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Ecological and Evolutionary Determinants of Bark Beetle — Fu ngus
Symbioses
Article    in  Insects · Dec ember 2012
DOI: 10.3390/ insects3010339
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Insects 2012 , 3, 339-366; doi:10.3390/insects3010339

insects
ISSN 2075-4450
www.mdpi.com/journal/insects/
Review
Ecological and Evolutionary Determinants of Bark Beetle —
Fungus Symbioses
Diana L. Six
Department of Ecosystem and Conservation Scie nces, College of Forestry and Conservation,
University of Montana, Missoula, MT 59812, USA; E-Mail: [anonimizat]
Received: 16 February 2012; in revised form: 1 March 2012 / Accepted: 15 March 2012 /
Published: 22 March 2012

Abstract: Ectosymbioses among bark beetles (C urculionidae, Scolytinae) and fungi
(primarily ophiostomatoid Ascomycetes) are wi despread and diverse. Associations range
from mutualistic to commensal, and from f acultative to obligate. Some fungi are highly
specific and associated only with a single bee tle species, while others can be associated
with many. In addition, most of these symb ioses are multipartite, with the host beetle
associated with two or more consistent pa rtners. Mycangia, structures of the beetle
integument that function in fungal transp ort, have evolved numerous times in the
Scolytinae. The evolution of su ch complex, specialized structures indicates a high degree
of mutual dependence among the beetles and their fungal partners. Unfortunately, the
processes that shaped current day beetle -fungus symbioses rema in poorly understood.
Phylogeny, the degree and type of dependenc e on partners, mode of transmission of
symbionts (vertical vs. horizontal), effects of the abiotic environment, and interactions
among symbionts themselves or with other members of the biotic community, all play
important roles in determining the compositio n, fidelity, and longevity of associations
between beetles and their fungal associates. In this review, I provide an overview of these
associations and discuss how evolution and eco logical processes acted in concert to shape
these fascinating, complex symbioses.
Keywords : Ophiostoma ; Grosmannia ; Leptographium ; Ceratocystiopsis ; Ceratocystis ;
Raffaelea ; Ambrosiella ; cospeciation; host-switching; sy mbiosis; symbiont redundancy;
ambrosia beetle
OPEN ACCESS

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1. Scolytinae-Fungus Symbioses
The term symbiosis was coined by Albert Fra nk in 1877 to describe nonparasitic interactions
involving microbes [1]. The meaning was further refined by de Bary in 1879 to mean “the living
together of two differently named organisms” [1], a definition that remains in widespread use today.
Symbioses encompass a wide range of interaction types. Among the least studied are mutualisms, once
relegated to the status of curiosit ies of nature, but now considered im portant determinants of biological
organization, and community structur e and process [2–5]. In this review , I consider several factors that
may have shaped a diverse array of ectosymbioses, including mutualisms, amo ng bark beetles and fungi.
For more general treatments of these symbioses, I re fer the reader to severa l recent reviews [6–12].
In the context of scolytine beetle -fungus interactions, both the beetle and the tree they infest are often
referred to as hosts. To avoid confus ion, I will confine my use of the term “host” in this chapter to
denote strictly the beetle.
Bark beetles make up approximately 3700 of th e 7500 species in the weevil (Curculionidae)
subfamily Scolytinae [13–15]. The rema inder consists of ambrosia b eetles (3400 species) and various
seed and pith-feeding beetles (~400 species). A st riking characteristic of the Scolytinae is the
widespread association of its memb ers with fungi. All ambrosia beet les, and many bark beetles, are
associated with fungi [7,9,16]. Of the seed and pith feeders, little is known. However, fungi are
associated with members of this group as diverse as conifer cone beetles ( Conophthorus spp.) (Six,
pers. obs.) and the coffee berry borer ( Hypothenemus hampei ) [17].
Bark beetles are commonly associated with Ascomycetes in four teleomorph genera,
Ophiostoma , Ceratocystiopsis , Grosmannia , and Ceratocystis [7,9,10,18]. While these fungi produce
morphologically similar teleomorphs, Ophiostoma , Grosmannia , and Ceratocystiopsis form a
monophyletic group in the Ophios tomatales, separate from Ceratocystis , which is inthe Microascales
[19,20]. The two fungal groups also have different host plant affiliations. The fungi in the
Ophiostomatales are most often associated with conifers, while Ceratocystis species are usually
associated with angiosperms [ 21]. Anamorphs associated with Ophiostoma and Ceratocystiopsis include
Hyalorhinocladiella and Sporothrix , while some Ophiostoma species also produce Pesotum .
Grosmannia species produce Leptographium anamorphs [18], whereas Ceratocystis produce
Thielaviopsis anamorphs [22]. A relatively small number of bark be etles are consistently associated
with Basidiomycetes in the genera Entomocorticium and Phlebiopsis [23,24].
Ambrosia beetles are often associated with anamorphic species in the genera Ambrosiella and
Raffaelea but some are also associated with Ophiostoma , Leptographium , and Fusarium [9,16,25–28].
Interestingly, early molecular phylogenies revealed that Ambrosiella and Raffaelea were each
paraphyletic and multiply derived out of Ophiostoma and Ceratocystis [29,30]. Furthermore, one
monospecific genus Dryadomyces was found to nest within a clade containing both Ambrosiella
and Raffaelea species allied with Ophiostoma [31]. These inconsiste ncies were addressed by
Harrington et al. [32] who retained all Ambrosiella with Ceratocystis affinities within Ambrosiella but
transferred those associated with the Ophiostomatales to Hyalorhinocladiella . New combinations were
made in Raffaelea for Ambrosiella species allied with the Ophiostomatales as well as a transfer of
Dryadomyces to Raffaelea .

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Figure 1. Examples of ambrosia beetles and their galleries. From left to right, top to
bottom: Diuncus gallery; Trypodendron gallery; Xyleborina ambrosia beetles; Xylosandrus
crassiusculus gallery. All photos cour tesy of Jiri Hulcr.

Bark and ambrosia beetles are ca tegorized by their use of host plan t substrate, but there is no
absolute distinction between the two groups and most are associated with fungi to some extent.
Most ambrosia beetles construct galleries in the sapwood of trees (Figure 1). The term ‘ambrosia’
refers to the fungal gardens the beetles cultivate on their gallery walls and us e as an exclusive food
source [16,33]. The beetles are obligately dependen t upon the fungi, from which they acquire amino
acids, vitamins and sterols [16,33]. The activities of female beetles have been hypothesized to control
the growth and composition of ambros ial gardens. If the female dies, the garden is quickly overgrown
by contaminating fungi and bacteria, which ultimat ely results in the death of the brood [26,34].
The activities of the larvae may al so control non-mutualistic fungi, a lthough the mechanism for this is
unknown (X). Dispersing adult beetle s transport the fungi to new host trees in highly specialized
structures of the exoskeleton called mycangia (F igure 2), thus maintaini ng the association from

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generation to generation [7,35]. The in teraction is clearly mutualistic. The symbiosis allows the beetles
to exploit a nutritionally poor re source (wood) and reduce interspeci fic competition, while providing
the fungi consistent transport to a relatively rare and ephemeral resource (a new host tree of the
appropriate condition and successional stage) [11,16].
Figure 2. Examples of mycangia. From left to ri ght, top to bottom: maxillary cardine of
Dendroctonus ponderosae showing opening of sac myca ngium (arrow) courtesy of
Katherine Bleiker; Close up of mycangium of D. ponderosae showing fungal mass extruding
from opening courtesy of Katherine Blei ker; Oval brush mycangium on female Pityoborus
rubentris Mal Furniss; close up of brush mycangium of P. rubentris containing spores Mal
Furniss; Ascospores in p it mycangium (puncture) of Ips pini Mal Furniss; mesonotal paired
sac mycangia of Xylosandrus mutilates (dissected from beetle) courtesy of W. Doug Stone.

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Figure 2. Cont.

Figure 3. Examples of bark beetles and their galle ries. Left to right, top to bottom: Pupal
chambers containing Dendroctonus.ponderosae pupae and spore layers of fungi, courtesy
of the author; D. ponderosae adult, courtesy of the author; Bark section showing extensive
beetle development in light portions colonized by mutualistic fungal symbionts and lack of
development in highly stained portion of ba rk colonized by the antagonistic fungus, O.
minus (arrow) courtesy of Fred Stephen; I. pini courtesy of Jesse Logan.

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In contrast, bark beetles construc t their galleries in the phloem la yer of trees just under the outer
bark (Figure 3). Unlike ambrosia beetles, bark beet les feed on tree tissues (phloem), and gain some of
their nutrients directly from the host. Phloem co ntains more nutrients than sapwood, but nonetheless
has a low nutritional value relative to the dietary requirements of insects [36–38]. Nitrogen is the
limiting factor in the diets of most herbivorous insects [39]. This is tr ue even for insects that feed on
foliage, which is relatively high in nitrogen comp ared with other tree tissues, including phloem. For
instance, the nitrogen content of lobl olly pine phloem (a host to several bark beetles) is approximately
0.38% [40] compared with 1–5% in the foliage [39]. Insects cont ain approximately 6–10% nitrogen,
indicating that to complete development they must either consume large amounts of plant material
relative to their final body size [41,42] or modify their diet in such a way as to increase the nitrogen
content [38]. In the case of bark be etles, diet modification may include the use of fungal associates to
supplement the nutritional limitations of their phloem diet [38,43].
Evidence supports the existe nce of both high consump tion and diet modificati on strategies in bark
beetles. Ayres et al. [38] compared nitrogen budgets of two co-occurring bark beetles, Ips grandicollis
and D. frontalis , which have different feeding strategies. Ips grandicollis is a non-mycangial beetle
that constructs long feeding galle ries in phloem. In contrast, Dendroctonus frontalis , a mycangial
beetle, produces short galleries terminating in ‘feeding chambers’ where it spends most of its
development feeding on ambrosial growth of its my cangial fungi [44, S.J. Barras, pers. comm.].
Ayres et al. [38] found that th e nitrogen concentration around succe ssfully developing larvae of
D. frontalis is more than twice that of phloem of uninfested trees; the phl oem with the highest nitrogen
concentration was located where feeding chambers were colonized by the mycangial fungi. Similarly,
Hodges et al. [43] also found that phloem nitrogen in Pinus taeda increased 131% when D. frontalis
and its associated f ungi were introduced.
Ayres et al. [38] also found nitrogen concen trations significantly impacted D. frontalis fitness.
Regions in trees where larvae survived to pupate contained the highest ni trogen concentration, and
trees and regions with the highest n itrogen concentrations produced the biggest beetles. Beetle size is
strongly correlated with beetle survival, fecundity, pheromone production and dispersal [45–53], and
thus, is a good indicator of beetle fitn ess. Interestingly, one mycangial fungus, Entomocorticium sp.,
was superior to another, Ceratocystiopsis ranaculosus , at concentrating nitrog en [38]. This difference
may explain why D. frontalis individuals that develop with Entomocorticium are larger and have
higher lipid contents than those that develop with C. ranaculosus [54], and why beetle populations
with a higher prevalence of Entomocortium sp. exhibit more rapi d population gr owth [54–56].
In contrast to D. frontalis , Ips grandicollis appears to employ the high consumption rather than the
diet modification strategy [38]. These beetles f eed extensively in phloem, do not produce feeding
chambers, and do not appear to depend on fungi fo r nutrition, although they do vector ophiostomatoid
fungi [57,58 ]. Although I. grandicollis adults are only sli ghtly larger than D. frontalis adults, their larvae
consumed 79% more phloem than D. frontalis larvae [38], supporting the hypot hesis that without diet
supplementation with fungi, larvae must consume mo re phloem to meet thei r nitrogen requirements.
Given that I. grandicollis is likely to feed at least incidenta lly on the various fungi it vectors, these
results indicate that not all fungi areequally effective as su pplements to beetle diets.
Other dietary requirements of the insect macros ymbiont may also influence feeding strategy.
For example, insects require sterols for normal growth, metamorphosis, and reproduction. However,

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insects, unlike most other animals, are unable to synthesize these compounds, and thus, are dependent
upon a dietary source [59–61]. Sterols are present in plant tissues, but t ypically only in low
concentrations [62], or in forms not usable by in sects [59]. For phloem-feeding bark beetles, whose
food may contain inadequate concentr ations of usable types of sterols, fungal symbionts may provide
an alternate source. Fungi typica lly produce ergosterol, a sterol wh ich is highly usable by many
insects [59]. In several insect-fungus symbioses, the insect associat e depends on ergosterol production
by the fungal associate to meet its sterol requirement s [63,64]. This is the case for xyleborine ambrosia
beetles [33,65,66] and possibl y the coffee berry borer, H. hampei [17, but see 67], and may also be true
for some bark beetles [68].
The ergosterol contents of ophiosto matoid fungi associated with am brosia and bark beetles have
been investigated for only a few species. For fungi associated with Xyleborus ambrosia beetles,
ergosterol content ranged from 0.12–0.24% [69]. However, for three species of fungi associated with
two Dendroctonus bark beetle species, the ergosterol content was much higher at 0.88–1.06% [68],
indicating that these fungi may also provi de good sources of sterols for their hosts.
For phloeomycophagous bark beetles, the importance and role of fungi in host nutrition may vary
by life stage. An experimental study on D. ponderosae reported that larvae feed primarily in sterile
phloem, and thus do not depend on fungi to complete development [70]. In that study, single pairs of
D. ponderosae were introduced into logs with ends waxe d to retard drying, then held at constant
temperatures. Some first instar larvae and all teneral adults were associated with fungi, but intermediate
stages of development occurred in sterile phloem. However, in a recent study [71] conducted under
field conditions, in naturally infested trees with natural attack densities of beetles (and fungi),
approximately two-thirds of 1st instars and 100% of all later instar s were located in phloem colonized
by fungi. Gut dissections re vealed that the symbioti c fungi were ingested by larvae along with their
phloem diet. In addition, larvae often migrated back into older portions of th e gallery, presumably to
feed where the fungi were best es tablished. Such turning behavior by larvae in axenic phloem was also
observed by [72], who specula ted that such behavior may be linked to the need for larvae to feed in
areas containing fungal growth.
Development and feeding on fungus-colonized phlo em is common for many bark beetles and has
also been observed in othe r experimental studies [73]. However, not all fungi ar e equally desirable as
food and each association must be considered inde pendently when assessing potential benefits from
fungal feeding. For example, D. frontalis encountering areas stained by the antagonistic fungus,
O. minus , turn to avoid feeding in these areas . However, the tunneling behavior of D. ponderosae and
I. pini is unaffected by the presence of staining caused by G. clavigera and O. ips [73]. Furthermore, in
choice tests, D. ponderosae larvae chose stained phloem (containing G. clavigera and O. montium ) for
feeding significantly more ofte n than unstained phloem [74].
Although Adams & Six [71] found that larvae of D. ponderosae are phloeomycophagous, the mere
ingestion of fungi does not, by itself , indicate that fungal feeding is be neficial to a de veloping brood.
Unfortunately, the relative intractability of these systems to manipulative experimentation has limited
our knowledge of how mycophagy affects host developm ent and fitness. However, studies conducted
on two mycangial Dendroctonus species in naturally infested materi al indicate that fungal associates
can have a considerable impact on hos t beetle fitness by affecting larvae. Dendroctonus frontalis
individuals that develop with myca ngial fungi are larger than thos e that develop without mycangial

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fungi [38,54,75]. Because adult beetle size is determined by larval nut rition, larger adult size in the
fungus-associated beetles cannot be a result of matura tion feeding on spore layers by teneral
adults [76]. Furthermore, larval surviv al is higher, and feeding galleries of Dendroctonus are shorter,
in the presence of mutualistic fungi than in their absence, indicating that fungus-colonized tissues have
higher nutritional contents [38,75,77]. Not surprisingly, th e multiple fungal partners associated with a
host tend to vary in their e ffects on beetle broods. For D. frontalis , Entomocorticium sp. supports
higher host survival and larg er body size than does C. ranaculosus . For D. ponderosae , G. clavigera
supports faster brood development a nd higher brood production than does O. montium [77]. Similar
results were found in an experiment conducted with a non-mycangial beetle, I. paraconfusus . Axenically
reared beetles, and those reared with the antagonistic fungus O. minus , were smaller than beetles
reared with symbiotic fungi associated with the b eetle, and larval tunnels were significantly longer
when larvae were associated with O. minus than when not associated with fungi [72].
The role of mycophagy in adult nutrition is poorly understood. Tenera l adults of mycangial bark
beetles feed on dense layers of spores that gr ow on the pupal chamber walls, before emerging to
disperse to new host trees (Figure 3) [70,77]. This also may be true for several non-mycangial beetles
that are consistently associated with fungi that produce spore laye rs in their pupal chambers. This
period of feeding on spores as new adults may be important for beetles to acquire fungi in their
mycangia and/or on their exoskelet ons for dispersal to the next hos t tree and the next generation of
beetles. However, feeding on spores at this time also appears to be impo rtant in adult reproduction.
New adults of D. ponderosae that did not feed on the co nidia of mutualistic fungi ( G. clavigera ,
O. montium ), tunneled and fed extensively in phloem. In contrast, insects that fed on spores did not
tunnel and feed in phloem and emerged ve ry close to the pupa l chamber [74]. New D. ponderosae
adults that did not feed on spores had very high ra tes of rejection of logs, produced few galleries, and
did not produce broods. In contrast, new adults that fed on spores of either of the beetle’s symbiotic
fungi tended not to reject logs , usually produced galle ries, and many also produced broods [77].
Axenic I. paraconfusus adults also did not oviposit, while those a ssociated with fungi did [72]. These
results indicate that feeding on fungal spores by new adults may be critical for adult nutrition and
reproduction for at least so me bark beetle species.
Obligate symbiosis is typically defined as the inabi lity of one or both interacting partners to live
without the other. At its simplest, this can mean that if, in a single reproductive cycle of a partner pair,
one partner is removed, the other partner dies or cannot reproduce. However, the term can also denote
partnerships where the separation of host and symbiont results in fitness costs that, over only a few
generations, eventually result in the loss of one or both partners. Determining whether a particular
symbiosis is obligate can be an immensely difficult task. It is challenging, and sometimes impossible,
to produce aposymbiotic hosts. Furthermore, the pro cesses used to remove sy mbionts can be extremely
stressful to hosts, bringing into question the validity of experime nts conducted with such hosts.
A challenge in testing for dependence is that hosts mu st be reared at least th rough the F2 generation to
control for maternal effects [66,78]. For insects such as bark beetle s that can be difficult to rear
through the F1 generation, this is a serious obstacl e. To date, obligacy has been shown (and looked for)
in only a few bark beetle-fungus symbioses [56,77]. No studies that claimed to successfully rear
beetles without symbiotic fungi meet stringent re quirements for testing for dependence on symbiotic
fungi for nutritional supplementati on, either because they were conducted only through the F1

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generation [72,79], or because the beetle’s diet was supplemented or contaminated with fungi or fungal
products [80–82].
For bark beetles, detecting obligacy can be fu rther complicated by multipartite associations
involving hosts with two, less often three, consistent fungal associates. In some associations, these
symbionts may provide a similar benefit to the hos t (symbiont redundancy) [56,77]. In such cases, the
host may be dependent on the presence of a symbiont , but not any one symbi ont, in particular. The
concept of ecological (or functiona l) redundancy has been particularly well-developed in the field of
biodiversity conservation, but much less so in symbio logy, where most efforts have focused on pollinator
assemblages [83]. The concept of symbiont redunda ncy is further developed for bark beetle-fungus
symbioses in a later section.
To this point, I have focused primarily on fungi as mutualists of bark beetles. However, many
ophiostomatoid fungi are inconsistently associated with particular beetle species and often are associated
with several beetle species across a wide geographic area (ex. O. piceae , O. penicilliatum ). Such
broadly distributed fungi are probab ly opportunistic commensals, benef iting from transport, but without
significant reciprocal effects on the host [7,10]. Other fungi in this group are antagonists and their
presence results in lowered host fitness. For example, D. frontalis developing in areas colonized by
O. minus seldom survive (Figure 3) [ 84,85]. Why some ophiostomatoid fungi are beneficial while
others are antagonistic, or have no apparent effect on their host, is unknow n, but may reflect their
ability to concentrate n itrogen [38], to produce adequate amount s of sterols [68], or to produce
toxic metabolites [86].
Our ability to make generalizations about bark b eetle-fungus symbioses is c onstrained by a lack of
knowledge on all but a very few systems. Only a few studies have been conducted and the majority of
these have focused on the tree-k illing, economically important bee tles. This focus on aggressive
beetles has yielded a highly biased view of bark beetle-fungus interactions, including a near exclusive
focus for many years on the potential, and still uns ubstantiated, role of the symbiotic fungi in
tree-killing [12]. However, in the Scolytinae, tree-k illing is actually a relati vely rare event of life
history. Instead, most scolytines are restricted to weak, dying, or more often, recently killed trees. For
example, of the hundreds of scolytine species in North America, only 7–10 commonly kill trees [14].
The majority of the remaining non-tree-killing species are associated with fungi in one way or another,
but remain mostly unstudied.
2. Evolution of Scolytinae-Fungus Symbioses
The Scolytinae are thought to have arisen in the Late Jurassic or Ea rly Cretaceous periods, with the
most recent estimates dating to about 100 milli on years ago [87–89]. Conifers are probably the
ancestral hosts of the Scolytinae and its most clos ely related subfamilies in the Curculionidae [90,91].
The putative sister group to these subfamilies, the De rolominae, is associated with monocots, implying
that a common ancestor shifted from angiosperms to conifers [91]. In the Scolytinae, this switch was
followed by several returns to angiosperms, then severa l subsequent reversals to conifers. Each shift to
angiosperms was accompanied by increased species divers ity, whereas reversals to conifers resulted in
low diversity [91].

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Ophiostomatoid fungi apparent ly arose 200 million years ago [ 92], with the groups containing
Ophiostoma (and allied genera) and Ceratocystis probably diverging around 170 million years ago [91].
Therefore, these fungi predate th e Scolytinae and may have evolved adaptations for insect dispersal
prior to their association with scolytine beetles. They were probably orig inally vectored by other
arthropods, possibly including weevil ancestors of the Scolytinae [91].
The ambrosia and bark beetles do not form exclus ive monophyletic groups within the Scolytinae;
rather, the two fungal feeding strategies evolved se veral times independently. The origins of ambrosia
feeding all followed shifts to angiosperms, although th ere apparently were reversals to conifer feeding
by some temperate ambrosia beetles [88]. The ambrosial feeding habit has evolved at least eight times
(possibly more) from different be etle tribes containing phloem-f eeding beetles associated with
Ophiostoma , Grosmannia , and/or Ceratocystiopsis species [91,93]. These ambr osial feeding strategies
have been estimated to have evolved 21–60 milli on years ago, depending on beetle lineage. Likewise,
within the Scolytinae, phloeomycophagous bark beetle s occur in several dispersed tribes, ranging from
the Tomicini to the Ipini [91].
The paraphyletic nature of the am brosia beetle-associated genera, Ambrosiella and Raffaelea , with
derivations from both Ophiostoma and Ceratocystis , may reflect these multiple origins and host shifts.
When some beetles switched to angiosperms, some apparently maintained associations with
Ophiostoma . Others may have switched to Ceratocystis , which they may have encountered for the first
time in their new hosts. Ceratocystis species have morphological adap tations for insect dissemination
similar to those of Ophiostoma , and may have been pre-adapted fo r vector relationships with these
beetles. If some Ceratocystis species also provided nut ritional benefits, then once associations formed,
similar lifestyles may have led to a convergence of form in the fungi, and to the multiply derived
genera that are evident today. The modern association of Ceratocystis species with a very few
conifer-using bark beetles may indicate that some fungi ‘followed’ beetles back to conifers.
Interestingly, at least one lineage of Ambrosiella (now transferred to Hyalorhinocladiella ) is not
associated with ambrosia beetle s, but rather with species of Ips, Polygraphus , and Hylurgops [30],
indicating an independent origin of this morphological form with bark beetles in conifers. Past reliance
of fungal taxonomy on morphology has led to the current unnatural classificati on used for many fungi
associated with Scolytinae. In many cases, convergent evolution for an insect-a dapted lifesty le has led
to similar forms resulting in unrelated fungi being placed within the same genus. Rigorous revisions of
these genera to better reflect actual relationships will vastly improve our unde rstanding of these fungi
and how interactions with scoly tine hosts ultimately influence thei r form, function, and distribution.
Floristic composition and diversity may be important driver s of diversity in herbivorous
insects [94,95]. Indeed, enhanced rates of divers ification in angiosperm -feeding beetle lineages
resulted in nearly half of the species in the or der Coleoptera, which contai ns much of the insect
biodiversity on Earth [95]. However, for many insects, including the Scolytinae, host plant diversity
may be only one of several factors influencing diversification. For ambr osia beetles, th e adoption of a
strictly mycophagous habit may have led to extens ive species radiations in the Xyleborini and the
Platypodini [96]. However, these radiations occurred mainly in tr opical rainforests, where both warm
temperatures and high humidity fa vor fungal growth [97] and the di versity of trees is very high,
confounding our ability to detect dr ivers of diversity in these sy stems. In addition, the massive
radiation of the Xyleborini occurr ed simultaneously with the devel opment of inbreeding. Because, in

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several lineages of ambrosia beetles, the developm ent of a strictly fungus-f eeding lifestyle did not
result in extensive radiations and they remain re latively species poor, we cannot conclude that the
development of strict fu ngal feeding in and of itself supports radiation. However, while conifer-using
lineages within the Scolytinae ar e species-poor, relative to some angiosperm-using lineages, three
tribes [Tomicini (including the Hy lastini), Ipini, and Corthylini] are among the most species-rich
conifer associations known [91] i ndicating that fungus feeding may, at least at times, support greater
species diversity.
The development of mutualisms with fungi also ma y have supported the divers ification of scolytine
lineages inhabiting conifers. Two of the three most di verse conifer-using tribes in the Scolytinae, the
Tomicini and the Ipini, contain most known examples of mycophagous bark beetles. The third tribe,
the Corthylini (which also contains an ambrosia bee tle lineage), contains the species-rich Pityophthorina,
many of which use conifers, and which are also associated with fungi [98–100], but remain
uninvestigated for mycophagy.
Mutualism allows organisms to excel in marg inal habitats, exploit new niches, avoid
competition, and buffer environmental variability [ 11,101]. In the cases of both ambrosia beetles and
mycophloeophagous (combined fungus-phl oem feeders) bark beetles, the use of fungi for food
has expanded the capacity of these insect s to use nutrient-poor plant resources [15].
Nutrition/transport-based mutualisms evolved ma ny times in the Scolytinae and transitions from a
strictly plant-based diet to a combined or stri ctly fungus-feeding strategy perhaps evolved relatively
rapidly. The evolution of mycangia ma y be a particularly useful metric of both the advantage, and the
rapidity, of the evolution of fungus-beetle mutua lisms. Mycangia evolved independently many times in
the Scolytinae. They are present in almost all am brosia beetle species a nd in many bark beetles.
Furthermore, mycangia within the same genus o ccur in different body regions, or differ in their
distribution between the sexes, i ndicating independent, rapid origins over a very short evolutionary
time frame [91,102]. Mycangia occur across many bee tle tribes, including some basal groups, suggesting
that fungus feeding has been advantage ous to the Scolytinae from its origin.
The propensity of Scolytinae to form nutrition/tran sport-based mutualisms with fungi is probably
linked to two characteristics that have exemplifie d the subfamily since its beginnings: the exploitation
of inner plant tissues and the forma tion of associations with fungi that grow there. However, the exact
path leading to the formation of these mutualisms is unknown. Two m odels for evolutionary transitions
from a plant-based diet to ‘fungiculture’ in insects have been proposed [103]. In the ‘transmission first’
model, the insect is first associated with a fungus as a vector, then begins to obtain nutrition from the
fungus, and finally relies on the fun gus as a food source [11,103]. In the ‘consumption first’ model,
an insect lineage begins to incorporate fungi into a generalized diet and then becomes a specialized
fungivore. Implicit in the second m odel is that both insect and fungus must also develop adaptations
for vectoring to ensure transmissi on from generation to generation. Both models are tenable for the
Scolytinae, and it is likely that various forms of both models have occurred to produce the associations
that we see today.
If current day associations with fungi reflect phylogenetic history, then scolytine beetles were
associated with Ophiostoma (and allied genera) from their or igin. Many, if not all, of the most
primitive members of this subfamily (ex. Hylurgops , Hylastes , Pseudohylesinus ) vector Grosmannia
and Ophiostoma species, but with no evident benefit to the host. Such apparently strictly vector

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associations occur thro ughout the Scolytinae (ex. Scolytus , Orthotomicus ), interspersed between the
phloeomycophagous bark beetle and ambrosia b eetle lineages. Such vect or associations are
unsurprising, given that ophiostomatoid fungi are very well adapted to insect dispersal [104] and that
these adaptations appear to have arisen prior to the origins of th e Scolytinae [91]. In addition, both
beetles and their associated fungi colonize early in succession, colonizing living (at least in the initial
stages of attack) or freshly killed plant material. As a consequence, both must arrive very early in the
colonization sequence. Among the many loose associa tions that formed, some eventually developed
into nutrition/transport-based mutualisms of the am brosial type with beetle s exploiting angiosperms,
and of the phloeomycophagous type for beetles expl oiting conifers. Of note is that while some
ambrosia beetles attack conife rs, there are no known phloeomyc ophagous species among the bark
beetles that colonize angiosperms.
Regardless of how these associatio ns originated, it appears that on ce established, reversals from the
fungus-feeding state are rare or nonexi stent. No reversals to a non-ambrosia feeding state are known in
ambrosia beetles [91] or for ot her insect-fungus nutrition/transport- based mutualisms, including the
fungus-gardening ants and termites [ 11]. This indicates that the tran sition to obligate mycophagy is a
major and potentially irreve rsible change that constrains subseque nt evolution [11]. Even where beetles
have lost the capacity to vector the fungi, they co ntinue to exploit fungi through mycocleptism [105].
The independent evolution of fungus feeding many tim es in the Scolytinae suggests that an overall
tight concordance of phylogenies of the beetles a nd their fungal associates should not be expected.
However, for particular lineages of beetles, espe cially those with shared mycangial types and common
obligate associations with fungi, we might expect ev idence of tightly linked e volutionary histories and
cospeciation. This has not been explicitly investig ated, except in one study where it was found that
some Ceratocystiopsis and Dendroctonus possessing pronotal mycangia, and some Grosmannia and
Dendroctonus possessing maxillary mycangia, show evid ence of cospeciation [102]. However, the
same study revealed that host switching and/or colo nization events also oc curred in these same
associations. While no other stud ies looking explicitly for cospecia tion have been conducted in the
Scolytinae, the distribution of f ungal species among various host beetle s indicates that host switching
has been common, even among ambrosia beetle lineages and their f ungal associates [7,28,91].
There are several reasons why strict cospeciation of beetle ho sts and fungal symbionts may be rare,
or at least difficult to detect, in the Scolytinae. Tw o factors appear to greatl y facilitate cospeciation:
strict vertical transmission of sy mbionts, and restricted options to acquire hosts or symbionts from
outside the relationship [106,107]. Ne ither criterion appears to be strictly met by scolytine-fungus
associations. The presence of highly specific organs to transmit symbionts (mycangia) at first may
seem to indicate strict vertical transmission. Howe ver, unlike endosymbioses with symbionts transmitted
directly from mother to offspring via the egg, in scolytine-fungus ectosymbioses, the fungi are inoculated
by the beetles into plant tissues where they grow fo r a period of time independent of the host before
being reacquired by offspring as teneral adults. This period of growth in wood presents a weak link in
the transmission process and provides an opportun ity for horizontal transm ission of symbionts.
Vertical transmission may be more reliable in so me ambrosial systems than in others, and more
reliable in ambrosial systems than in phloeomycopha gous systems. For example, in ambrosial species
of the Xyleborini, only females possess mycangia, and mating occurs between siblings in the natal
substrate [108–110]. For these beetles, males do not di sperse and only females contribute inoculum to

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the brood. However, for some ambrosia and most ba rk beetles, both sexes di sperse to, and mate in,
new substrates prior to initiating a brood [108]. For these insect s, both sexes carry fungi to the
breeding substrate, greatly decreas ing the likelihood of strict verti cal transmission. This is true
regardless of whether one or both sexes, or neith er sex, possess mycangia. For mycangial beetles, one
or both parents may transmit mycangial fungi not only in mycangia but also on their exoskeletons
(although mycangial fungi are often transmitted at much lower rates on the exoskeleton than in
mycangia, [111]). For non-mycangial beetles, f ungi are transported on the exoskeleton, although
efficacy of vectoring can vary by sex [112]. Very importantly, parents often originate from different
broods and often from differe nt trees. This means that the fungi th at each contributes to its offspring
may be different species or differe nt genotypes of the same species.
For both ambrosia and bark beetles, this is further complicated because commensal ophiostomatoid
fungi are often also transported by parents. Mu ltiple scolytine beetle species (and their fungal
associates) often cohabit one tree, further increasing the potential pool of fungi that a brood might
contact. Therefore, even if a beetle begins de velopment with one fungus faithfully transmitted by only
one parent, it is liable to be exposed to, and pot entially acquire, several ot her fungi by adulthood. Such
exposure, over time, may result in host switching or colonization events. It may also account for the
multipartite nature of many of th ese associations. The ability of hosts to occasionally acquire new
partners might have led, not only to the replacement of old associates with new, but also to the addition
of new associates to old. In some cases, new asso ciates may be acquired because of their superior
qualities. In contrast , some symbionts may be ‘cheaters’ that have infiltrated esta blished associations
between the host and superior , established symbionts.
However, despite evidence that host switching and colonization events were common over
evolutionary time, many mutualistic beetle-fungus symbioses are highly specific. This indicates that
host switching is constrained, and that mechanisms ex ist to ensure fidelity of partners. In contrast,
associations of fungi with beetles that merely act as vectors are le ss constrained. This may explain why
some beetles easily acquire novel o phiostomatoid species when introduc ed into new habitats or when
new fungi are introduced into their native range by exotic beetles or in wood [100,113,114].
Abiotic factors may also greatly affect acquisition of fungal associates by beetles, and thus may also
act to disrupt vertical transmission. As a season pr ogresses, variation in environmental conditions can
cause variability in the relative growth rates of fungal symbionts. This influences which fungi
sporulate in the pupal chamber at the time of tene ral adult maturation feeding, and thus determines
which fungi are acquired by the beetles and dispersed to the next host plant and the next generation of
beetles [115] (discussed further in a later section). Therefore, as e nvironmental conditi ons vary over a
season, over years, and by location, f ungal assemblages associated with a beetle species may vary and
shift merely by the influence of abiotic factors. Indeed, the abiotic environment has played, and
continues to play, an important role in determining the distribution of the fungi with beetle hosts on
both local and regional scales.
Absence of evidence of strict cospeciation does not imply that these are wholly unconstrained
associations. Cospeciation and host switching/col onization events represent phylogenetically- and
ecologically-mediated evolutionary processes [116]. These processe s, while seemingly independent,
can be coupled, with phylogenetic re lationships strongly infl uencing the nature of a host shift that is
otherwise ecologically mediated [ 116]. In the case of scolytines a nd ophiostomatoid fungi, host shifts

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occur, but usually to phylogeneti c relatives (within Ophiostomatale s or Microascales), although often
not to a sister species. Therefore, while we see littl e evidence of cospeciation, host transfers appear to
be mostly constrained to members within the Scolytinae and the ophiostomatoid fungi.
Phylogenetic conservatism, howeve r, has not been absolute be tween ophiostomatoid fungi and
scolytines. For example, D. frontalis possesses two mycangial fungi. One, Entomocorticium sp. A, is a
Basidiomycete. This fungus appears to be a superi or symbiont compared with the more coevolved
ophiostomatoid associate, C. ranaculosus , indicating that this Basidiomycete was acquired
opportunistically because of its benefit to the host . Furthermore, ophiostomatoid fungi can also be
consistently found in Protea infructescences, in soil, and even in the mounds of fungus-gardening
termites [117,118]. These ophiostomatoid fungi in Prot eas and termite mounds li e in a highly-derived
clade within Ophiostoma and thus these associations pr obably formed after those between Ophiostoma
and bark beetles [18]. Th erefore, while phylogenetic conservati sm clearly has imposed constraints,
new opportunities have been exploited, resulting in the formation of associat ions between beetles and
non-ophiostomatoid fungi and ophiostomato id fungi and non-scolytine hosts.
3. The Role of Biotic and Abiotic Factor s in Shaping Scolytinae-Fungus Symbioses
The structure of biological communiti es is seldom determined by a si ngle major factor or process,
but by many independent and interacti ng processes. This is also true for subsets of interactions within
the broader community including symbioses. Below, I discuss the major biotic and abiotic factors and
processes that influence th e structure of symbiotic fungal assembla ges associated with bark beetles.
3.1. The Host Plant
The host plant provides the substrate and nutr itional resources that support the growth and
reproduction of both beetles and fungi. The majority of scolytines and their associated fungi colonize
freshly killed plant material (whether the beetles them selves kill the plant or arrive after the fact),
which means that, at least initially, the plant is a relatively inhospitable environment. Host tree
defenses present at the time of colonization [119] can repel or even kill host beetles and are often
fungitoxic or fungistatic. Aggre ssive beetles reduce host tree effects by a pheromone-mediated mass
attack that kills the tree and quickly reduces tree defenses [120]. Fungal associates are often
pathogenic to the host plant, facilitating their survival in still living or newly- killed plant tissues until
defenses subside. Interestingly, most fungi associat ed with tree-killing beetles (primary and secondary,
e.g., D. frontalis , I. pini ) possess relatively low levels of virulence [6,10]. In c ontrast, fungi associated
with beetles that develop in living trees, where the tree does not die (e.g., Hylurgops , Hylastes , D.
valens , D. terebrans ), possess relatively high levels of vi rulence [121–123]. These differences in
virulence may reflect differences in fungal life historie s. For fungi associated w ith tree-killing beetles,
high levels of virulence are unnecessary because plan t defenses are active only briefly. On the other
hand, fungi associated with beetle s developing in living hosts may re quire greater virulence to avoid
containment and to be able to persist in a contin uously defensive tree until new brood adults disperse
up to a year after initial introduction.
The challenge of using trees as substrate does not end once defenses have abated. The quality and
condition of a host tree changes, often radically, over the development period of the beetles. Tree

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tissues are highest in nutrients a nd moisture at the time of coloniza tion, but by the time of brood adult
emergence and dispersal, much of the phloem resour ce has either been consumed or has become badly
degraded and depleted of nutrients [8]. Furthermore, moisture loss over this period can be considerable,
often contributing to the mortality of substantia l numbers of the beetle brood and contributing to
decreasing areas in the tree colo nized by symbiotic fungi [124,125].
Changes in chemistry, moisture and nutritional conten t of the host plant can a ffect the distribution
and relative prevalence of funga l associates within a tree. Adam s and Six [71] observed that the
relative prevalence of G. clavigera and O. montium (the former a moderately virulent pathogen, the
latter a weak pathogen/sa probe) associated with D. ponderosae shifted dramatically over beetle
development. These shifts were probably driven by changes in tree defenses and moisture conditions
(and temperature, discussed below). Variation in virulence among fungal associates affects the rate and
timing of their capture of resources within the tree. Initia lly, fungi with greater virulence (and typically
greater tolerance to high levels of moisture and low levels of oxygen) grow more rapidly and capture
more resource [126]. However, as defenses decline a nd tree tissues begin to dr y, the less virulent, more
saprophytic fungi, begin to dominate. Furthermore, wh ile some fungi are highly competitive in one set
of conditions, they may be poor competitors under others [125]. Thus, changes over time within the
tree influence not only re lative rates of growth and primary res ource capture, but al so the outcome of
direct competition among the various fungi [125,127].
3.2. Microbes
Bark beetles and their symbiotic fungi coexist with a multitude of microbes. These include yeasts
and bacteria that colonize beetle galleries and that are likely vectored into the tree by the beetles, and
endophytic bacteria and fungi that grow within hos t tree tissues irrespective of the presence of the
beetles. While most studies conducted on microbes asso ciated with beetle galleries are surveys [128 and
others], only a few have focused on the potential ecological roles of these microbes in these
microhabitats [129–133]. Nair et al. [134] isolated a bacterium, Bacillus mojavensis , from galleries of
the ambrosia beetle, Xylosandrus compactus , that inhibited several fungi, including the ambrosial
fungus of the beetle. Adams et al. [135] found that both yeasts and bact eria have substantial effects on
the growth of the tw o mycangial fungi of D. ponderosae . The yield of O. montium grown in vitro
individually with two yeasts and a bacterium isolated from larval galleries was much greater than the
yield of O. montium grown alone. However, the relative yield of G. clavigera grown with these same
microbes was less than when it wa s grown alone. These results sugge st that at least some microbes
found in larval galleries f acilitate the growth of O. montium and are antagonistic to G. clavigera .
A bacterium isolated from uncolonized phloem (a put ative endophyte) strongly i nhibited relative yield
of both G. clavigera and O. montium and appears to be an antagonist to both. Subsequent work has
characterized various effects of ba cteria associated with bark beet les on symbiotic fungi indicating
they may, at least in part, mediat e interactions between the symbiotic fungi and the host beetle [136].
Cardoza et al. [132] observed D. rufipennis producing oral secretions th at inhibited the growth of
fungi associated with the host beetle. These oral s ecretions contained bacteria that inhibited one or
more of the fungi, including the ophiostomatoid symbiont, L. abietinum . Further, actinomycetes in
mycangia may provide some protection to bene ficial fungi from anta gonistic ones [137].

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Work on bark beetle gut communities indicates a hi gh diversity of microbes associated with this
niche; however, the roles of these microbes and their potential interactions with bark beetle symbiotic
fungi remain poorly understood [ 138,139]. Overall, it appears that at least some co-occurring microbes
impact the distribution of symbio tic fungi through antagonistic or facilitative interactions, with
potentially important indirect eff ects on the fitness of host beetles.
3.3. Arthropods
Bark beetles and their symbiotic fungi also sh are trees with many arthropods. These arthropods
include natural enemies (predators and parasitoids), phloem and w ood borers, and fungivores, as well
as other bark beetle species. Some of these arth ropods significantly affect beetle-fungus symbioses.
Bark beetle species that cohabi t the same tree can compete for resources. Their fungi may also
compete for space and resources wh ile also disrupting c ontact between a beetle and its normal fungal
assemblage.
Some mites, phoretic on bark beetles, have cl ose symbioses with ophios tomatoid fungi [140,141].
These mites feed on their associated fungi and vect or them in sporothecae, the structures of their
exoskeletons being analogous to bark beetle mycangi a. Mites and their associates can have profound
effects on the fitness and population dynamics of ba rk beetles and their associated fungi [141].
Interestingly, a mite-scarab be etle-ophiostomatoid fungus intera ction recently reported from Protea
infructescences [116] indicat es that such complex asso ciations involving mites are not limited to bark
beetle systems.
Some natural enemies of bark beetles also interact , at least indirectly, with bark beetle-associated
fungi. In the Ips pini—O. ips and the D. ponderosae-O. montium-G. clavigera systems, parasitoids are
attracted to fungus-colonized tree tissues and apparently use fungus -produced volatiles for locating
beetle larvae and pupae [142,143]. In contrast, in the D. frontalis -fungus symbiosis, fungi were not
required for attraction to occur [ 144]. Whether such exploitation of fungal symbionts by parasitoids to
locate hosts affects beetle or fungal fitness or population dynamics is unknown.
3.4. Temperature
Fungi are extremely sensitive to temperature and mo st species grow only within a relatively narrow
range of temperatures. Optimal growth temperatur es and ranges of temperatures supporting growth
vary substantially among species. Such differences can greatly affect the di stribution of fungi, their
relative prevalence, and the outcome of competitive interactions when fung i occur together in a substrate.
For example, Six and Bentz [115] found that temperature plays a key role in determining the relative
abundance of the two symbiotic f ungi associated with dispersing D. ponderosae . The two fungi
possess different optimal growth temperatures . When temperatures are relatively warm, O. montium is
dispersed by new adult beetles, but when temperatures are cool, G. clavigera is dispersed. Shifts in the
prevalence of the two fungi proba bly reflect the effects of temp erature on sporulation in pupal
chambers when brood adults eclose, begin to feed, and pack their mycangia with spores. The two fungi
are not highly antagonistic to one another when grown in culture [145] and are often observed or
isolated together from phloem or from the same pupal chamber [71,146,147]. The ability of these
species to intermingle in tree substrates, and the rarity of fungus-free dispersi ng beetles, indicates that

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both fungi are probably present in many pupal ch ambers, but that depending upon temperature,
typically only one will sporulate and be acquired in mycangia at a particular point in time. This
determines which fungus is disper sed to the next tree and the next generation of beetles, with
substantial implications for the f itness of both beetles and fungi.
Significant effects of temperature on interactions between D. frontalis and its two mycangial fungi,
and an antagonistic phoretic fungus (associated with mites phoretic on D. frontalis ) were also
observed. The relative abundance of the two mycangial fungi of D. frontalis changes seasonally, with
Entomocorticium sp. A prevailing in winter and C. ranaculosus in summer [84]. Their relative
frequency was significantly affected by temperature. Increased temperatures probably decreases beetle
reproduction directly through effects on the physiol ogy of progeny and indirect ly through effects on
mycangial fungi. Entomocorticium performs poorly at higher temperatures while C. ranaculosus
is unaffected.
4. Stability and Redundancy in Multipartite Systems
Symbioses, particularly mutualisms, are predicted to be inherently unstable and prone to erosion
because of cheating by established symbionts or inva sion by exploiters [148]. This may be especially
true for multipartite symbioses, such as most bark beetle-fungus symbioses, where interactions among
symbionts may also affect stability. Many fungal associ ates of bark beetles are phylogenetically related
and have similar life histories. They are introduced into trees by the host beetle , are thought to use the
same resources within the tree, and potentially compete for the same space, and ultimately, for the
same host beetles when it comes time for dispersal. Thus, the multiple fungal associates of beetle
species appear to occupy essentially the same niche. This should result in strong direct competition
among symbionts, leading to repl acement of weaker competitors by stronger competitors. Moreover,
for mutualisms, different symbionts, being different organisms, are not expected to provide exactly the
same degree of benefit to the host. Therefore, sy mbionts that provide inferior benefits should be
selected against, and superior sy mbionts should move toward fixa tion with the host. Despite these
predictions, many multiple-partner associations have apparently been relatively stable for long periods
of evolutionary time [102], indicati ng the existence of factors or m echanisms that contribute to
their stability.
Questions of how and why a host maintains two or more mutualistic symbionts are particularly
interesting. At first glance, inferior symbionts appear to be inherently detrimental to the host because
they displace the more beneficial symbiont(s) from a proportion of the host population. This should
lower the fitness of individual hosts relative to thos e with superior symbionts. This may be especially
important for aggressive beetle species that mass a ttack trees, and whose succe ss ultimately is linked to
host population size.
When considering which symbionts are superior, it is important to remember that roles and intensities
of effects vary with environmental conditions. Envi ronmental heterogeneity is a fundamental attribute
of biological communities [149], and the function of any given species can vary considerably across
natural gradients, both within a community and among different communities [150] . This variability in
function as conditions change has been called ‘context dependency’ [1 51]. Gradients of temperature,
moisture, and other environmental variables comprise the essential axes of species’ ecological niches

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and these factors exert major influences on the ecol ogical performance of orga nisms in nature [152].
Within the geographic range of an organism, some c onditions will be more suitable for survival growth
and reproduction. This means that so me symbionts that are ecologically extraneous (or inferior) at one
point on a multifactoral environmental gradient may be essential (or superior) at another.
Symbionts associated with a bee tle can appear to occupy a comm on niche when in actuality the
niches may differ greatly. Each pa rtner in these symbioses responds differently to the same set of
environmental gradients. This may translate to relatively large differences in the effectiveness of different symbiont genotypes (differe nt species or strains of one sp ecies) under different environmental
conditions. Furthermore, if shifts in the enviro nment are unpredictable or rapid relative to the
generation time of the host, then host specialization on one symbiont may not be favored. Under such
circumstances, multiple symbionts may be advantageous, because they increase the chance that at least
one symbiont partner is effective under a ny prevailing set of environmental conditions.
For example, as reviewed above, the two fungi associated with D. ponderosae possess different
temperature tolerances [115,153,154]. These differences determine which fungus is vectored by
dispersing host beetles as temper atures fluctuate over a season. This temperature-driven symbiont
shifting may provide a mechanism that has allowed bot h fungi to persist in a long-term symbiosis with
their host. By growing at different temperatures, and thus at diffe rent times, the fungi minimize
competition with one another except at a narrow range of temperatures where th e growth of both fungi
is equally supported. In tu rn, the beetle may benefit by reduci ng its risk of being ‘left alone’ by
exploiting not one, but two symbionts, whose co mbined growth optima span a wide range of
environmental conditions. Fo r bark beetles, such as D. ponderosae , which inhabit a broad geographic
range and highly variable habitats, possessing mu ltiple symbionts may be especially important.
It may be useful to view multip artite symbioses from the persp ective of functional redundancy. The
idea that many species in ecosystems perform the sa me or very similar f unctions (members of a
functional group) has been used ex tensively in conservation theory [155]. The concept of functional
redundancy suggests that the presence of a diversity of f unctionally equivalent species enhances the
resilience of an ecosystem and its ability to functi on after perturbation [155]. Th is concept may also be
applicable to symbioses, especially ectosymbioses , where hosts often have multiple symbionts that
fulfill similar roles (symbiont redundancy) and wher e both partners are exposed to vagaries of the
environment. Symbiont redundancy may contribute to resilience and help maintain functions in
symbioses that occur in variable habitats where one symbiont alone may not su ffice. Symbionts in the
same ‘functional group’ may be redundant in the re sources provided to a hos t, but possess different
responses along environmental gradients, allowing th e symbiont community as a whole to respond to
changes in the environment that occur bot h seasonally and from year to year.
5. Conclusions and Future Directions
Symbioses between Scolytinae and fungi are co mplex, varied and still poorly understood. While
our understanding of these systems remains rudimentary, the recent revival of interest in them has led
to a rapid accumulation of information. Molecular taxonomic tools have enabled researchers to
accurately identify fungal partners a nd to resolve phylogenetic relationshi ps of beetles and fungi alike.
This renaissance emerged because of the willingness of investigators to test new paradigms and to

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apply ecological and evolutionary theory to these in teractions. Because of this , the near future should
be a very exciting period, moving us rapidly to ward an integrated understanding of how these
organisms interact with each other and the envir onment, revealing how their interactions have
developed and been maintained over time.
Acknowledgements
Many thanks to Aaron Adams, Stan Barras, Roge r Beaver, and Kier Klep zig for their thoughtful
comments on an earlier draft of this chapter. Special thanks to Mike Wingfield for many lively discussions on this topic.
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