Context-dependent interactions of insects and defensive symbionts: insights from a novel system in siricid woodwasps

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ScienceDirect Context-dependent interactions of insects and defensive symbionts: insights from a novel system in siricid woodwasps Ann E Hajek1, Elizabeth Erin Morris2 and Tory A Hendry3 Many insect species derive fitness benefits from associations with defensive microbial symbionts that confer protection against pathogens and parasites. These relationships are varied and diverse, but a number of studies highlight important trends. The effects of defensive symbionts can be contextdependent and influenced by variable selection imposed by the organism against which the symbiont protects. Additionally, genetic variation in both hosts and symbionts can greatly influence the outcome of these interactions. Here, we describe interactions between siricid woodwasps, their fungal symbionts and parasitic nematodes and show how defense by symbionts in this system is also context-dependent. The species or strain of the white rot fungus used as a symbiont by Sirex can influence parasitism of these hosts by Deladenus nematodes. Addresses 1 Department of Entomology, Cornell University, Ithaca, NY 14853-2601, USA 2 Department of Biological Sciences, University of New Hampshire, Durham, NH 03823, USA 3 Department of Microbiology, Cornell University, Ithaca, NY 14853, USA Corresponding author: Hajek, Ann E ([email protected])

Current Opinion in Insect Science 2019, 33:77–83 This review comes from a themed issue on Pests and resistance Edited by Jørgen Eilenberg and Ann E Hajek For a complete overview see the Issue and the Editorial Available online 3rd April 2019 https://doi.org/10.1016/j.cois.2019.03.006 2214-5745/ã 2019 Published by Elsevier Inc.

Introduction Resistance to natural enemies is critically important for survival of insects. For many insects, bacterial or fungal symbionts can provide a fitness advantage by protecting hosts from pathogens, as well as parasites like parasitoid wasps or parasitic nematodes. Extreme diversity exists in the relationships between insects and defensive symbionts; the phylogenetic identity of the symbiont varies, as does the type of protection conferred, where the symbiont is located in relation to the host, and how the symbiont is transmitted to new hosts [for reviews www.sciencedirect.com

see Refs. 1–3]. Although common themes have been developed from these examples, two observations show the importance of continued exploration across a breadth of diverse symbionts and hosts. One emerging point is that the effects of a given symbiont on a given host are often context-dependent [4,5,6], making it difficult to predict when symbionts will be protective. Another observation is that research continues to uncover novel defensive symbioses, each of which improves our understanding of protective host-microbe interactions [3]. Here we review how defensive symbioses are often context-dependent in their effects and we highlight this trend with examples from interactions between woodwasps (Siricidae), their fungal symbionts, and parasitic nematodes.

Defensive microbial symbionts of insects Insects are commonly associated with microorganisms that act as mutualistic symbionts [7,8]. Symbionts can be obligately required by the host for development or reproduction, or facultatively associated with hosts. Obligate symbionts often fulfill a nutritional role, such as the bacterial aphid primary symbiont Buchnera aphidicola, that is required for reproduction and which synthesizes amino acids that are missing in the host’s diet [9,10], or symbionts in termite guts that digest recalcitrant plant material [11]. Facultative symbionts may only be beneficial in some contexts. For instance, pea aphids, Acyrthosiphon pisum, associate with at least eight species of bacterial secondary symbionts that are not required for reproduction, and which provide diverse benefits ranging from heat tolerance to protection against pathogens or parasitoid wasps [11]. A growing number of studies suggest that such protective symbiotic interactions are quite common in nature [12]. Insect symbionts conferring protection from pathogens, parasites and parasitoids include those living in all kinds of associations: intracellular endosymbionts as well as extracellular symbionts such as gut symbionts and external ectosymbionts (Figure 1; Table 1). Although mainly bacteria have been identified in these roles, some extracellular protective fungal symbionts have been found. These examples show protection from a diversity of natural enemies, including for example fungal pathogens [4,21–23,29], bacterial pathogens [25,32,33], RNA viruses [26–28,29,30], parasitic nematodes [14], trypanosomes [34], and parasitoid wasps [5,17]. Current Opinion in Insect Science 2019, 33:77–83

78 Pests and resistance

Figure 1

Sirex

Deladenus

wasp larvae feed on fungus-decayed wood; female adult wasps vector the fungus, and can vector the nematodes (which may or may not sterilize the wasp)

+

– +

parasitic form: infests wasp larvae, and is vectored by female adult wasps; mycophagous form: feeds on the fungus

– +

+

Amylostereum wood-decaying fungus Current Opinion in Insect Science

Interactions between Sirex woodwasps, their symbiotic nutritional white rot fungi (Amylostereum), and parasitic nematodes (Deladenus). The nematodes are dimorphic, with mycophagous stages that specifically eat the same white rot fungi associated with Sirex and parasitic stages that live within Sirex larvae. The parasitic nematodes do not usually kill the Sirex larvae, instead sometimes sterilizing the females once they become adult, and the nematodes are then vectored to new trees by ovipositing females.

Protective symbioses are often context-dependent Some protective symbionts are frequently found associated with their hosts, whereas others show patchy distributions across individuals, both within and between populations. This is thought to be related to the distribution of the particular enemy, which leads to selection on symbionts in some, but potentially not all, contexts [42,43]. For instance, antibiotic-producing bacteria on the surfaces of beetle eggs [38] or in the walls of bee wolf cocoons [37] provide generalized protection from pathogens that are common in the soil where these insects are developing, possibly explaining why these hosts have tight associations with their symbionts. In contrast, the presence of protective symbionts in aphids can vary greatly across individuals and populations [12,42]. Laboratory experiments have shown that the presence of parasitoid wasps can select for increased frequencies of the bacterial symbiont Hamiltonella defensa in pea aphids [42]. This experimental work also suggests that symbiont infection may come at a cost when parasitoids are absent [5,13]. This is further supported by the fact that aphids that are tended by ants that protect them from parasitoids tend to have fewer protective symbionts [43]. Therefore, the biotic environment of an individual insect influences whether a given protective symbiont will provide a fitness advantage or not, and can lead to spatial heterogeneity in symbiont distributions. Current Opinion in Insect Science 2019, 33:77–83

The specific identity of both the symbiont and the enemy can also influence the ultimate outcome of protective symbioses. For instance, H. defensa strains (=genotypes) vary in their ability to protect aphids against parasitoids due to differences in phage toxins encoded in the symbiont’s genome [44], and variation in defense also depends on which parasitoid species or even genotypes are attacking the host [[45]]. Genotype by genotype interactions have also been found for aphid symbionts that protect against fungal pathogens [6], and in Drosophila, both the host species and specific strain influence whether this symbiont can protect the host against viral pathogens [28,29,30]. Together, these levels of variation create complexity in protective interactions that can cascade across ecological communities [45] and influence biological control applications [[45]]. These trends are highlighted by the relationship between the ectosymbiotic obligate mutualist fungi associated with woodwasps and the protection that some strains of these fungi confer against parasitic nematodes, which we report below.

Woodwasp communities: fungal symbionts and parasitic nematodes Wood-boring insects that must utilize the xylem and phloem of wood as food are well known for obligate relationships with microbial symbionts that facilitate nutrient accessibility from wood. Associations with critically important wood-degrading symbionts are variable. For www.sciencedirect.com

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Table 1 Examples of fungal and bacterial symbionts that provide protection from pathogens and parasitoids for insect hosts Symbiont group a

Symbiont

Insect Order and Family

Insect host(s)

Protective activity

Reference

Bacteria, Endo

Spiroplasma poulsonii

Diptera, Drosophilidae

Drosophila neotestacea

[14–16]

Bacteria, Endo

Hamiltonella defensa, Serratia symbiotica, Regiella insecticola

Hemiptera, Aphididae

Acyrthosiphuon pisum, Myzus persicae, Aphis fabae

Bacteria, Endo

Hemiptera, Aphididae

Acyrthosiphuon pisum

Hemiptera, Aphididae

Acyrthosiphuon pisum

Protection from the fungal entomopathogen Pandora neoaphidis

[24]

Bacteria, Endo

Regiella insecticola, Rickettsiella viridis, Rickettsia, and Spiroplasma Co-infection by Fukatsuia symbiotica (=X-type) and Spiroplasma Rickettsia

Nematode Howardula aoronymphium does not sterilize hosts and nematode reproduction decreases; toxin implicated Protection from parasitoid wasps such as Aphidius ervi, Aphidius colemani, and Lysiphlebus fabarum; mechanism of protection known for some strains Protection from the fungal entomopathogen Pandora neoaphidis

Hemiptera, Aleyrodidae

Bemisia tabaci

[25]

Bacteria, Endo

Regiella sp.

Hemiptera, Aphididae

Acyrthosiphon pisum

Bacteria, Endo

Wolbachia pipientis

Diptera, Drosophilidae

Bacteria, Endo

Wolbachia pipientis

Diptera, Drosophilidae

Drosophila melanogaster, D. simulans, D. suzukii Drosophila melanogaster

Bacteria, Gut

Gut bacterial community

Orthoptera, Acrididae

Schistocerca gregaria

Bacteria, Gut

Lactobacillus and Bifidobacterium

Hymenoptera, Apidae

Apis mellifera larvae

Bacteria, Gut

Gut bacterial community

Hymenoptera, Apidae

Bombus terrestris

Bacteria, Gut

Gilliamella sp.

Hymenoptera, Apidae

Bombus spp.

Bacteria, Ecto

Streptomyces spp.

Hymenoptera, Crabronidae

Philanthus triangulum

Bacteria, Ecto

Burkholderia gladioli

Coleoptera, Tenebrionidae

Fungi

Hymenoptera, Apidae

Fungi

Microbial community including Aspergillus spp. and Penicillium sp. Ogataea pini (yeast)

Lagriine beetles (Subfamily Lagriinae) Apis mellifera

Fungi Fungi

Protection from the facultative bacterial entomopathogen Pseudomonas syringae Protection from the fungal entomopathogen Zoophthora occidentalis Defense against Drosophila C virus and other RNA viruses that can be context-dependent Protection against the fungal entomopathogen Beauveria bassiana Inhibition by gut microbiota prevents invasion by Metarhizium robertsii (=anisopliae) through gut Lactic acid bacteria in gut protect against Paenibacillus larvae (American foulbrood) and Melisococcus plutonius (European foulbrood) Reducing load of the parasitic trypanosomatid Crithidia bombi Infection by Crithidia bombi negatively associated with abundance of Gilliamella Antimicrobial defense due to nine symbiontproduced antibiotics in cocoon walls Antimicrobial defense due to antibiotics on egg surfaces protect eggs Yeasts and molds contaminating stored pollen prevented contamination by Ascosphaera apis (fungus causing chalkbrood) Volatiles produced by the yeast inhibited growth of Beauveria bassiana Protection from parasitic nematodes that only feed on A. chailletii Protection from parasitic nematode Deladenus proximus

Bacteria, Endo

Sirex noctilio

Amylostereum areolatum IGS D

Hymenoptera, Siricidae

Sirex nigricornis

Type of symbiosis: Endo = Endosymbiont, Gut = Gut symbiont, Ecto = Ectosymbiont.

Dendroctonus brevicomis

[21–23]

[4] [26–28,29,30] [31] [32]

[33,34]

[35] [36] [37] [38] [39]

[40] [41] This publication

Context dependence of defense by symbionts Hajek, Morris and Hendry 79

Current Opinion in Insect Science 2019, 33:77–83

a

Amylostereum areolatum

Coleoptera, Curculionidae, Scolytinae Hymenoptera, Siricidae

[17–20]

80 Pests and resistance

many hosts, nutritional symbionts occur as part of microbiome communities within their guts. For bark beetles (Coleoptera, Curculionidae, Scolytinae), with larvae developing beneath tree bark, fungal nutritional symbionts are often carried in specialized structures of the exoskeleton called mycangia and are inoculated into or onto wood before or during oviposition [46]. For woodwasps (Hymenoptera, Scolytidae), with immature stages developing within the xylem of trees, fungal nutritional symbionts are carried by adult females within mycangia located at the base of the ovipositor and are inoculated into the xylem before or during oviposition. It was previously thought that woodwasps in the genus Sirex were highly specific regarding the species of fungal symbiont that they used but more recent studies have shown that fungal fidelity can be flexible, although this is species-dependent [47,48]. For example, while Sirex nigricornis and Sirex nitidus are more flexible and can be associated with either the white rot fungi Amylostereum areolatum or Amylostereum chailletii, the woodwasp Sirex noctilio is very specific and is virtually always associated with A. areolatum [48] and only rarely with A. chailletii [49]. Although feeding within wood provides a cryptic and protected habitat, larvae of wood-boring insects are still vulnerable to predation or parasitism by natural enemies. In particular, parasitic nematodes are known from numerous wood borers, e.g., the Deladenus (Tylenchida, Neotylenchidae) nematodes parasitic on Sirex woodwasps. In this complex system, Sirex develop in stressed and/or dying trees, an ephemeral resource. Deladenus are dimorphic, being mycophagous when inserted into a tree during Sirex oviposition. The free-living mycophagous stage undergoes numerous generations while spreading within the tree and only develops into parasitic forms when in proximity with a Sirex larva. When these nematodes are mycophagous, they specifically feed on Amylostereum spp., the symbionts of Sirex. The mycophagous and parasitic forms of Deladenus are so different in appearance (the mycophagous nematodes are much larger while the parasitics have longer stylets) that when first found, they would have been placed in different families [50]. This dimorphic strategy suits the needs of the nematodes: mycophagy allows extensive development and increase of nematodes within trees for many generations, but one stressed and dying tree is a finite and ephemeral habitat and the parasitic form then allows the nematodes to be vectored to a new tree. Free-living mycophagous nematodes develop into a parasitic generation when exposed to high CO2 and low pH in vitro and it is thought that these cues likewise are used by Deladenus within trees [50]. After parasitic Deladenus females bore into a Sirex larva, the nematodes do not kill the host and their juvenile offspring eventually migrate to the reproductive tissues of females. They are then vectored by female Sirex during oviposition in new trees. Nematodes of some strains are Current Opinion in Insect Science 2019, 33:77–83

vectored within Sirex eggs and are therefore sterilizing, while for other strains nematodes are not inside the woodwasp eggs but are on the egg surfaces or in proximity to eggs within woodwasp females and are vectored with accessory fluids during oviposition [51]. Deladenus siricidicola is mass produced and has been used extensively for biological control of the most aggressive species among the woodwasps, the invasive Eurasian S. noctilio, on numerous continents in the Southern Hemisphere where this invasive has been introduced. In accordance with a worldwide survey of Deladenus in the 1960s and 1970s, dimorphic species in this nematode genus are generally considered more specific to the fungal species and strains that they feed on than they are to the Sirex hosts that they parasitize [41]. Flexibility in siricid species hosts parasitized by nematodes has been confirmed in recent years when D. siricidicola was found to parasitize both S. noctilio and S. nigricornis in North America [52,53]. In this instance, D. siricidicola is thought to have evolved with S. noctilio where this invasive originated in Eurasia, and this nematode only encountered the North American native S. nigricornis after having been introduced to North America with S. noctilio [51]. When a Sirex larva is feeding within wood, it is surrounded by or adjacent to its symbiotic fungus, which produces enzymes that degrade the wood that the Sirex will eat; the fungus has thus been referred to as an external rumen [54]. Therefore, the free-living mycophagous stage of Deladenus will remain in the vicinity of a Sirex larva if they feed on the fungus used by that Sirex. Thus, the Amylostereum species or strain being used by the Sirex could also provide protection for the host against Deladenus, if the Sirex uses a fungal species or strain that does not support growth of that nematode.

Fungal symbionts protecting against parasitic nematodes A worldwide survey for nematodes parasitizing siricids was conducted to find nematodes parasitizing the invasive S. noctilio to use for control in the Southern Hemisphere. According to results, Bedding and Akhurst [41] hypothesized that Deladenus species with mycophagous forms that exclusively feed on the fungus Amylostereum chailletii would not parasitize S. noctilio because S. noctilio is virtually always associated with A. areolatum (i.e. S. noctilio larvae are surrounded by A. areolatum (Figure 2a). Thus, being surrounded by a fungal food source that is not suitable for a given Deladenus species could confer protection of S. noctilio from parasitism by that Deladenus. The nematode used for biological control of S. noctilio only feeds on strains of A. areolatum [48,51]. In contrast, the North American nematode species Deladenus proximus has been found to feed on some strains of either A. areolatum or A. chailletii. However, among the strains of A. areolatum in North America we know of one specific fungal strain, www.sciencedirect.com

Context dependence of defense by symbionts Hajek, Morris and Hendry 81

Figure 2

A. chailletii

A. chailletii

A. chailletii

D. beddingi

D. canii

D. nevexii

surrounded by A. areolatum IGS D, on which D. proximus does not survive and reproduce, all or most of these nematodes would not remain in the vicinity of this fungus long enough to form a parasitic generation; therefore, A. areolatum IGS D would provide protection of its host Sirex from D. proximus (Figure 2b).

Summary Sirex noctilio larvae

D. siricidicola

A. areolatum

(a)

A. areolatum

A. chailletii

IGS BD or BE

D. proximus

D. proximus

S. nigricornis larvae

S. nigricornis larvae

S. nigricornis larvae

A. chailletii

A. areolatum

A. areolatum IGS D

IGS BD or BE

(b) Current Opinion in Insect Science

Associations between Sirex and Deladenus, indicating how these can be influenced by the Sirex-symbiotic fungus, Amylostereum. The diagrams indicate how the symbiotic fungus that a Sirex larva is associated with can provide protection when mycophagous stages of nematodes cannot use the same fungus. Red lines indicate associations that will not occur and bolded text indicates fungal species and strains associated with Sirex that prevent nematode parasitism. (a) Sirex noctilio is virtually always associated with A. areolatum (and only very rarely with A. chailletti), so these 3 Deladenus species (beddingi, canii, and nevexii) that are only known to eat A. chailletii will not impact this host. (b) Sirex nigricornis is associated with either A. areolatum or A. chailletii as is its parasite Deladenus proximus. However, we have identified one strain of A. areolatum (IGS D) that the mycophagous forms of this nematode will not use as food. Therefore when an S. nigricornis larvae is associated with A. areolatum IGS D, we hypothesize that D. proximus will not (or will rarely) develop into parasitics in the vicinity of that larva, and the larva will therefore be protected by the fungus occurring around it within the xylem.

A. areolatum IGS D (putatively introduced with S. noctilio), that is a special case. When mycophagous stage D. proximus were only offered A. areolatum IGS D as food, they failed to develop into adults, so no reproduction occurred [55]. In regions where S. noctilio and S. nigricornis infest the same trees, horizontal transmission of fungal symbionts as well as nematodes can occur [48,52,53]. We therefore hypothesize that if the host larvae of either of these Sirex species are www.sciencedirect.com

We have described a system where a fungal symbiont associated with an insect host determines whether a dimorphic nematode will parasitize that host. This adds to the growing diversity of examples of protection of insect hosts by their symbionts. For this system, as well as most others, more research is needed to understand mechanisms of conferred protection and this is likely to be a rich area for future work. Some studies show only correlations between symbionts and effects of pathogens [33], whereas others have hypothesized protection of insect hosts by symbionts using experiments that were conducted in vitro, often because these are difficult systems to investigate [5]. Furthermore, experiments often rely on model pathogens or parasites, rather than understanding which enemies are the most important in nature. Although the woodwasp-fungus mutualism presented here is difficult to study, it indicates the importance of studying diverse systems and genetic diversity across all interacting organisms within a given system. For instance, this system demonstrates how the effects of potentially protective symbionts can be dependent on context. For Sirex, the species or strain of their fungal symbiont can influence, and even determine, whether nematodes will become parasites or not. Including biotic diversity in studies of these fascinatingly complex interactions is therefore important for understanding their ecology, but could also play a role in whether control efforts are successful.

Conflict of interest statement Nothing declared.

Acknowledgements We thank Dr Melanie Smee for comments and suggestions on early versions of the manuscript and Dr Sana Gardescu for assistance with figures. Funding for woodwasp research was provided by the USDA Forest Service.

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50. Bedding RA: Controlling the pine-killing woodwasp, Sirex noctilio, with nematodes. In Use of Microbes for Control and Eradication of Invasive Arthropods. Edited by Hajek AE, Glare TR, O’Callaghan M. Springer; 2009:213-235. 51. Hajek AE, Morris EE: Biological control of Sirex noctilio. In The Use of Classical Biological Control to Preserve Forests in North America. Edited by Van Driesche RG, Reardon R. USDA Forest Service; 2014:331-346.

45. McLean AH: Cascading effects of defensive endosymbionts. Curr Opin Insect Sci 2019, 32:42-46.  This review summarizes the impact of defensive symbionts on insect communities, demonstrating that defensive symbionts can have indirect effects at trophic levels above, below or similar to the insect host.

52. Haavik LJ, Yu Q, Turgeon JJ, Allison JD: Horizontal transmission of a parasitic nematode from a non-native to a native woodwasp? Biol Invasions 2016, 18:355-358.

46. Hofstetter RW, Dinkins-Bookwalter J, Davis TS, Klepzig KD: Symbiotic associations of bark beetles. In Bark Beetles: Biology and Ecology of Native and Invasive Species. Edited by Vega FE, Hofstetter RW. Academic Press; 2015:209-245.

53. Morris EE, Kepler RM, Long SJ, Williams DW, Hajek AE: Phylogenetic analysis of Deladenus nematodes parasitizing northeastern North American Sirex species. J Invertebr Pathol 2013, 113:177-183.

47. Nielsen C, Williams DW, Hajek AE: Putative source of the invasive Sirex noctilio fungal symbiont, Amylostereum areolatum, in the eastern United States and its association with native siricid woodwasps. Mycol Res 2009, 113:1242-1253.

54. Thompson BM, Bodart J, McEwen C, Gruner DS: Adaptations for symbiont-mediated external digestion in Sirex noctilio (Hymenoptera: Siricidae). Ann Entomol Soc Am 2014, 107:453460.

48. Hajek AE, Nielsen C, Kepler RM, Long SJ, Castrillo L: Fidelity among Sirex woodwasps and their fungal symbionts. Microb Ecol 2013, 65:753-762.

55. Morris EE, Hajek AE, Zieman E, Williams DW: Deladenus  (Tylenchida: Neotylenchidae) reproduction on species and strains of the white rot fungus Amylostereum. Biol Control 2014, 73:50-58. This study shows that Amylostereum strains can have enormous impacts on Deladenus fitness, which then impacts whether nematodes will remain around potential hosts long enough to form parasitics.

49. Wooding AL, Wingfield MJ, Hurley BP, Garnas JR, De Groot P, Slippers B: Lack of fidelity revealed in an insect–fungal mutualism after invasion. Biol Lett 2013, 9:20130342.

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Current Opinion in Insect Science 2019, 33:77–83