Aphid facultative symbionts reduce survival of the predatory lady beetle Hippodamia convergens

BMC Ecology

Volumn 14, Issue , 2014, Pages

  Costopoulos, Kelly ^a   Kovacs, Jennifer L ^a,b   Kamins, Alexandra ^a   Gerardo, Nicole M ^a  

^a EMORY UNIVERSITY   (United States)

^b SPELMAN COLLEGE   (United States)

Author keywords

Acyrthosiphon pisum; Defensive mutualism; Hamiltonella defensa; Mutualism; Pea aphid; Predation; Protective symbiosis; Serratia symbiotica; Symbiont conferred protection; Symbiosis

Indexed keywords

APHID; BEETLE; ECOLOGICAL IMPACT; INTERSPECIFIC INTERACTION; MUTUALISM; PARASITISM; PREDATION; SURVIVAL; SYMBIONT;

ACYRTHOSIPHON PISUM; APHIDIDAE; BACTERIA (MICROORGANISMS); CANDIDATUS HAMILTONELLA DEFENSA; CANDIDATUS SERRATIA SYMBIOTICA; COCCINELLIDAE; COLEOPTERA; HIPPODAMIA; HIPPODAMIA CONVERGENS; SERRATIA;

ANIMAL; APHID; ARTICLE; BEETLE; FEEDING BEHAVIOR; FEMALE; GROWTH, DEVELOPMENT AND AGING; LARVA; MALE; MICROBIOLOGY; POPULATION DYNAMICS; PREDATION; REGRESSION ANALYSIS; STATISTICAL MODEL; SYMBIOSIS;

ANIMALS; APHIDS; BEETLES; FEEDING BEHAVIOR; FEMALE; LARVA; LEAST-SQUARES ANALYSIS; LINEAR MODELS; MALE; POPULATION DYNAMICS; PREDATORY BEHAVIOR; SYMBIOSIS;

EID: 84896404394     PISSN: None     EISSN: 14726785     Source Type: Journal    
DOI: 10.1186/1472-6785-14-5     Document Type: Article

References (48)

1. Stouthamer R, Breeuwer JAJ, Hurst GDD. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 1999, 53:71-102. 10.1146/annurev.micro.53.1.71, 10547686.
2. Zchori-Fein E, Perlman SJ. Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 2004, 13:2009-2016. 10.1111/j.1365-294X.2004.02203.x, 15189221.
3. Terry RS, Smith JE, Sharpe RG, Rigaud T, Littlewood DTJ, Ironside JE, Rollinson D, Bouchon D, MacNeil C, Dick JT. Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum microspora. Proc R Soc B 2004, 271:1783-1789. 10.1098/rspb.2004.2793, 1691802, 15315893.
4. Moran NA, Dunbar HE. Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci USA 2006, 103:12803-12806. 10.1073/pnas.0605772103, 1568928, 16908834.
5. Kaltenpoth M, Engl T. Defensive microbial symbionts in hymenoptera. Funct Ecol 2013, [Epub ahead of print]10.1111/1365-2435.12089.
6. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 2003, 100:1803-1807. 10.1073/pnas.0335320100, 149914, 12563031.
7. Duron O, Hurst GDD. Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biol 2013, 11:45. 10.1186/1741-7007-11-45, 3626882, 23587344.
8. Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 2008, 42:165-190. 10.1146/annurev.genet.41.110306.130119, 18983256.
9. Moran NA, Baumann P. Bacterial endosymbionts in animals. Curr Opin Microbiol 2000, 3:270-275. 10.1016/S1369-5274(00)00088-6, 10851160.
10. Buchner P. Endosymbiosis of animals with plant microorganims. 1965, New York: Wiley & Sons, Inc.
11. Haine ER. Symbiont-mediated protection. Proc Biol Sci 2008, 275:353-361. 10.1098/rspb.2007.1211, 2213712, 18055391.
12. Brownlie JC, Johnson KN. Symbiont-mediated protection in insect hosts. Trends Microbiol 2009, 17:348-354. 10.1016/j.tim.2009.05.005, 19660955.
13. Oliver KM, Degnan PH, Burke GR, Moran NA. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 2010, 55:247-266. 10.1146/annurev-ento-112408-085305, 19728837.
14. Gil-Turnes MS, Hay ME, Fenical W. Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 1989, 246:116-118. 10.1126/science.2781297, 2781297.
15. Warr E, Aguilar R, Dong Y, Mahairaki V, Dimopoulos G. Spatial and sex-specific dissection of the Anopheles gambiae midgut transcriptome. BMC Genomics 2007, 8:37. 10.1186/1471-2164-8-37, 1804276, 17261194.
16. Teixeira L, Ferreira, Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 2008, 6:e1000002.
17. Gil-Turnes MS, Fenical W. Embryos of Homarus americanus are protected by epibiotic bacteria. Biol Bull 1992, 182:105-108.
18. Scarborough CL, Ferrari J, Godfray HCJ. Aphid protected from pathogen by endosymbiont. Science 2005, 310:1781-1781. 10.1126/science.1120180, 16357252.
19. Parker BJ, Spragg CJ, Altincicek B, Gerardo NM. Symbiont-mediated protection against fungal pathogens in pea aphids: a role for pathogen specificity?. Appl Environ Microbiol 2013, 79:2455-2458. 10.1128/AEM.03193-12, 3623210, 23354709.
20. Oliver KM, Moran NA, Hunter MS. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 2005, 102:12795. 10.1073/pnas.0506131102, 1200300, 16120675.
21. Oliver KM, Moran NA. Defensive symbionts in aphids and other insects. Defensive Mutualism in Microbial Symbiosis 2009, 129-148. Boca Raton: CRC Press, White JF, Torres MS.
22. Haine ER, Boucansaud K, Rigaud T. Conflict between parasites with different transmission strategies infecting an amphipod host. Proc R Soc B 2005, 272:2505-2510. 10.1098/rspb.2005.3244, 1599785, 16271976.
23. Oliver KM, Degnan PH, Hunter MS, Moran NA. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 2009, 325:992-994. 10.1126/science.1174463, 19696350.
24. Kellner RL. Stadium-specific transmission of endosymbionts needed for pederin biosynthesis in three species of Paederus rove beetles. Entomol Exp Appl 2003, 107:115-124.
25. Kellner RLL, Dettner K. Differential efficacy of toxic pederin in deterring potential arthropod predators of Paederus (Coleoptera: Staphylinidae) offspring. Oecologia 1996, 107:293-300.
26. Piel J, Höfer I, Hui D. Evidence for a symbiosis island involved in horizontal acquisition of pederin biosynthetic capabilities by the bacterial symbiont of Paederus fuscipes beetles. J Bacteriol 2004, 186:1280-1286. 10.1128/JB.186.5.1280-1286.2004, 344417, 14973122.
27. Lopanik N, Lindquist N, Targett N. Potent cytotoxins produced by a microbial symbiont protect host larvae from predation. Oecologia 2004, 139:131-139. 10.1007/s00442-004-1487-5, 14747940.
28. Russell JA, Moran NA. Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl Environ Microbiol 2005, 71:7987-7994. 10.1128/AEM.71.12.7987-7994.2005, 1317397, 16332777.
29. Baungaard J. A simple method for sexing Coccinella septempunctata L. Coleoptera: Coccinellidae). Enomologiske Meddelelser 1980, 48:26-28.
30. Pro JMP v10. 2012, Cary, NC: SAS, Pro JMP.
31. Kellner RL. What is the basis of pederin polymorphism in Paederus riparius rove beetles? The endosymbiotic hypothesis. Entomol Exp Appl 1999, 93:41-49.
32. Schardl CL, Leuchtmann A, Spiering MJ. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 2004, 55:315-340. 10.1146/annurev.arplant.55.031903.141735, 15377223.
33. de Sassi C, Müller CB, Krauss J. Fungal plant endosymbionts alter life history and reproductive success of aphid predators. Proc R Soc B 2006, 273:1301-1306. 10.1098/rspb.2005.3442, 1560287, 16720406.
34. Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M, Soler JJ. Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc R Soc B 2010, 277:123-130. 10.1098/rspb.2009.1377, 2842625, 19812087.
35. Loxdale HD. The nature and reality of the aphid clone: genetic variation, adaptation and evolution. Agric Forest Entomol 2008, 10:81-90.
36. Duff KM, Mondor EB. All clone-mates are not created equal: fitness discounting theory predicts pea aphid colony structure. J Insect Behav 2012, 25:48-59.
37. Dixon AFG. Structure of aphid populations. Annu Rev Entomol 1985, 30:155-174.
38. Doumbia M, Hemptinne JL, Dixon AFG. Assessment of patch quality by ladybirds: role of larval tracks. Oecologia 1998, 133:197-202.
39. Dixon AFG. An experimental study of the searching behaviour of the predatory coccinellid beetle Adalia decempunctata (L.). J Ecol 1959, :259-281.
40. Yasuda H, Shinya Y. Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 1997, 42:153-163.
41. Nowak MA, Tarnita CE, Wilson EO. The evolution of eusociality. Nature 2010, 466:1057-1062. 10.1038/nature09205, 3279739, 20740005.
42. Linksvayer TA. Direct, maternal, and sibsocial genetic effects on indvidual and colony traits in an ant. Evolution 2006, 60:2552-2561. 10.1111/j.0014-3820.2006.tb01889.x, 17263116.
43. Fox CW, Czesak ME. Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 2000, 45:341-369. 10.1146/annurev.ento.45.1.341, 10761581.
44. Fischer B, Taborsky B, Kokko H. How to balance the offspring quality-quantity tradeoff when environmental cues are unreliable. Oikos 2011, 120:258-270.
45. Honek A. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 1993, 66:483-492.
46. Oliver KM, Noge K, Huang EM, Campos JM, Becerra JX, Hunter MS. Parasitic wasp responses to symbiont-based defense in aphids. BMC Biol 2012, 10:11. 10.1186/1741-7007-10-11, 3312838, 22364271.
47. Stern DL, Foster WA. The evolution of soldiers in aphids. Biol Rev 1996, 71:27-79. 10.1111/j.1469-185X.1996.tb00741.x, 8603120.
48. Stern DL, Foster WA. The evolution of sociality in aphids: a clone's-eye view. The evolution of social behavior in insects and arachnids 1997, 150-165. Cambridge: Cambridge University Press, Crespi BJ.