilitates the growth of the mutualist and the elimination of nonmutual- ists (31). Each independently evolved clade of ambrosia beetles has evolved its own mycangium (Table 1), which has been a source of fascination since the beginning of the ambrosia symbiosis research (42). Mycangia are often considered relatively static, but some of the most complex types have flexible ontogenesis. In Anisandrus, Xylosandrus, and possibly most members of the same clade, the mesonotal mycangium is absent in callow adults, but it expands dramatically and becomes filled with fungus during migration (70). The interactions between the symbionts in the gallery also require more investigation. The fungal aerial mycelium (the garden) is most apparent just before and during larval development. Grazing seems to increase its vigor (15, 42), and the garden is said to die and overgrow with nonsymbiotic fungi in the absence of the beetle (6). However, the visible garden is only a minute portion of the fungal biomass. Most of the fungal mycelium occurs within the wood, but it has not been investigated. Raffaelea lauricola persists in inoculated tree tissues for weeks even without Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org the presence of beetles, far away from the entry point (52). Volatiles from ambrosia fungi attract their beetle vectors (49, 67). Whether this short-range attraction is adaptive remains unclear, but fungal odors do have significant value as olfactory cues. Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. For example, the fungus-stealing mycocleptae (see below) are able to locate established ambrosia gardens in the forest (47).

Farming Societies There are two essential differences between the phloem-eating bark beetles and the fungus- farming ambrosia beetles. First, fungus farming provides more nutrition faster and allows for the colonization of much broader host diversity. Therefore, wherever fungus farming is possible (mostly in regions with higher humidity), ambrosia beetles tend to be more abundant than bark beetles, which depend on ﬁnding the optimal tissue of the correct host species (7, 50). Similarly,

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among humans, farming societies eventually prevailed over hunter-gatherers except where farming was difficult (23). Another intriguing difference is that the evolution of fungus farming in beetles also seems to have triggered the expansion of complexity in social structure. The entire family often co-occurs within the same tunnel, leading to overlap of multiple developmental stages as well as a rich array of interactions, including allogrooming, cooperation in gallery maintenance, and disposal of de- bris (15). In several instances, this spatial arrangement is combined with an important innovation, long-term persistence of the fungus garden, which has enabled the evolution of even greater degrees of sociality. The most social of ambrosia beetles—the eusocial Austroplatypus, the subsocial Ambrosiophilus, and several species of Xyleborus and Xyleborinus—all display a higher degree of sociality due to long-term stability of the garden, though they all significantly differ biologically. In Austroplatypus, the fungus identity has not been reported, but the beetle-fungus complex contin- ually expands the gallery system in living eucalyptus host trees without killing them, maintaining a stable environment for decades (59). In Ambrosiophilus and the related Ambrosiodmus, stability is achieved through association with an aggressive wood-rot fungal mutualist, which is capable of outcompeting free-living fungi and also allows the development of interconnected multifamily colonies, sometimes containing thousands of individuals (27, 57). In Xyleborus and Xyleborinus, subsociality is not the default strategy but does occur frequently in large dead tree trunks, where the symbiotic Raffaelea spp. can persist long enough to support multiple life cycles. This allows young females to defer dispersal and instead lay eggs in their native gallery (15). In summary, the ecology of the fungal mutualist has a direct effect on the degree of complexity of the beetle society. Fungus farming facilitates not only intraspecific sociality but also between-species interactions that are absent in nonfarming bark beetles. One such interaction is fungus stealing or sharing, described as mycocleptism (47). Multiple ambrosia beetle species have evolved the capacity to find galleries freshly established by other ambrosia beetle species and create their galleries just a few millimeters apart. This allows the already established fungus to also grow into the new tunnel.

Fungus-Dependent Bark Beetles All ambrosia beetle groups in the subfamily Scolytinae evolved from bark beetle ancestors. Like- wise, members of Platypodinae, of which all but a few basal taxa are ambrosia beetle species, appear to have originated from phloem-feeding weevils (53). The bark beetles include over 3,000 species, and many species depend on fungal nutritional mutualists [phloeomycetophagy (91)]. Therefore, the difference between bark and ambrosia beetles is not a sharp boundary but rather a continuum

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org in the degrees of mycophagy. Many of the fungus-feeding bark beetles are of great economic signiﬁcance and as such have been well researched, particularly within the genus Dendroctonus (92). This research focus resulted

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. in the somewhat surprising fact that the relationships between the phloeomycetophagous bark beetles and their fungi are much better known than between the mycetophagous ambrosia beetles and their fungi. Within the bark beetle–fungus literature, an important pattern in beetle-fungus coevolution emerges: It is the fungus that determines the degree of mutual speciﬁcity. The fungus is also evolutionarily more speciﬁc to the tree hosts than to the beetles. One extensively investigated phloeomycetophagous association includes the basidiomycete Entomocorticium and bark beetles in North America. Entomocorticium is a monophyletic genus with several species that are all specialized on decaying phloem of conifers, primarily Pinaceae. There are at least three different beetle groups that evolved associations with this fungal genus: several species of Dendroctonus (Scolytinae: Hylurgini), Pityoborus comatus (Scolytinae: Corthylini), and Ips avulsus (Scolytinae:

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Ipini) (33, 37, 103). In other words, it appears that Entomocorticium has become associated with multiple beetle vectors among those sharing the same decaying-phloem niche. The key may be just a few adaptations, such as the capacity to produce fruiting bodies in the pupal chambers and the ability to proliferate and dominate over other fungal species within beetle mycangia.

AMBROSIA BEETLE PESTS Two questions have puzzled ambrosia beetle researchers significantly: Why are these saprophytic beetles and fungi turning into tree killers in invaded regions? And, which of their features have changed, or contributed to, the new pest status? To assume that ambrosia beetles and fungi are becoming pests is not entirely correct; in reality, only between five and ten species are serious pests of important tree species (48). A few other species are minor cosmetic pests, and the vast majority of ambrosia beetle species remain harmless forest dwellers with minimal effect on human industries. There are, however, ambrosia beetles and fungi that do kill trees. How do they do it, and why does it seem to be a new phenomenon? Most of the tree-killing ambrosia beetles share one feature: the capacity to colonize living tree tissues. That does not mean that they have always been pests, nor that they use tree killing as their principal ecological strategy. Most of these species are opportunistic in their native habitats. They typically live in dead trees, but in addition, they are also capable of colonizing trees that are stressed or weakened (55, 69, 85). Consequently, their fungi are adapted to colonizing compromised but still living tissues more effectively than do symbionts of beetles that can colonize only dead trees. These features can manifest themselves as pestilence in trees that are out of their metabolic optima, for example, in plantations or cities. Ambrosia beetle and fungal species that are ecologically restricted to dead trees remain harmless even after establishment in nonnative regions, and the pest species are not necessarily pestiferous in all circumstances. It is thus important to recognize that ambrosia beetle pests are not a homogeneous group. Here, we define the three known distinct modes of ambrosia beetle damage.

Mode 1: Association with a Virulent Tree Pathogen The most feared mode of tree killing among ambrosia beetles is through the inoculation of a virulent fungus partner. Paradoxically, there is really only a single case of this mode, albeit a catastrophic one: laurel wilt. Laurel wilt is a deadly disease of New World Lauraceae caused by Raffaelea lauricola and its vector Xyleborus glabratus. This one symbioclone, progeny of the introduction of a single beetle and a single fungus genotype, has killed over a half-billion trees in

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org just a decade after its introduction into North America (43). The most economically important impact has been on avocado in south Florida, where thousands of cultivated trees have been killed. Several reviews have summarized the disease ecology and management recommendations (44,

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. 58), and we refrain from repeating this information. Instead, we present an interpretation of this unique disease in the context of general ambrosia symbiosis ecology. The X. glabratus and R. lauricola mutualism is the most intensely studied ambrosia system, yet it continues to yield discoveries that demonstrate the unusual nature of this particular symbiosis. For example, the vector beetles search for live host trees by following speciﬁc sesquiterpenes, which is not known to occur in other ambrosia beetles (58). The fungus-tree interaction is also unusual, as it appears that the tree death is partly due to excessive and suicidal formation of tyloses—swellings of veins that normally block pathogens (19). Laurel wilt is a threat to Lauraceae throughout the New World and to the sustainability of avocado production, in part because of its complex epidemiology. There are many avenues for dispersal

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and the persistence of both the vector and the pathogen through the landscape. Raffaelea lauricola is a promiscuous fungal symbiont that can colonize many different ambrosia beetles (20) and readily travel through root grafts (52). The beetle populations are relatively cold tolerant despite their tropical origin (28) and are frequently spread through anthropogenic wood transport. The beetles persist in the landscape long after the main epidemic has killed all typical hosts (18, 74). Whether they persist on suboptimal hosts or the host spectrum is broader than Lauraceae is unknown. Measures to control the disease in avocado groves or among high-value individual trees include aggressive sanitation of attacked trees (95) and prophylactic injection of fungicides directly into the trunk. There are few landscape-level management options available for the epidemics in natural habitats. The most promising is breeding for resistance, which naturally occurs in a few percent of redbays (43).

Mode 2: Mass Accumulation on Stressed Trees The most common mode of ambrosia beetle tree killing is linked to beetle attraction to semio- chemical cues from trees in distress. Many invasive species in the United States, such as multiple Xylosandrus and Euwallacea species, are exquisitely sensitive to stress-related volatiles, primarily ethanol (82) or quercivorol (21). Some of these beetles often congregate on trees affected by late frost, waterlogged soil, or an internal pathogen. Such attacks are chronic in intensely managed nurseries and fruit orchards. These ambrosia beetles are both the cause and the symptom of death. Their attacks are a symptom of physical stress to trees that may be unapparent to the grower. Poor drainage, graft incompatibility, unsuitability for a particular growing zone, poor soil or site conditions, or excessive or improperly timed nutrients and irrigation cause cryptic stress to trees (82). Under traditional circumstances, most trees would be sufﬁciently resilient to recover. However, as aggressive ambrosia beetles are now present throughout the landscape, such conditions trigger fatal attacks. That the invasive species within Xylosandrus and Euwallacea preferentially attack trees in non- natural, stressful settings, such as urban environments and orchards (25, 69, 77), is true in both the invaded and the native regions. For example, the tea shot hole borer (E. fornicatus s. str.) also causes losses in tea plantations in its native Asia (41), but there are no reports of damage from nonagricultural habitats. Damage to living trees that have been preinfected by a pathogen has been well documented for E. validus and E. interjectus (55, 56). Ambrosia beetles that use pheromones, including those of Platypodinae and Corthylini, can synchronize their arrival and accumulation on trees when their population densities are large, causing outbreaks similar to those of tree-killing bark beetles (26, 68, 90). However, we distinguish

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org mass accumulation from mass attack. The latter occurs in bark beetles that specialize in attacking healthy conifers by a rapid and synchronized attack (98). In ambrosia beetles, in contrast, the accumulation process can last for months and only a fraction of the participating individuals

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. colonize living host tissue. Most beetles arrive at tissues that are already weakened or dead and colonized by the ambrosia fungus. Plant pathologists have long understood the tripartite balance among a pathogen, the host, and the host well-being as the so-called disease triangle. In ambrosia beetle research, the role of the environment and preexisting conditions of the trees has not yet been well appreciated, even though it appears to determine the impact of these beetles. No other description of this phenomenon is more eloquent than that by the father of biogeography, A.R. Wallace (101, p. 219):

I am led, therefore, to conclude that the Scolyti, &c. attack wood in which the vital forces have ceased to act; and they are able to detect this before any external change has taken place. It is only at a later

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period that we observe the tree to be suffering, and in the parts most affected we discover the Scolyti to have been at work, and erroneously impute the mischief to them.

The invasions of several aggressive species of Xylosandrus and Euwallacea throughout the temperate zones present a new management challenge for tree nurseries. The only practical management option is prevention of infestation as infested trees or branches are typically not recoverable. The two greatest predictors of ambrosia beetle damage in nurseries and urban trees are ﬂooding (including excessive irrigation) and late frost. Both of these triggers can be forecasted, and management can be proactive (84). Trunks of small trees can be protected mechanically or by surface spray (30). The second component of proactive management is sanitation. Brush piles surrounding the nurseries are ideal breeding areas for ambrosia beetles and need to be minimized. At the same time, such brush and cut branches attacked by beetles can also function as traps in that their timely burning or chipping removes a substantial proportion of the beetle population (95). Monitoring is an essential part of the control of nursery pests. Here, the attraction of most ambrosia beetle pests to ethanol is an advantage. Beetle activity can be monitored using ethanol-based commercial lures (83), homemade lures (96), or sentinel trees with ethanol infusion (82).

Mode 3: Structural Damage A historically well-known mode of ambrosia beetle damage is colonization and staining of freshly sawn timber. In warm and humid regions where ambrosia beetles are abundant, freshly cut timber can be immediately colonized by large numbers of ambrosia beetles and fungi (17). In northern latitudes, temperate genera such as Trypodendron and Gnathotrichus have caused the degradation of millions of dollars of sawn timber annually, rivaling the losses due to tree-killing bark beetles (72). In the southern portions of North America, swarms of ambrosia beetles are a new phenomenon associated with invasive tropical beetles (particularly Xylosandrus crassiusculus) and occasionally force managers of timber lots to adjust their methods of stock management.

OUTLOOK The ambrosia symbiosis has evolved at least 15 times among bark beetles and an unknown number of times among fungi. Many of these associations include unique taxa, degrees of speciﬁcity or promiscuity, host ranges, mycangia, and other features, suggesting that many of these independently evolved associations employ different regulatory mechanisms. There is not one but many ambrosia symbioses. There are as many different strategies and patterns as there are origins of ambrosia beetles and fungi. We believe that the most exciting discoveries regarding the ambrosia Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org symbiosis are yet to come.

New Methods Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. There is a need to reconcile the currently used methods for assessment of fungal communities. Culturing and culture-independent approaches often arrive at vastly different conclusions about which fungi colonize the mycangium or the gallery. The metric by which the presence and abundance of fungi should be measured is unclear. The traditional count of fungus colonies on a culture dish likely overemphasizes richly sporulating commensals or parasites (73), particularly where the mutualistic fungi are fastidious. Similarly, counting of reads in an amplicon sequencing output is fraught with biases in polymerase chain reaction (PCR) and in copy number of the template sequences within cells (12). Future assessments of the fungal communities would beneﬁt from combining culturing and sequencing techniques, using appropriate positive controls and mock

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communities, and using more quantitative molecular assessment methods such as quantitative PCR or ampliﬁcation-free metagenomics.

Mechanism of Interactions What mechanism assures that the primary ambrosial mutualist ends up being the dominant fungus within the mycangium? Many different fungi enter the mycangium in a young adult beetle, but only the most coevolved mutualists thrive there (31). This is the pivotal moment of the entire symbiosis, yet it has never been addressed with a satisfactory conclusion. Do the beetles use selective antibiotics or do they create a speciﬁc nutritional environment that enables the coevolved symbiont to dominate? Is it a physiological interaction relying on signaling between the partners, or an ecological process where stochastic community assembly plays a greater role (6)? Bacteria may be involved, but the data are ambiguous (51). Is it perhaps something completely unexpected? These questions are difﬁcult to answer by inference from natural settings; therefore, it is time for studies of the ambrosia symbiosis to use manipulative experiments.

Predicting Future Pests Why are some species or populations of ambrosia beetles destructive and others harmless, despite being closely related? Understanding the mechanism of ambrosia beetle damage is important as it allows us to predict which species may eventually become invasive and pestiferous in the future. The tropical forest entomology literature contains records of species observed to colonize living trees, and those species should be targeted for research and monitoring. For example, in South America, Gnathotrupes ﬁmbriatus and several other species bore into living branches of southern beech and occasionally cause tree death (97). These species and their fungi should be investigated for their potential effects on Fagaceae in other parts of the world. Similarly, Euwallacea destruens has been reported to cause signiﬁcant mortality in plantations of various trees within its native range in Asia and may be capable of damage similar to or greater than its infamous congener, Euwallacea fornicatus (17).

Conclusion The rise in damage by ambrosia beetles and fungi is a testimony to the continuing homogenization of the Earth’s biota by humans. Many insect and fungus communities around the world are losing their uniqueness; for example, the ambrosia beetle fauna in the southern United States is now Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org similar to that in southern Japan. The invasions are not stopping: The authors received two new reports of ambrosia beetle damage even as this review was being written. Rather than only raising alarm, however, the intent of this review is to emphasize the opportunities that arise from our Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. growing knowledge of the beetle-fungus mutualism. Few other organisms provide the combination of a dynamic symbiosis, diversity of genetic and reproductive systems, and common presence in most people’s environments, accessible even to children (96). A system that is so rich and at the same time so easy to study may become the future model for the science of symbioses.

DISCLOSURE STATEMENT The authors are not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

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ACKNOWLEDGMENTS J.H. was funded by the US Department of Agriculture (USDA) Forest Service (FS) Coop agree- ments 14-CA-11330130-032 and 12-CA-11420004-042, USDA-APHIS Farm Bill Section 10007 agreement 14-8130-0377-CA, and the National Science Foundation DEB 1256968 and 1556283. L.L.S. was funded by USDA-NIFA grant 2015 · 51181-24257. The material may not necessarily express USDA-APHIS views.

LITERATURE CITED 1. Alamouti S, Tsui C, Breuil C. 2009. Multigene phylogeny of filamentous ambrosia fungi associated with ambrosia and bark beetles. Mycol. Res. 113:822–35 2. Aylward FO, Suen G, Biedermann PHW, Adams AS, Scott JJ, et al. 2014. Convergent bacterial micro- biotas in the fungal agricultural systems of insects. mBio 5:10 3. Baker J, Norris D. 1968. A complex of fungi mutualistically involved in the nutrition of the ambrosia beetle Xyleborus ferrugineus. J. Invertebr. Pathol. 11:246–50 4. Bateman CC, Huang Y-T, Simmons D, Kasson MT, Stanley EL, Hulcr J. 2016. Ambrosia beetle Prem- nobius cavipennis (Scolytinae: Ipini) carries highly divergent ascomycotan ambrosia fungus, Afroraffaelea ambrosiae gen. nov. sp. nov. (Ophiostomatales). Fungal Ecol.Inpress 5. Batra LR. 1963. Ecology of ambrosia fungi and their dissemination by beetles. Trans. Kans. Acad. Sci. 66:213–36 6. Batra LR. 1966. Ambrosia fungi: extent of specificity to ambrosia beetles. Science 153:193–95 7. Beaver RA. 1979. Host specificity of temperate and tropical animals. Nature 281:138–41 8. Beaver RA. 1984. The biology of the ambrosia beetle, Sueus niisimai (Eggers) (Col., Scolytidae), in Fiji. Entomol. Mon. Mag. 120:99–102 9. Beaver RA. 1986. The taxonomy, mycangia and biology of Hypothenemus curtipennis (Schedl), the first known cryphaline ambrosia beetle (Coleoptera, Scolytidae). Entomol. Scand. 17:131–35 10. Beaver RA, Gebhardt H. 2006. A review of the Oriental species of Scolytoplatypus Schaufuss (Coleoptera, Curculionidae, Scolytinae). Dtsch. Entomol. Z. 53:155–78 11. Belhoucine L, Bouhraoua R, Meijer M, Houbraken J, Harrak M, et al. 2011. Mycobiota associated with Platypus cylindrus (Coleoptera: Curculionidae, Platypodidae) in cork oak stands of North West Algeria, Africa. Afr. J. Microbiol. Res. 5:4411–23 12. Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H. 2010. ITS as an envi- ronmental DNA barcode for fungi: An in silico approach reveals potential PCR biases. BMC Microbiol. 10:189 13. Berkov A, Feinstein J, Small J, Nkamany M. 2007. Yeasts isolated from neotropical wood-boring beetles in SE Peru. Biotropica 39:530–38 14. Biedermann PH, Klepzig KD, Taborsky M, Six DL. 2013. Abundance and dynamics of filamentous

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org fungi in the complex ambrosia gardens of the primitively eusocial beetle Xyleborinus saxesenii Ratzeburg (Coleoptera: Curculionidae, Scolytinae). FEMS Microbiol. Ecol. 83:711–23 15. Biedermann PH, Taborsky M. 2011. Larval helpers and age polyethism in ambrosia beetles. PNAS 108:17064–69 Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. 16. Bracewell R, Six D. 2014. Broadscale speciﬁcity in a bark beetle–fungal symbiosis: a spatio-temporal analysis of the mycangial fungi of the western pine beetle. Microb. Ecol. 68:859–70 17. Browne FG. 1961. The Biology of Malayan Scolytidae and Platypodidae. Malay. Forest Rec. Ser. 22. Malaya: Gov. Press 18. Cameron R, Hanula J, Fraedrich S, Bates C. 2015. Progression and impact of laurel wilt disease within redbay and sassafras populations in southeast Georgia. Southeast. Nat. 14:650–74 19. Campbell A. 2014. Characterizing pathogen-vector-host interactions in laurel wilt, a disease of avocado.PhD Thesis, Univ. Florida, Gainesville 20. Carrillo D, Duncan R, Ploetz J, Campbell A, Ploetz R, Pena J. 2014. Lateral transfer of a phytopathogenic symbiont among native and exotic ambrosia beetles. Plant Pathol. 63:54–62

www.annualreviews.org • The Ambrosia Symbiosis 299 EN62CH16-Hulcr ARI 19 December 2016 12:15

21. Carrillo D, Narvaez T, Cosse A, Stouthamer R, Cooperband M. 2015. Attraction of Euwallacea nr. fornicatus (Coleoptera: Curculionidae: Scolytinae) to lures containing quercivorol. Fla. Entomol. 98:780– 82 22. Davis T. 2015. The ecology of yeasts in the bark beetle holobiont: a century of research revisited. Microb. Ecol. 69:723–32 23. Diamond J. 2002. Evolution, consequences and future of plant and animal domestication. Nature 418:700–7 24. Dreaden T, Davis J, de Beer Z, Ploetz R, Soltis P, et al. 2014. Phylogeny of ambrosia beetle symbionts in the genus Raffaelea. Fungal Biol. 118:970–78 25. Eskalen A, Stouthamer R, Lynch S, Rugman-Jones P, Twizeyimana M, et al. 2013. Host range of Fusarium dieback and its ambrosia beetle (Coleoptera: Scolytinae) vector in southern California. Plant Dis. 97:938–51 26. FAO (Food Agric. Organ.), CONAF (Corp. Nac. For.). 2008. Manual de Plagas y Enfermedades del Bosque Nativo en Chile. Asistencia para la Recuperación y Revitalización de los Bosques Templados de Chile, con Enfasis´ en los Nothofagus Caducifolios. FAO RLC (Reg. Off. Lat. Am. Caribb.), Santiago, Chile 27. Faccoli M, Frigimelica G, Mori N, Toffolo E, Vettorazzo M, Simonato M. 2009. First record of Am- brosiodmus (Hopkins, 1915) (Coleoptera: Curculionidae, Scolytinae) in Europe. Zootaxa 2303:57–60 28. Formby J, Krishnan N, Riggins J. 2013. Supercooling in the redbay ambrosia beetle (Coleoptera: Cur- culionidae). Fla. Entomol. 96:1530–40 29. Francke-Grosmann H. 1967. Ectosymbiosis in wood-inhabiting insects. Symbiosis 2:141–205 30. Frank S, Sadof C. 2011. Reducing insecticide volume and nontarget effects of ambrosia beetle management in nurseries. J. Econ. Entomol. 104:1960–68 31. Freeman S, Sharon M, Dori-Bachash M, Maymon M, Belausov E, et al. 2015. Symbiotic association of three fungal species throughout the life cycle of the ambrosia beetle Euwallacea nr. fornicatus. Symbiosis 68:115–28 32. Funk A. 1970. Fungal symbionts of the ambrosia beetle Gnathotrichus sulcatus. Can. J. Bot. 48:1445–48 33. Furniss MM, Woo JY, Deyrup MA, Atkinson TH. 1987. Prothoracic mycangium on pine-infesting Pityoborus spp. (Coleoptera: Scolytidae). Ann. Entomol. Soc. Am. 80:692–96 34. Ganter PF. 2006. Yeast and invertebrate associations. In Biodiversity and Ecophysiology of Yeasts,ed.G Peter,´ CA Rosa, pp. 303–70. Berlin: Springer 35. Gebhardt H, Weiss M, Oberwinkler F. 2005. Dryadomyces amasae: a nutritional fungus associated with ambrosia beetles of the genus Amasa (Coleoptera: Curculionidae, Scolytinae). Mycol. Res. 109:687–96 36. Grubbs K, Biedermann P, Suen G, Adams S, Moeller J, et al. 2011. Genome sequence of Streptomyces griseus strain XylebKG-1, an ambrosia beetle-associated actinomycete. J. Bacteriol. 193:2890–91 37. Harrington TC. 2005. Ecology and evolution of mycophagous bark beetles and their fungal partners. In Insect-Fungal Associations: Ecology and Evolution, ed. FE Vega, M Blackwell, pp. 257–92. New York: Oxford Univ. Press 38. Harrington TC, Aghayeva D, Fraedrich S. 2010. New combinations in Raffaelea, Ambrosiella,and Hyalorhinocladiella, and four new species from the redbay ambrosia beetle, Xyleborus glabratus. Mycotaxon Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org 111:337–61 39. Harrington TC, Fraedrich S. 2010. Quantification of propagules of the laurel wilt fungus and other mycangial fungi from the redbay ambrosia beetle, Xyleborus glabratus. Phytopathology 100:1118–23

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. 40. Harrington TC, McNew D, Mayers C, Fraedrich S, Reed S. 2014. Ambrosiella roeperi sp. nov. is the mycangial symbiont of the granulate ambrosia beetle, Xylosandrus crassiusculus. Mycologia 106:835–45 41. Hazarika LK, Bhuyan M, Hazarika BN. 2009. Insect pests of tea and their management. Annu. Rev. Entomol. 54:267–84 42. Hubbard HG. 1897. The ambrosia beetles of the United States. USDA Div. Entomol. Bull. (New Ser.) 7:9–30 43. Hughes MA. 2013. The evaluation of natural resistance to laurel wilt disease in redbay (Persea borbonia). PhD Thesis, Univ. Florida, Gainesville 44. Hughes MA, Smith J, Ploetz R, Kendra P, Mayﬁeld AIII, et al. 2015. Recovery plan for laurel wilt on redbay and other forest species caused by Raffaelea lauricola and disseminated by Xyleborus glabratus. Plant Health Prog. 16:174–210

300 Hulcr · Stelinski EN62CH16-Hulcr ARI 19 December 2016 12:15

45. Hulcr J, Adams AS, Raffa K, Hofstetter RW, Klepzig KD, Currie CR. 2010. Presence and diversity of Streptomyces in Dendroctonus and sympatric bark beetle galleries across North America. Microb. Ecol. 61:759–68 46. Hulcr J, Atkinson T, Cognato A, Jordal B, McKenna D. 2015. Morphology, taxonomy and phylogenetics of bark beetles. See Reference 100, pp. 41–84 47. Hulcr J, Cognato A. 2010. Repeated evolution of crop theft in fungus-farming ambrosia beetles. Evolution 64:3205–12 48. Hulcr J, Dunn R. 2011. The sudden emergence of pathogenicity in insect-fungus symbioses threatens naive forest ecosystems. Proc. R. Soc. B 278:2866–73 49. Hulcr J, Mann R, Stelinski LL. 2011. The scent of a partner: ambrosia beetles are attracted to volatiles from their fungal symbionts. J. Chem. Ecol. 37:1374–77 50. Hulcr J, Mogia M, Isua B, Novotny V. 2007. Host specificity of ambrosia and bark beetles (Col., Cur- culionidae: Scolytinae and Platypodinae) in a New Guinea rainforest. Ecol. Entomol. 32:762–72 51. Hulcr J, Rountree N, Diamond S, Stelinski L, Fierer N, Dunn RR. 2012. Mycangia of ambrosia beetles host communities of bacteria. Microb. Ecol. 64:784–93 52. Inch S, Ploetz R, Held B, Blanchette R. 2012. Histological and anatomical responses in avocado, Persea americana, induced by the vascular wilt pathogen, Raffaelea lauricola. Botany 90:627–35 53. Jordal B. 2015. Molecular phylogeny and biogeography of the weevil subfamily Platypodinae reveals evolutionarily conserved range patterns. Mol. Phylogenet. Evol. 92:294–307 54. Jordal B, Cognato A. 2012. Molecular phylogeny of bark and ambrosia beetles reveals multiple origins of fungus farming during periods of global warming. BMC Evol. Biol. 12:133 55. Kajii C, Morita T, Jikumaru S, Kajimura H, Yamaoka Y, Kuroda K. 2013. Xylem dysfunction in Ficus carica infected with wilt fungus Ceratocystis ficicola and the role of the vector beetle Euwallacea interjectus. IAWA J. 34:301–12 56. Kasson M, O’Donnell K, Rooney A, Sink S, Ploetz R, et al. 2013. An inordinate fondness for Fusarium: phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts. Fungal Genet. Biol. 56:147–57 57. Kasson M, Wickert K, Stauder C, Macias A, Berger M, et al. 2016. Mutualism with aggressive wood- degrading Flavodon ambrosius (Polyporales) facilitates niche expansion and communal social structure in Ambrosiophilus ambrosia beetles. Fungal Ecol. 23:86–96 58. Kendra P, Montgomery W, Niogret J, Pruett G, Mayfield A, et al. 2014. North American Lauraceae: terpenoid emissions, relative attraction and boring preferences of redbay ambrosia beetle, Xyleborus glabratus (Coleoptera: Curculionidae: Scolytinae). PLOS ONE 9:e102086 59. Kent D, Simpson J. 1992. Eusociality in the beetle Austroplatypus incompertus (Coleoptera, Curculionidae). Naturwissenschaften 79:86–87 60. Kim K, Choi Y, Seo S, Shin H. 2009. Raffaelea quercus-mongolicae sp. nov. associated with Platypus koryoensis on oak in Korea. Mycotaxon 110:189–97 61. Kinuura H. 1995. Symbiotic fungi associated with ambrosia beetles. Jpn. Agric. Res. Q. 29:57–63

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org 62. Kirkendall LR, Biedermann PH, Jordal BH. 2015. Evolution and diversity of bark and ambrosia beetles. See Reference 100, pp. 85–156 63. Kolarik M, Hulcr J. 2009. Mycobiota associated with the ambrosia beetle Scolytodes unipunctatus (Coleoptera: Curculionidae, Scolytinae). Mycol. Res. 113:44–60 Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. 64. Kolarik M, Kirkendall L. 2010. Evidence for a new lineage of primary ambrosia fungi in Geosmithia Pitt (Ascomycota: Hypocreales). Fungal Biol. 114:676–89 65. Kostovcik M, Bateman C, Kolarik M, Stelinski L, Jordal B, Hulcr J. 2015. The ambrosia symbiosis is speciﬁc in some species and promiscuous in others: evidence from community pyrosequencing. ISME J. 9:126–38 66. Kubono T, Ito S. 2002. Raffaelea quercivora sp. nov. associated with mass mortality of Japanese oak, and the ambrosia beetle (Platypus quercivorus). Mycoscience 43:255–60 67. Kuhns EH, Tribuiani Y, Martini X, Meyer WL, Pena˜ J, et al. 2014. Volatiles from the symbiotic fungus Raffaelea lauricola are synergistic with manuka lures for increased capture of the redbay ambrosia beetle Xyleborus glabratus. Agric. Forest Entomol. 16:87–94

www.annualreviews.org • The Ambrosia Symbiosis 301 EN62CH16-Hulcr ARI 19 December 2016 12:15

68. La Spina S, De Canniere` C, Dekri A, Gregoire´ J. 2013. Frost increases beech susceptibility to scolytine ambrosia beetles. Agric. Forest Entomol. 15:157–67 69. Li Q, Zhang G, Guo H, He L, Liu B. 2014. Euwallacea fornicatus, an important pest insect attacking Acer buergerianum. Forest Pest Dis. 33:25–27 70. Francke-Grosmann H. 1956. Hautdrusen¨ als trager¨ der pilzsymbiose bei ambrosiakafern.¨ Z. Morphol. Okol¨ Tiere. 45:275–308 71. Li Y, Simmons DR, Bateman CC, Short DPG, Kasson MT, et al. 2015. New fungus-insect symbiosis: culturing, molecular, and histological methods determine saprophytic Polyporales mutualists of Ambro- siodmus ambrosia beetles. PLOS ONE 10:e0137689 72. Lindgren B, Fraser R. 1994. Control of ambrosia beetle damage by mass trapping at a dryland log sorting area in British Columbia. For. Chron. 70:159–63 73. Lynch SC, Twizeyimana M, Mayorquin JS, Wang DH, Na F, et al. 2016. Identiﬁcation, pathogenicity and abundance of Paracremonium pembeum sp.nov.andGraphium euwallaceae sp. nov.—two newly dis- covered mycangial associates of the polyphagous shot hole borer (Euwallacea sp.) in California. Mycologia 108:313–29 74. Maner M, Hanula J, Horn S. 2014. Population trends of the redbay ambrosia beetle (Coleoptera: Cur- culionidae: Scolytinae): Does utilization of small diameter redbay allow populations to persist? Fla. Entomol. 97:208–16 75. Mayers CG, McNew DL, Harrington TC, Roeper RA, Fraedrich SW, et al. 2015. Three genera in the Ceratocystidaceae are the respective symbionts of three independent lineages of ambrosia beetles with large, complex mycangia. Fungal Biol. 119:1075–92 76. MacLean DB, Giese RL. 1967. The life history of the ambrosia beetle Xyloterinus politus (Coleoptera: Scolytidae). Can. Entomol. 99:285–99 77. Mendel Z, Protasov A, Sharon M, Zveibil A, Ben Yehuda S, et al. 2012. An Asian ambrosia beetle Euwallacea fornicatus and its novel symbiotic fungus Fusarium sp. pose a serious threat to the Israeli avocado industry. Phytoparasitica 40:235–38 78. Miller KE, Hopkins K, Inward DJG, Vogler AP. 2016. Metabarcoding of fungal communities associated with bark beetles. Ecol. Evol. 6:1590–1600 79. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR. 2005. The evolution of agriculture in insects. Annu. Rev. Ecol. Evol. Syst. 36:563–95 80. Nakashima T. 1989. Observation on the ambrosia fungus, Ambrosiella sp., growing in the gallery of Scolytoplatypus shogun Blandford (Coleoptera, Scolytidae) and on the concurrent damage of wood tissue. J. Fac. Agric. Hokkaido Univ. 64:99–105 81. O’Donnell K, Sink S, Libeskind-Hadas R, Hulcr J, Kasson MT, et al. 2015. Discordant phylogenies suggest repeated host shifts in the Fusarium-Euwallacea ambrosia beetle mutualism. Fungal Genet. Biol. 82:277–90 82. Ranger C, Reding M, Schultz P, Oliver J, Frank S, et al. 2016. Biology, ecology, and management of nonnative ambrosia beetles (Coleoptera: Curculionidae: Scolytinae) in ornamental plant nurseries.

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org J. Integr. Pest Manag. 7:9 83. Reding M, Oliver J, Schultz P, Ranger C. 2010. Monitoring flight activity of ambrosia beetles in ornamental nurseries with ethanol-baited traps: influence of trap height on captures. J. Environ. Hortic. 28:85 Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. 84. Reding M, Ranger C, Oliver J, Schultz P. 2013. Monitoring attack and flight activity of Xylosandrus spp. (Coleoptera: Curculionidae: Scolytinae): the influence of temperature on activity. J. Econ. Entomol. 106:1780–87 85. Saito K. 1959. Outbreak of Crossotarus quercivorus. For. Pests 87:101–2 86. Schedl K. 1959. Scolytidae und Platypodidae Afrikas. Band 1. Familie Scolytidae. Rev. Entomol. Mo¸cam. 2:357–422 87. Schedl W. 1962. Ein Beitrag zur Kenntnis der Pilzübertragungsweise bei xylomycetophagen Scolytiden (Coleoptera). Vienna: Springer-Verlag 88. Schmidberger J. 1836. Naturgeschichte des Apfelborkenkafers¨ Apate dispar. Beitr. Obstbaumzucht Naturgeschichte Obstbäumen schädlichen Insekten 4:213–30

302 Hulcr · Stelinski EN62CH16-Hulcr ARI 19 December 2016 12:15

89. Seifert KA, de Beer ZW, Wingﬁeld MJ. 2013. The Ophiostomatoid Fungi: Expanding Frontiers.CBS- KNAW Fungal Biodivers. Cent., Utrecht, Neth. 90. Shoda-Kagaya E, Saito S, Okada M, Nozaki A, Nunokawa K, Tsuda Y. 2010. Genetic structure of the oak wilt vector beetle Platypus quercivorus: inferences toward the process of damaged area expansion. BMC Ecol. 10:1 91. Six DL. 2012. Ecological and evolutionary determinants of bark beetle—fungus symbioses. Insects 3:339–66 92. Six DL, Bracewell R. 2015. Dendroctonus. See Reference 100, pp. 305–50 93. Smith SM. 2013. Phylogenetics of the Scolytini (Coleoptera: Curculionidae: Scolytinae) and host-use evolution. PhD Thesis, Michigan State Univ., East Lansing 94. Snyder JR. 2014. Ecological implications of laurel wilt infestation on Everglades tree islands, southern Florida. Open-File Rep. 2014-1225, US Geol. Surv., Reston, VA 95. Spence D, Smith J, Ploetz R, Hulcr J, Stelinski L. 2013. Effect of chipping on emergence of the redbay ambrosia beetle (Coleoptera: Curculionidae: Scolytinae) and recovery of the laurel wilt pathogen from infested wood chips. J. Econ. Entomol. 106:2093–100 96. Steininger M, Hulcr J, Sigutˇ M, Lucky A. 2015. Simple and efﬁcient trap for bark and ambrosia beetles (Coleoptera: Curculionidae) to facilitate invasive species monitoring and citizen involvement. J. Econ. Entomol. 108:1115–23 97. Suh SO, Zhou J. 2010. Yeasts associated with the curculionid beetle Xyloterinus politus: Candida xyloterini sp. nov., Candida palmyrensis sp. nov. and three common ambrosia yeasts. Int. J. Syst. Evol. Microbiol. 60:1702–8 98. Sullivan BT. 2011. Southern pine beetle behavior and semiochemistry. In Southern Pine Beetle II,ed.RN Coulson, KD Klepzig, pp. 25–50. Gen. Tech. Rep. SRS-140, US Dep. Agric. Forest Serv., Asheville, NC 99. van der Walt J. 1972. The yeast genus Ambrosiozyma gen. nov. (Ascomycetes). Mycopathol. Mycol. Appl. 46:305–15 100. Vega FE, Hofstetter RW, eds. 2015. Bark Beetles: Biology and Ecology of Native and Invasive Species. London: Academic 101. Wallace A. 1859. Note on the habits of Scolytidae and Bostrichidae. Trans. Entomol. Soc. Lond. 5:218–20 102. Wood SLW. 2007. Bark and Ambrosia Beetles of South America (Coleoptera, Scolytidae). Monte L. Bean Life Sci. Mus., Brigham Young Univ., Provo, UT 103. Yearian W, Gouger R, Wilkinson R. 1972. Effects of the bluestain fungus, Ceratocystis ips, on development of Ips bark beetles in pine bolts. Ann. Entomol. Soc. Am. 65:481–87 Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only.

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Annual Review of Entomology Volume 62, 2017 Contents

Following the Yellow Brick Road Charles H. Calisher pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Behavioral Sabotage of Plant Defenses by Insect Folivores David E. Dussourd ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp15 Neuropeptides as Regulators of Behavior in Insects Liliane Schoofs, Arnold De Loof, and Matthias Boris Van Hiel pppppppppppppppppppppppppppp35 Learning in Insect Pollinators and Herbivores Patricia L. Jones and Anurag A. Agrawal ppppppppppppppppppppppppppppppppppppppppppppppppppp53 Insect Pathogenic Fungi: Genomics, Molecular Interactions, and Genetic Improvements Chengshu Wang and Sibao Wang ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp73 Habitat Management to Suppress Pest Populations: Progress and Prospects Geoff M. Gurr, Steve D. Wratten, Douglas A. Landis, and Minsheng You pppppppppppppp91 MicroRNAs and the Evolution of Insect Metamorphosis Xavier Belles ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp111 The Impact of Trap Type and Design Features on Survey and Detection of Bark and Woodboring Beetles and Their Associates: A Review and Meta-Analysis Jeremy D. Allison and Richard A. Redak pppppppppppppppppppppppppppppppppppppppppppppppppp127

Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org Tephritid Integrative Taxonomy: Where We Are Now, with a Focus on the Resolution of Three Tropical Fruit Fly Species Complexes Mark K. Schutze, Massimiliano Virgilio, Allen Norrbom, and Anthony R. Clarke ppppp147 Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. Emerging Themes in Our Understanding of Species Displacements Yulin Gao and Stuart R. Reitz ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp165 Diversity of Cuticular Micro- and Nanostructures on Insects: Properties, Functions, and Potential Applications Gregory S. Watson, Jolanta A. Watson, and Bronwen W. Cribb pppppppppppppppppppppppp185 Impacts of Insect Herbivores on Plant Populations Judith H. Myers and Rana M. Sarfraz pppppppppppppppppppppppppppppppppppppppppppppppppppp207

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Past, Present, and Future of Integrated Control of Apple Pests: The New Zealand Experience James T.S. Walker, David Maxwell Suckling, and C. Howard Wearing ppppppppppppppp231 Beekeeping from Antiquity Through the Middle Ages Gene Kritsky pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp249 Phylogeny and Evolution of Lepidoptera Charles Mitter, Donald R. Davis, and Michael P. Cummings pppppppppppppppppppppppppp265 The Ambrosia Symbiosis: From Evolutionary Ecology to Practical Management Jiri Hulcr and Lukasz L. Stelinski pppppppppppppppppppppppppppppppppppppppppppppppppppppppp285 Social Life in Arid Environments: The Case Study of Cataglyphis Ants Rapha¨el Boulay, Serge Aron, Xim Cerd´a, Claudie Doums, Paul Graham, Abraham Hefetz, and Thibaud Monnin ppppppppppppppppppppppppppppppppppppppppppppppp305 Processionary Moths and Associated Urtication Risk: Global Change–Driven Effects Andrea Battisti, Stig Larsson, and Alain Roques pppppppppppppppppppppppppppppppppppppppppp323 African Horse Sickness Virus: History, Transmission, and Current Status Simon Carpenter, Philip S. Mellor, Assane G. Fall, Claire Garros, and Gert J. Venter pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp343 Spatial Self-Organization of Ecosystems: Integrating Multiple Mechanisms of Regular-Pattern Formation Robert M. Pringle and Corina E. Tarnita pppppppppppppppppppppppppppppppppppppppppppppppp359 Evolution of Stored-Product Entomology: Protecting the World Food Supply David W. Hagstrum and Thomas W. Phillips pppppppppppppppppppppppppppppppppppppppppppp379 Ecoinformatics (Big Data) for Agricultural Entomology: Pitfalls, Progress, and Promise Jay A. Rosenheim and Claudio Gratton pppppppppppppppppppppppppppppppppppppppppppppppppppp399 Annu. Rev. Entomol. 2017.62:285-303. Downloaded from www.annualreviews.org Molecular Evolution of Insect Sociality: An Eco-Evo-Devo Synthesis Amy L. Toth and Sandra M. Rehan ppppppppppppppppppppppppppppppppppppppppppppppppppppppp419

Access provided by University of Florida - Smathers Lib Gainesville on 02/01/17. For personal use only. Physicochemical Property Variation in Spider Silk: Ecology, Evolution, and Synthetic Production Sean J. Blamires, Todd A. Blackledge, and I-Min Tso ppppppppppppppppppppppppppppppppppp443

Indexes

Cumulative Index of Contributing Authors, Volumes 53–62 ppppppppppppppppppppppppppp461 Cumulative Index of Article Titles, Volumes 53–62 ppppppppppppppppppppppppppppppppppppp467

Contents ix