Abstract
The successful establishment of bark beetle–fungus symbionts on plants is required to overcome host defenses. However, little is known about how different bark beetle–fungus symbionts adapt to different niches on the same host plant. Here, we investigated the niche partitioning mechanism of two co-occurring bark beetle–fungus symbiotic systems, Ips nitidus–Ophiostoma bicolor and Dendroctonus micans–Endoconidiophora laricicola, on Qinghai spruce (Picea crassifolia) tree. The lower niche of the spruce trunk inhabited by D. micans showed a higher content of monoterpenes than the upper niche of the trunk inhabited by I. nitidus. Dendroctonus micans showed greater tolerance and higher metabolic efficiency toward monoterpenes than I. nitidus. However, both beetle species showed a similar metabolic profile toward α-pinene, albeit with different levels of metabolites. Additionally, O. bicolor, transmitted by I. nitidus, showed a significantly higher tolerance to monoterpenes and pathogenicity to spruce trees than E. laricicola, transmitted by D. micans. In particular, monoterpenoid metabolites were observed to attenuate the inhibitory effect of high-dose α-pinene on E. laricicola, thus increasing its fitness in a high-dose monoterpene microhabitat. These results show that these two bark beetle–fungus symbionts have adapted to different niches, leading to fitness differences in niche distribution that are at least partly related to the different distribution of monoterpene concentration in the spruce trunk. This research provides a novel perspective for understanding the coevolution between bark beetle–fungus symbionts and their host plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data generated and analyzed in this study are available from the corresponding author upon request.
References
Agbulu V, Zaman R, Ishangulyyeva G, Cahill JF, Erbilgin N (2022) Host defense metabolites alter the interactions between a bark beetle and its symbiotic fungi. Microb Ecol 84(3):834–843. https://doi.org/10.1007/s00248-021-01894-6
Behmer ST, Joern A (2008) Coexisting generalist herbivores occupy unique nutritional feeding niches. Proc Natl Acad Sci 105(6):1977–1982. https://doi.org/10.1073/pnas.0711870105
Birgersson G, Schlyter F, Löfqvist J, Bergström G (1984) Quantitative variation of pheromone components in the spruce bark beetle Ips typographus from different attack phases. J Chem Ecol 10(7):1029–1055. https://doi.org/10.1007/BF00987511
Boone CK, Aukema BH, Bohlmann J, Carroll AL, Raffa KF (2011) Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Can J Res 41(6):1174–1188. https://doi.org/10.1139/x11-041
Byers JA (1981) Pheromone biosynthesis in the bark beetle, Ips paraconfusus, during feeding or exposure to vapours of host plant precursors. Insect Biochem 11(5):563–569. https://doi.org/10.1016/0020-1790(81)90024-X
Cale JA, Muskens M, Najar A, Ishangulyyeva G, Hussain A, Kanekar SS, Klutsch JG, Taft S, Erbilgin N (2017) Rapid Monoterpene induction promotes the susceptibility of a novel host pine to mountain pine beetle colonization but not to beetle–vectored fungi. Tree Physiol 37(12):1597–1610. https://doi.org/10.1093/treephys/tpx089
Chang R, Duong TA, Taerum SJ, Wingfield MJ, Zhou X, de Beer ZW (2020) Ophiostomatoid fungi associated with mites phoretic on bark beetles in Qinghai, China. IMA Fungus 11(1). https://doi.org/10.1186/s43008-020-00037-9
Chen GF, Song YS, Wang PX, Chen JY, Zhang Z, Wang SM, Huang XB, Zhang QH (2015) Semiochemistry of Dendroctonus Armandi Tsai and Li (Coleoptera: Curculionidae: Scolytinae): both femaleproduced aggregation pheromone and host tree kairomone are critically important. Chemoecology 25(3):135–145. https://doi.org/10.1007/s00049-014-0182-1
Chiu CC, Keeling CI, Bohlmann J (2018) Monoterpenyl esters in juvenile mountain pine beetle and sex-specific release of the aggregation pheromone trans-verbenol. Proc Natl Acad Sci 115(14):3652–3657. https://doi.org/10.1073/pnas.1722380115
Erbilgin N (2019) Phytochemicals as mediators for host range expansion of a native invasive forest insect herbivore. New Phytol 221(3):1268–1278. https://doi.org/10.1111/nph.15467
Erbilgin N, Ma C, Whitehouse C, Shan B, Najar A, Evenden M (2014) Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naive host ecosystem. New Phytol 201(3):940–950. https://doi.org/10.1111/nph.12573
Everaerts C, Grégoire JC, Merlin J (1988) The toxicity of norway spruce monoterpenes to two bark beetle species and their associates. In: W. J. Mattson, J. Levieux, C. Bernard-Dagan (eds.) Mechanisms of woody plant defenses against insects, Springer New York, pp 335–344
Faccoli M, Blaženec M, Schlyter F (2005) Feeding response to host and nonhost compounds by males and females of the spruce bark beetle Ips typographus in a tunneling microassay. J Chem Ecol 31(4):745–759. https://doi.org/10.1007/s10886-005-3542-z
Fang JX, Liu M, Zhang SF, Liu F, Zhang Z, Zhang QH, Kong XB, Foyer C (2020a) Chemical signal interactions of the bark beetle with fungal symbionts, and host/non-host trees. J Exp Bot 71(19):6084–6091. https://doi.org/10.1093/jxb/eraa296
Fang JX, Zhang SF, Liu F, Cheng B, Zhang Z, Zhang QH, Kong XB (2020b) Functional investigation of monoterpenes for improved understanding of the relationship between hosts and bark beetles. J Appl Entomol 145(4):303–311. https://doi.org/10.1111/jen.12850
Fang JX, Du HC, Shi X, Zhang SF, Liu F, Zhang Z, Zu PJ, Kong XB (2021) Monoterpenoid signals and their transcriptional responses to feeding and juvenile hormone regulation in bark beetle Ips hauseri. J Exp Biol 224(9):jeb238030. https://doi.org/10.1242/jeb.238030
Francke W, Vité JP (1983) Oxygenated terpenes in pheromone systems of bark beetles. Z Angew Entomol 96(1–5):146–156. https://doi.org/10.1111/j.1439-0418.1983.tb03655.x
Heidel-Fischer HM, Vogel H (2015) Molecular mechanisms of insect adaptation to plant secondary compounds. Curr Opin Insect Sci 8:8–14. https://doi.org/10.1016/j.cois.2015.02.004
Köhler A, Maag D, Veyrat N, Glauser G, Wolfender JL, Turlings TCJ, Erb M (2015) Within-plant distribution of 1,4-benzoxazin-3-ones contributes to herbivore niche differentiation in maize. Plant Cell Environ 38(6):1081–1093. https://doi.org/10.1111/pce.12464
Kursar TA, Dexter KG, Lokvam J, Pennington RT, Richardson JE, Weber MG, Murakami ET, Drake C, McGregor R, Coley PD (2009) The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc Natl Acad Sci 106(43):18073–18078. https://doi.org/10.1073/pnas.0904786106
Libbey LM, Ryker LC, Yandell KL (1985) Laboratory and field studies of volatiles released by Dendroctonus ponderosae Hopkins (Coleoptera, Scolytidae). J Appl Entomol 100(1–5):381–392. https://doi.org/10.1111/j.1439-0418.1985.tb02795.x
Lieutier F, Vouland G, Pettinetti M, Garcia J, Romary P, Yart A (1992) Defence reactions of Norway spruce (Picea abies Karst.) To artificial insertion of Dendroctonus micans Kug. Scolytidae) J Appl Entomol 114(1–5):174–186. https://doi.org/10.1111/j.1439-0418.1992.tb01112.x. Col.
Liu L, Yan W, Luo YQ, Wu J, Li ZY, Ma JH (2007) Spatial niches of bark beetle population in Picea crassifolia natural forests. J Beijing For Univ 29(5): 165–169 (in Chinese). https://doi.org/10.13332/j.1000-1522.2007.05.030
Liu F, Fang JX, Kong XB, Zhang SF, Zhang Z (2020) Stereospecific synthesis of S-(–)-trans-verbenol and its antipode by inversion of sterically hindered alcohols. J Asian Nat Prod Res 24(6):569–576. https://doi.org/10.1080/10286020.2020.1839433
Liu Y, Anastacio GR, Ishangulyyeva G, Rodriguez-Ramos JC, Erbilgin N (2021) Mutualistic ophiostomatoid fungi equally benefit from both a bark beetle pheromone and host tree volatiles as nutrient sources. Microb Ecol 81(4):1106–1110. https://doi.org/10.1007/s00248-020-01661-z
Lu M, Wingfield MJ, Gillette NE, Mori SR, Sun JH (2010) Complex interactions among host pines and fungi vectored by an invasive bark beetle. New Phytol 187(3):859–866. https://doi.org/10.1111/j.1469-8137.2010.03316.x
Menkis A, Lynikienė J, Marčiulynas A, Gedminas A, Povilaitienė A (2016) The great spruce bark beetle (Dendroctonus micans Kug.) (Coleoptera: Scolytidae) in Lithuania: occurrence, phenology, morphology and communities of associated fungi. Bull Entomol Res 107(4):431–438. https://doi.org/10.1017/s0007485316001048
Moreira X, Lundborg L, Zas R, Carrillo-Gavilán A, Borg-Karlson AK, Sampedro L (2013) Inducibility of chemical defences by two chewing insect herbivores in pine trees is specific to targeted plant tissue, particular herbivore and defensive trait. Phytochemistry 94:113–122. https://doi.org/10.1016/j.phytochem.2013.05.008
Pansu J, Hutchinson MC, Anderson TM et al (2022) The generality of cryptic dietary niche differences in diverse large-herbivore assemblages. Proc Natl Acad Sci 119(35):e2204400119. https://doi.org/10.1073/pnas.2204400119
Pierce HD, Conn JE, Oehlschlager AC, Borden JH (1987) Monoterpene metabolism in female mountain pine beetles, Dendroctonus ponderosae Hopkins, attacking Ponderosa pine. J Chem Ecol 13(6):1455–1480. https://doi.org/10.1007/bf01012291
Raffa KF, Powell EN, Townsend PA (2013) Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses. Proc Natl Acad Sci 110(6):2193–2198. https://doi.org/10.1073/pnas.1216666110
Redfern DB, Stoakley JT, Steele H, Minter DW (1987) Dieback and death of larch caused by ceratocystis laricicola sp. nov. Following attack by Ips cembrae. Plant Pathol 36(4):467–480. https://doi.org/10.1111/j.1365-3059.1987.tb02264.x
Schlyter F, Birgersson G, Byers JA, Bakke A (1992) The aggregation pheromone of Ips duplicatus and its role in competitive interactions with I. typographus (Coleoptera: Scolytidae). Chemoecology 3(3): 103–112. https://doi.org/10.1007/bf01370137
Schlyter F, Jakuš R, Han FZ, Ma JH, Kalinová B, Mezei P, Sun JH, Ujhelyiová L, Zhang QH (2015) Reproductive isolation of Ips Nitidus and I. Shangrila in mountain forests of western China: responses to chiral and achiral candidate pheromone components. J Chem Ecol 41(7):678–688. https://doi.org/10.1007/s10886-015-0594-6
Seybold SJ, Huber DPW, Lee JC, Graves AD, Bohlmann J (2006) Pine monoterpenes and pine bark beetles: a marriage of convenience for defense and chemical communication. Phytochem Rev 5(1):143–178. https://doi.org/10.1007/s11101-006-9002-8
Shi ZH, Sun JH (2010) Quantitative variation and biosynthesis of hindgut volatiles associated with the red turpentine beetle, Dendroctonus valens LeConte, at different attack phases. Bull Entomol Res 100(3):273–277. https://doi.org/10.1017/s0007485309990228
Shi X, Fang J, Du H, Zhang S, Liu F, Zhang Z, Kong X (2022) Performance of two Ips bark beetles and their associated pathogenic fungi on hosts reflects a species-specific association in the beetle–fungus complex. Front Plant Sci 13:1029526. https://doi.org/10.3389/fpls.2022.1029526
Six DL (2012) Ecological and evolutionary determinants of bark beetle–fungus symbioses. Insects 3(1):339–366. https://doi.org/10.3390/insects3010339
Six DL (2020) Niche construction theory can link bark beetle–fungus symbiosis type and colonization behavior to large scale causal chain-effects. Curr Opin Insect Sci 39:27–34. https://doi.org/10.1016/j.cois.2019.12.005
Solheim H, Krokene P, Långström B (2001) Effects of growth and virulence of associated blue-stain fungi on host colonization behaviour of the pine shoot beetles Tomicus minor and T. Piniperda. Plant Pathol 50(1):111–116. https://doi.org/10.1046/j.1365-3059.2001.00541.x
Tittiger C, Blomquist GJ (2017) Pheromone biosynthesis in bark beetles. Curr Opin Insect Sci 24:68–74. https://doi.org/10.1016/j.cois.2017.09.005
Ullah A, Klutsch JG, Erbilgin N (2021) Production of complementary defense metabolites reflects a co-evolutionary arms race between a host plant and a mutualistic bark beetle–fungal complex. Plant Cell Environ 44(9):3064–3077. https://doi.org/10.1111/pce.14100
Viiri H, Annila E, Kitunen V, Niemelä P (2001) Induced responses in stilbenes and terpenes in fertilized norway spruce after inoculation with blue-stain fungus, Ceratocystis Polonica. Trees 15(2):112–122. https://doi.org/10.1007/s004680000082
Wang Z, Zhou Q, Zheng G, Fang J, Han F, Zhang X, Lu Q (2021) Abundance and diversity of Ophiostomatoid fungi associated with the great spruce bark beetle (Dendroctonus micans) in the Northeastern Qinghai–Tibet Plateau. Front Microbiol 12:721395. https://doi.org/10.3389/fmicb.2021.721395
Wang Z, Liu Y, Wang H, Roy A, Liu H, Han F, Zhang X, Lu Q (2023) Genome and transcriptome of Ips nitidus provide insights into high-altitude hypoxia adaptation and symbiosis. 26(10):107793. https://doi.org/10.1016/j.isci.2023.107793
Yin M, Wingfield MJ, Zhou X, de Beer ZW (2016) Multigene phylogenies and morphological characterization of five new Ophiostoma Spp. Associated with spruce-infesting bark beetles in China. Fungal Biol 120(4):454–470. https://doi.org/10.1016/j.funbio.2015.12.004
Zhang QH, Ma JH, Zhao FY, Song LW, Sun JH (2009) Aggregation pheromone of the Qinghai spruce bark beetle, Ips Nitidus Eggers. J Chem Ecol 35(5):610–617. https://doi.org/10.1007/s10886-009-9634-4
Zhao T, Kandasamy D, Krokene P, Chen J, Gershenzon J, Hammerbacher A (2018) Fungal associates of the tree-killing bark beetle, Ips typographus, vary in virulence, ability to degrade conifer phenolics and influence bark beetle tunneling behavior. Fungal Ecol 38:71–79. https://doi.org/10.1016/j.funeco.2018.06.003
Acknowledgements
We acknowledge the anonymous reviewers and subject editor for their constructive comments and help with revising this manuscript. We would also like to thank Nanjie Wanma and Jianyuan Ma (Maixiu Forest Farm of Huangnan Prefecture) for their assistance with fieldwork.
Funding
This work was funded by the National Natural Science Foundation of China (Project no. 32301601).
Author information
Authors and Affiliations
Contributions
XBK and JXF conceived the research. ZZB and JXF performed toxicological tests and chemical analyses, analyzed data and drafted the manuscript. FL synthesized the chemical standards. JXF, ZZB, CMY, FZH, GRZ and JHM carried out the field work. XBK and SFZ revised the manuscript and provided constructive comments. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Ethics Approval
Not applicable.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bai, Z., Fang, J., Yu, C. et al. Divergent Response of Two Bark Beetle–Fungal Symbiotic Systems to Host Monoterpenes Reflects Niche Partitioning Strategies. J Chem Ecol (2024). https://doi.org/10.1007/s10886-024-01535-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10886-024-01535-5