Endosymbiont diversity among sibling weevil species competing for the same resource

BMC Evolutionary Biology

Marie-Claude Bel-Venner²  Abdelaziz Heddi¹  Fabrice Vavre²  Frédéric Menu²  Agnès Vallier¹  Hélène Henri²  Samuel Venner²  Adrien Merville¹ 

[1] INSA-Lyon, UMR203 BF2I, INRA, Biologie Fonctionnelle Insectes et Interactions, Bat. L. Pasteur 20 ave A. Einstein, Villeurbanne, France;Université de Lyon, Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, Villeurbanne, France

关键词: Field study;    Niche partitioning;    Infection pattern;    Oak weevil;    Curculio;    Host community;    Endosymbiosis;   

Others  :  1130089
DOI  :  10.1186/1471-2148-13-28

 received in 2012-09-03, accepted in 2013-01-30,  发布年份 2013

【 摘 要 】

Background

Whereas the impact of endosymbionts on the ecology of their hosts is well known in some insect species, the question of whether host communities are influenced by endosymbionts remains largely unanswered. Notably, the coexistence of host species competing with each other, which is expected to be stabilized by their ecological differences, could be facilitated by differences in their endosymbionts. Yet, the composition of endosymbiotic communities housed by natural communities of competing host species is still almost unknown. In this study, we started filling this gap by describing and comparing the bacterial endosymbiotic communities of four sibling weevil species (Curculio spp.) that compete with each other to lay eggs into oak acorns (Quercus spp.) and exhibit marked ecological differences.

Results

All four species housed the primary endosymbiont Candidatus Curculioniphilus buchneri, yet each of these had a clearly distinct community of secondary endosymbionts, including Rickettsia, Spiroplasma, and two Wolbachia strains. Notably, three weevil species harbored their own predominant facultative endosymbiont and possessed the remaining symbionts at a residual infection level.

Conclusions

The four competing species clearly harbor distinct endosymbiotic communities. We discuss how such endosymbiotic communities could spread and keep distinct in the four insect species, and how these symbionts might affect the organization and species richness of host communities.

【 授权许可】

   
2013 Merville et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Feldhaar H, Gross R: Immune reactions of insects on bacterial pathogens and mutualists. Microbes Infect 2008, 10:1082-1088.
• [2]Clark EL, Karley AJ, Hubbard SF: Insect endosymbionts: manipulators of insect herbivore trophic interactions? Protoplasma 2010, 244:25-51.
• [3]Ferrari J, Vavre F: Bacterial symbionts in insects or the story of communities affecting communities. Phil Trans Biol Sci 2011, 366:1389-1400.
• [4]Moran NA, McCutcheon JP, Nakabachi A: Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 2008, 42:165-190.
• [5]Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS: Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 2011, 332:254-256.
• [6]Douglas AE: Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 1998, 43:17-37.
• [7]McCutcheon JP, McDonald BR, Moran NA: Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci U S A 2009, 106:15394-15399.
• [8]Lamelas A, Gosalbes MJ, Moya A, Latorre A: New clues about the evolutionary history of metabolic losses in bacterial endosymbionts, provided by the genome of buchnera aphidicola from the aphid cinara tujafilina. Appl Environ Microbiol 2011, 77:4446-4454.
• [9]Leonardo TE, Muiru GT: Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc R Soc B 2003, 270:S209-S212.
• [10]Simon J-C, Carré S, Boutin M, Prunier-Leterme N, Sabater-Mun B, Latorre A, Bournoville R: Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc R Soc B 2003, 270:1703-1712.
• [11]Tsuchida T, Koga R, Fukatsu T: Host plant specialization governed by facultative symbiont. Science 1989, 2004:303.
• [12]Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-daube N, Kontsedalov S, Gershon M, Gal S, Katzir N, Zchori-fein E: Identification and localization of a rickettsia sp. In bemisia tabaci (homoptera: aleyrodidae). Appl Environ Microbiol 2006, 72:3646-3652.
• [13]Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, Inbar M, Ghanim M: Biotype-dependent secondary symbiont communities in sympatric populations of bemisia tabaci. Bull Entomol Res 2007, 97:407-413.
• [14]Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D, Chiel E, Gottlieb Y, Ghanim M, Zchori-Fein E, Fleury F: Endosymbiont metacommunities, mtDNA diversity and the evolution of the bemisia tabaci (hemiptera: aleyrodidae) species complex. Mol Ecol 2010, 19:4365-4378.
• [15]Toju H, Fukatsu T: Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol 2010, 20:853-868.
• [16]Montllor CB, Maxmen A, Purcell AH: Facultative bacterial endosymbionts benefit pea aphids acyrthosiphon pisum under heat stress. Ecol Entomol 2002, 27:189-195.
• [17]Oliver KM, Russell JA, Moran NA, Hunter MS: Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 2003, 100:1803-1807.
• [18]Haine ER, Moret Y, Siva-jothy MT, Rolff J: Antimicrobial defense and persistent infection in insects. Science 2008, 322:1257-1259.
• [19]Brownlie JC, Johnson KN: Symbiont-mediated protection in insect hosts. Trends Microbiol 2009, 17:348-354.
• [20]Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ: Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 2010, 329:212-215.
• [21]Grenier A-M, Nardon C, Nardon P: The role of symbiotes in flight activity of Sitophilus weevils. Entomol Exp Appl 1994, 70:201-208.
• [22]Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P: Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci U S A 1999, 96:6814-6819.
• [23]Leonardo TE, Mondor EB: Symbiont modifies host life-history traits that affect gene flow. Proc R Soc B 2006, 273:1079-1084.
• [24]Goodacre SL, Martin OY, Bonte D, Hutchings L, Woolley C, Ibrahim K, Thomas CFG, Hewitt GM: Microbial modification of host long-distance dispersal capacity. BMC Biol 2009, 7:32. BioMed Central Full Text
• [25]Bordenstein SR: Symbiosis and the origin of species. In Insect Symbiosis. Edited by Bourtzis K, Miller TA. Boca Raton, FL: CRC Press; 2003:283-304.
• [26]Werren JH, Baldo L, Clark ME: Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008, 6:741-751.
• [27]Merçot H, Poinsot D: Infection by Wolbachia: from passengers to residents. C R Biol 2009, 332:284-297.
• [28]Müller JP, Hauzy C, Hulot FD: Ingredients for protist coexistence: competition, endosymbiosis and a pinch of biochemical interactions. J Anim Ecol 2011, 81:222-232.
• [29]Patot S, Allemand R, Fleury F, Varaldi J: An inherited virus influences the coexistence of parasitoid species through behaviour manipulation. Ecol Lett 2012, 15:603-610.
• [30]Harnett DC, Wilson GWT: Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 1999, 80:1187-1195.
• [31]Reynolds HL, Packer A, Bever JD, Clay K: Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 2003, 84:2281-2291.
• [32]Van der Heijden MGA, Bardgett RD, Straalen MV: The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 2006, 11:296-310.
• [33]Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M: Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 2010, 25:468-478.
• [34]Hoffmann A: Faune de France Coléoptères Curculionides (Deuxième partie). Paris, France: Fédération Française des Sociétés de Sciences Naturelles; 1954.
• [35]Coutin R: Original characteristics of the evolving cycles of some European weevil species: Curculio elephas Gyll., C. nucum L., C. glandium Marsh., C. venosus Grav. and C. villosus F. Memoires de la Societe royale belge d’Entomologie 1992, 35:259-266.
• [36]Hughes J, Vogler AP: The phylogeny of acorn weevils (genus curculio) from mitochondrial and nuclear DNA sequences: the problem of incomplete data. Mol Phylogenet Evol 2004, 32:601-615.
• [37]Venner S, Pélisson PF, Bel-Venner MC, Débias F, Rajon E, Menu F: Coexistence of insect species competing for a pulsed resource: toward a unified theory of biodiversity in fluctuating environments. Public Library of Science One 2011, 6:e18039.
• [38]Toju H, Hosokawa T, Koga R, Nikoh N, Meng XY, Kimura N, Fukatsu T: “Candidatus curculioniphilus buchneri,” a novel clade of bacterial endocellular symbionts from weevils of the genus curculio. Appl Environ Microbiol 2010, 76:275-282.
• [39]Schauff ME: Collecting and preserving insects and mites: tools and techniques. Washington: USDA Misc Publ n°1443: Museum of Natural History; 1986.
• [40]Sambrook J, Russell DW: Molecular cloning: a laboratory manual. 3rd edition. New York, NY: Cold Spring Harbor Laboratory Press; 2001.
• [41]Pélisson PF, Henri H, Bel-Venner MC, Allemand R, Merville A, Menu F, Venner S: Identification at the larval stage of four curculio species coexisting on oak trees using PCR-RFLP. Entomol Exp Appl 2011, 138:77-82.
• [42]Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P: Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymeras chain reaction primers. Ann Entomol Soc Am 1994, 87:651-701.
• [43]Lefèvre C, Charles H, Vallier A, Delobel B, Farrell B, Heddi A: Endosymbiont phylogenesis in the dryophthoridae weevils: evidence for bacterial replacement. Mol Biol Evol 2004, 21:965-973.
• [44]Werren JH, Windsor DM: Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc R Soc B 2000, 267:1277-1285.
• [45]Duron O: Never completely trust a model: insights from cytoplasmic incompatibility beyond wolbachia-drosophila interactions. Heredity 2008, 101:473-474.
• [46]Edgar RC: MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 2004, 5:1-19. BioMed Central Full Text
• [47]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [48]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
• [49]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [50]Shimodaira H, Hasegawa M: Multiple comparisons of loglikelihoods with applications to phylogenetic inference. Mol Biol Evol 1999, 16:1114-1116.
• [51]Shimodaira H: An approximately unbiased test of phylogenetic tree selection. Syst Biol 2002, 51:492-508.
• [52]Shimodaira H, Hasegawa M: CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001, 17:1246-1247.
• [53]Meier-Kolthoff JP, Auch AF, Huson DH, Göker M: COPYCAT: cophylogenetic analysis tool. Bioinformatics 2007, 7:898-900.
• [54]Legendre P, Desdevises Y, Bazin E: A statistical test for host-parasite coevolution. Syst Biol 2002, 51:217-234.
• [55]Fukatsu T, Shimada M: Molecular characterization of rickettsia sp in a bruchid beetle kytorhinus sharpianus. Appl Entomol Zool 1999, 34:391-397.
• [56]Sork VL, Bramble J, Sexton O: Ecology of mast-fruiting in three species of North American deciduous oaks. Ecology 1993, 74:528-541.
• [57]Leibold MA, McPeek MA: Coexistence of the niche and neutral perspectives in community ecology. Ecology 2006, 87:1399-1410.
• [58]Pélisson PF, Bel-Venner MC, Rey B, Burgevin L, Martineau F, Fourel F, Lecuyer C, Menu F, Venner S: Contrasted breeding strategies in four sympatric sibling insect species: when a proovigenic and capital breeder copes with a stochastic environment. Funct Ecol 2012, 26:198-206.
• [59]Mansour K: On the so-called symbiotic relationship between coleopterous insect and intracellular microorganisms. Q J Microsc Sci 1934, 77:255-272.
• [60]Boyle L, O’Neill SL, Robertson HM, Karr TL: Interspecific and intraspecific horizontal transfer of wolbachia in drosophila. Science 1993, 260:1796-1799.
• [61]Sandström JP, Russell JA, White JP, Moran NA: Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 2001, 10:217-228.
• [62]Russell JA, Latorre A, Sabater-Muñoz B, Moya A, Moran NA: Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 2003, 12:1061-1075.
• [63]Russell JA, Moran NA: Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Society 2005, 71:7987-7994.
• [64]Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon JC, Fukatsu T: Symbiotic bacterium modifies aphid body color. Science 2010, 330:1102-1104.
• [65]Huigens ME, de Almeida RP, Boons PAH, Luck RF, Stouthamer R: Natural interspecific and intraspecific horizontal transfer of parthenogenesis–inducing wolbachia in trichogramma wasps. Proc Roy Soc Lond B Biol Sci 2004, 271:509-515.
• [66]Mouton L, Dedeine F, Henri H, Boulétreau M, Profizi N, Vavre F: Virulence, multiple infections and regulation of symbiotic population in the wolbachia-asobara tabida symbiosis. Genetics 2004, 168:181-189.
• [67]Oliver KM, Moran NA, Hunter MS: Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc B 2006, 273:1273-1280.
• [68]Dowd PF: Insect fungal symbionts: a promising source of detoxifying enzymes. J Ind Microbiol Biotechnol 1992, 9:149-161.
• [69]Tokuda G, Watanabe H: Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 2007, 3:336-339.
• [70]Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL: Evidence for metabolic provisioning by a common invertebrate endosymbiont, wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 2009, 5:e1000368.
• [71]Carpenter KJ, Horak A, Keeling PJ: Phylogenetic position and morphology of spirotrichosomidae (parabasalia): new evidence from leptospironympha of cryptocercus punctulatus. Protist 2010, 161:122-132.
• [72]Oliver KM, Moran NA, Hunter MS: Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci U S A 2005, 102:12795-12800.
• [73]Engelstädter J, Telschow A: Cytoplasmic incompatibility and host population structure. Heredity 2009, 103:196-207.
• [74]Shoemaker DD, Katju V, Jaenike J: Wolbachia and the evolution of reproductive isolation between drosophila recens and drosophila subquinaria. Evolution 1999, 53:1157-1164.
• [75]Marshall JL: The allonemobius-wolbachia host-endosymbiont system: evidence for rapid speciation and against reproductive isolation driven by cytoplasmic incompatibility. Evolution 2004, 58:2409-2425.
• [76]Telschow A, Hammerstein P, Werren JH: The effect of wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution 2005, 59:1607-1619.
• [77]Jaenike J, Dyer KA, Cornish C, Minhas MS: Asymmetrical reinforcement and wolbachia infection in drosophila. PLoS Pathog 2006, 4:e325.