Abstract
Competitive displacement is not only the most extreme outcome of interspecific competition, but also an important strategy for invasive species to be successful invaders. Pinewood nematode, Bursaphelenchus xylophilus, the causal agent for pine wilt disease and global quarantine pest, usually displaces Bursaphelenchus mucronatus, a native sympatric sibling species, during its invasion process. Despite this prevalent outcome, the driving forces behind this displacement remain elusive. Ascarosides, an evolutionarily conserved family of nematode pheromones, are versatile in structure and function. We hypothesize these nematode pheromones play a role in species displacement. To investigate this hypothesis, we compared the ascarosides composition of B. xylophilus and B. mucronatus by LC–MS/MS followed by bioassays to test the responses of two nematodes to both crude and synthetic ascarosides. We found that asc-C5 (ascr#9) was the most abundant component and that there were no differences in pheromone composition between the two nematode species. B. xylophilus had faster growth rates under competition conditions. Furthermore, low concentrations of both crude and synthetic ascarosides [asc-C5, asc-C6 (ascr#12) and their mixture] enhanced female fecundity and body length growth in B. xylophilus but not in B. mucronatus. In contrast, body length of B. mucronatus was suppressed by a crude extract of its own ascarosides as well as by synthetic ascarosides (asc-C5, asc-C6 and their mixture). Our results strongly suggest that ascarosides play a role in the competitive displacement between two nematode species, which could explain the phenomena observed in B. xylophilus-invaded forests where B. mucronatus widely existed prior to B. xylophilus invasion.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amo L, Bonadonna F (2018) The importance of olfaction in intra-and interspecific communication. Front Ecol Evol 6:71. https://doi.org/10.3389/fevo.2018.00071
Ayala FJ (1971) Competition between species: frequency dependence. Science 171(3973):820–824. https://doi.org/10.1126/science.171.3973.820
Berenbaum MR (2016) Are mammals just furry bugs with fewer legs? Convergences in mammalian and insect chemical ecology. Chemical signals in vertebrates 13. Springer, Cham, pp 3–10
Blueweiss L, Fox H, Kudzma V, Nakashima D, Peters R, Sams S (1978) Relationships between body size and some life history parameters. Oecologia 37(2):257–272. https://doi.org/10.1007/BF00344996
Braendle C (2012) Pheromones: evolving language of chemical communication in nematodes. Curr Biol 22(9):R294–R296. https://doi.org/10.1016/j.cub.2012.03.035
Butcher RA, Fujita M, Schroeder FC, Clardy J (2007) Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat Chem Biol 3(7):420–422. https://doi.org/10.1038/nchembio.2007.3
Butcher RA, Ragains JR, Kim E, Clardy J (2008) A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components. Proc Natl Acad Sci U S A 105(38):14288–14292. https://doi.org/10.1073/pnas.0806676105
Butcher RA, Ragains JR, Clardy J (2009) An indole-containing dauer pheromone component with unusual dauer inhibitory activity at higher concentrations. Org Lett 11(14):3100–3103. https://doi.org/10.1021/ol901011c
Cheng XY, Xie PZ, Cheng FX, Xu RM, Xie BY (2009) Competitive displacement of the native species Bursaphelenchus mucronatus by an alien species Bursaphelenchus xylophilus (Nematoda: Aphelenchida: Aphelenchoididae): a case of successful invasion. Biol Invasions 11(2):205–213. https://doi.org/10.1007/s10530-008-9225-2
Choe A, Chuman T, Von Reuss SH, Dossey AT, Yim JJ, Ajredini R, Kolawa AA, Kaplan F, Alborn HT, Teal PEA, Schroeder FC, Sternberg PW, Schroeder FC (2012a) Sex-specific mating pheromones in the nematode Panagrellus redivivus. Proc Natl Acad Sci U S A 109(51):20949–20954. https://doi.org/10.1073/pnas.1218302109
Choe A, Von Reuss SH, Kogan D, Gasser RB, Platzer EG, Schroeder FC, Sternberg PW (2012b) Ascaroside signaling is widely conserved among nematodes. Curr Biol 22(9):772–780. https://doi.org/10.1016/j.cub.2012.03.024
Conover RJ (1988) Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiologia 167(1):127–142. https://doi.org/10.1007/BF00026299
De Guiran G, Bruguier N (1989) Hybridization and phylogeny of the pine wood nematode (Bursaphelenchus Spp). Nematologica 35(3):321–330. https://doi.org/10.1163/002825989X00421
Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost-benefit analysis rather than origin of compounds? Funct Ecol. https://doi.org/10.2307/2389687
Ekesi S, Billah MK, Nderitu PW, Lux SA, Rwomushana I IV (2009) Evidence for competitive displacement of Ceratitis cosyra by the invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) on mango and mechanisms contributing to the displacement. J Econ Entomol 102(3):981–991. https://doi.org/10.1603/029.102.0317
Evenden ML, Silk PJ (2016) The influence of Canadian research on semiochemical-based management of forest insect pests in Canada. Can Entomol 148(S1):S170–S209. https://doi.org/10.4039/tce.2015.17
Gao Y, Reitz SR (2017) Emerging themes in our understanding of species displacements. Annu Rev Entomol 62:165–183. https://doi.org/10.1146/annurev-ento-031616-035425
Greene JS, Brown M, Dobosiewicz M, Ishida IG, Macosko EZ, Zhang XX, Butcher RA, Cline DJ, McGrath PT, Bargmann CI (2016) Balancing selection shapes density-dependent foraging behaviour. Nature 539(7628):254. https://doi.org/10.1038/nature19848
Günther CS, Goddard MR, Newcomb RD, Buser CC (2015) The context of chemical communication driving a mutualism. J Chem Ecol 41(10):929–936. https://doi.org/10.1007/s10886-015-0629-z
Haldane JBS (1955) Animal communication and the origin of human language. Sci Prog 43(171):385–401
Hartley CJ, Lillis PE, Owens RA, Griffin CT (2019) Infective juveniles of entomopathogenic nematodes (Steinernema and Heterorhabditis) secrete ascarosides and respond to interspecific dispersal signals. J Invertebr Pathol 168:107257. https://doi.org/10.1016/j.jip.2019.107257
Izrayelit Y, Srinivasan J, Campbell SL, Jo Y, von Reuss SH, Genoff MC, Sternberg PW, Schroeder FC (2012) Targeted metabolomics reveals a male pheromone and sex-specific ascaroside biosynthesis in Caenorhabditis elegans. ACS Chem Biol 7(8):1321–1325. https://doi.org/10.1021/cb300169c
Jeong PY, Jung M, Yim YH, Kim H, Park M, Hong E, Lee W, Kim YH, Kim K, Paik YK (2005) Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433(7025):541. https://doi.org/10.1038/nature03201
Jikumaru S, Togashi K (2004) Inhibitory effect of Bursaphelenchus mucronatus (Nematoda: Aphelenchoididae) on B. xylophilus boarding adult Monochamus alternatus (Coleoptera: Cerambycidae). J Nematol 36(1):95
Kajita Y, Evans EW (2010) Relationships of body size, fecundity, and invasion success among predatory lady beetles (Coleoptera: Coccinellidae) inhabiting alfalfa fields. Ann Entomol Soc Am 103(5):750–756. https://doi.org/10.1603/AN10071
Kaplan F, Alborn HT, Von Reuss SH, Ajredini R, Ali JG, Akyazi F, Stelinski LL, Edison AS, Schroeder FC, Teal PE (2012) Interspecific nematode signals regulate dispersal behavior. PLoS ONE 7(6):e38735. https://doi.org/10.1371/journal.pone.0038735
Kishi Y (1995) Pine wood nematode and the Japanese pine sawyer. Thomas Company Limited.
Leroy PD, Sabri A, Verheggen FJ, Francis F, Thonart P, Haubruge E (2011) The semiochemically mediated interactions between bacteria and insects. Chemoecology 21(3):113–122. https://doi.org/10.1007/s00049-011-0074-6
Ludewig AH, Izrayelit Y, Park D, Malik RU, Zimmermann A, Mahanti P, Fox BW, Bethke A, Doering F, Riddle DL, Schroeder FC (2013) Pheromone sensing regulates Caenorhabditis elegans lifespan and stress resistance via the deacetylase SIR-2.1. Proc Natl Acad Sci USA 110(14):5522–5527. https://doi.org/10.1073/pnas.1214467110
Ludewig AH, Schroeder FC (2013) Ascaroside signaling in C. elegans. WormBook: the online review of C. elegans biology pp 1–22. ttps://doi.org/10.1895/wormbook.1.155.1.
Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, Clardy J, Bargmann CI (2009) A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458(7242):1171. https://doi.org/10.1038/nature07886
Mamiya Y, Enda N (1979) Bursaphelenchus mucronatus N. Sp. (Nematoda: Aphelenchoididae) from pine wood and its biology and pathogenicity to pine trees. Nematologica 25(3):353–361. https://doi.org/10.1163/187529279x00091
Manosalva P, Manohar M, Von Reuss SH, Chen S, Koch A, Kaplan F, Choe A, Micikas RJ, Wang XH, Kogel KH, Sternberg PW, Williamson VM, Schroeder FC, Klessig DF (2015) Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nat Commun 6:7795. https://doi.org/10.1038/ncomms8795
Nickle WR, Golden AM, Mamiya Y, Wergin WP (1981) On the taxonomy and morphology of the pine wood nematode, Bursaphelenchus xylophilus (Steiner & Buhrer 1934) Nickle 1970. J Nematol 13(3):385
Niu H, Zhao LL, Sun JH (2013) Phenotypic plasticity of reproductive traits in response to food availability in invasive and native species of nematode. Biol Invasions 15(7):1407–1415. https://doi.org/10.1007/s10530-012-0379-6
Noguez JH, Conner ES, Zhou Y, Ciche TA, Ragains JR, Butcher RA (2012) A novel ascaroside controls the parasitic life cycle of the entomopathogenic nematode Heterorhabditis bacteriophora. ACS Chem Biol 7(6):961–966. https://doi.org/10.1021/cb300056q
Nordlund DA, Lewis WJ (1976) Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. J Chem Ecol 2(2):211–220. https://doi.org/10.1007/bf00987744
Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128(4):573–592. https://doi.org/10.1086/284589
Penas AC, Tenreiro R, Mota M, Bravo MA, Correia P (2004) Species of Bursaphelenchus Fuchs, 1937 (Nematoda: Parasitaphelenchidae) associated with maritime pine in Portugal. Nematology 6(3):437–453. https://doi.org/10.1163/1568541042360573
Pereira F, Moreira C, Fonseca L, Van Asch B, Mota M, Abrantes I, Amorim A (2013) New insights into the phylogeny and worldwide dispersion of two closely related nematode species, Bursaphelenchus xylophilus and Bursaphelenchus mucronatus. PLoS ONE 8(2):e56288. https://doi.org/10.1371/journal.pone.0056288
Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47(1):435–465. https://doi.org/10.1146/annurev.ento.47.091201.145227
Sato T, Suzuki N (2010) Female size as a determinant of larval size, weight, and survival period in the coconut crab Birgus latro. J Crustac Biol 30(4):624–628. https://doi.org/10.1651/10-3279.1
Shapiro-Ilan DI, Kaplan F, Oliveira-Hofman C, Schliekelman P, Alborn HT, Lewis EE (2019) Conspecific pheromone extracts enhance entomopathogenic infectivity. J Nematol 51: 1–5. https://doi.org/10.21307/jofnem-2019-082
Smart LE, Aradottir GI, Bruce TJA (2014) Role of semiochemicals in integrated pest management. In: Abrol DP (ed.), Integrated pest management, pp 93–109. https://doi.org/10.1016/b978-0-12-398529-3.00007-5
Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, Teal PEA, Malik RU, Edison AS, Sternberg PW, Schroeder FC (2008) A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 454(7208):1115–1118. https://doi.org/10.1038/nature07168
Srinivasan J, Von Reuss SH, Bose N, Zaslaver A, Mahanti P, Ho MC, O’Doherty OG, Edison AS, Sternberg PW, Schroeder FC (2012) A modular library of small molecule signals regulates social behaviors in Caenorhabditis elegans. PLoS Biol 10(1):e1001237. https://doi.org/10.1371/journal.pbio.1001237
Stewart AJ (1996) Interspecific competition reinstated as an important force structuring insect herbivore communities. Trends Ecol Evol 11(6):233–234. https://doi.org/10.1016/0169-5347(96)30009-8
Vincent B, Altemayer V, Roux-Morabito G, Naves P, Sousa E, Lieutier F (2008) Competitive interaction between Bursaphelenchus xylophilus and the closely related species Bursaphelenchus mucronatus. Nematology 10(2):219–230. https://doi.org/10.1163/156854108783476403
Von Reuss SH, Bose N, Srinivasan J, Yim JJ, Judkins JC, Sternberg PW, Schroeder FC (2012) Comparative metabolomics reveals biogenesis of ascarosides: a modular library of small-molecule signals in C. elegans. J Am Chem Soc 134(3), 1817–1824. https://doi.org/10.1021/ja210202y.
Wang JL, Zhang JC, Gu JF (2011) Method of extracting DNA from a single nematode. Plant Quarantine 25(2):32–35
Wharam B, Weldon L, Viney M (2017) Pheromone modulates two phenotypically plastic traits–adult reproduction and larval diapause–in the nematode Caenorhabditis elegans. BMC Evol Biol 17(1):197. https://doi.org/10.1186/s12862-017-1033-9
Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signatures. Cambridge University Press, Cambridge
Yamada K, Hirotsu T, Matsuki M, Butcher RA, Tomioka M, Ishihara T, Clardy J, Kunitomo H, Iino Y (2010) Olfactory plasticity is regulated by pheromonal signaling in Caenorhabditis elegans. Science 329(5999):1647–1650. https://doi.org/10.1126/science.1192020
Yan X, Cheng XY, Wang YS, Luo J, Mao ZC, Ferris VR, Xie BY (2012) Comparative transcriptomics of two pathogenic pinewood nematodes yields insights into parasitic adaptation to life on pine hosts. Gene 505(1):81–90. https://doi.org/10.1016/j.gene.2012.05.041
Zhao LR, Liao JL, Zhong GQ (2005) A rapid method to detect Bursaphelenchus xylophilus and B. mucronatus by PCR. Journal of South China Agricultural University 26(2):59–61. https://doi.org/10.3969/j.issn.1001-411X.2005.02.015
Zhao LL, Mota M, Vieira P, Butcher RA, Sun JH (2014) Interspecific communication between pinewood nematode, its insect vector, and associated microbes. Trends Parasitol 30(6):299–308. https://doi.org/10.1016/j.pt.2014.04.007
Zhao LL, Zhang X, Wei Y, Zhou J, Zhang W, Qin PJ, Chinta S, Kong XB, Liu YP, Yu HY, Hu SN, Zhen Z, Butcher RA, Sun JH (2016) Ascarosides coordinate the dispersal of a plant-parasitic nematode with the metamorphosis of its vector beetle. Nat Commun 7:12341. https://doi.org/10.1038/ncomms12341
Acknowledgements
This work was funded by the National Natural Science Foundation of China (31630013, 31572272) and the Frontier Science Key Project of the Chinese Academy of Sciences (QYZDJ-SSW-SMC024).
Author information
Authors and Affiliations
Contributions
JM, LZ and JS conceived and designed the research. JM and WR carried out the experiments. JM analyzed the data. JM, JDW and JS wrote the manuscript. All authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Communicated by J.D. Sweeney.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Meng, J., Wickham, J.D., Ren, W. et al. Species displacement facilitated by ascarosides between two sympatric sibling species: a native and invasive nematode. J Pest Sci 93, 1059–1071 (2020). https://doi.org/10.1007/s10340-020-01206-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-020-01206-w