Maternal care provides antifungal protection to eggs in the European earwig

Behavioral Ecology

Volumn 25, Issue 4, 2014, Pages 754-761

  Boos, Stefan ^a   Meunier, Joël ^b   Pichon, Samuel ^a   Kölliker, Mathias ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

antimicrobial defense; Dermaptera; egg attendance; egg grooming; insect; Mucor; social defence; social evolution

Indexed keywords

EID: 84899556859     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/aru046     Document Type: Article

References (56)

1. Arce AN, Johnston PR, Smiseth P T, Rozen DE. 2012. Mechanisms and ftness efects of antibacterial defences in a carrion beetle. J Evol Biol. 25:930-937.
2. Blomquist GJ, Bagnères AG. 2010. Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge: Cambridge University Press.
3. Butnariu AR, Pasini A, Reis FS, Bessa E. 2013. Maternal care by the earwig Doru lineare Eschs. (Dermaptera: Forfculidae). J Insect Behav. 26:667-678.
4. Buxton JH, Madge DS. 1974. Artifcial incubation of eggs of the common earwig, Forfcula auricularia (L.). Entomol Mon Mag. 110:55-57.
5. Chauvin G, Hamon C, Vancassel M, Vannier G. 1991. The eggs of Forfcula auricularia L. (Dermaptera, Forfculidae): ultrastructure and resistance to low and high temperatures. Can J Zool. 69:2873-2878.
6. Cocroft RB. 1999. Parent-ofspring communication in response to predators in a subsocial treehopper (Hemiptera: Membracidae: Umbonia crassicornis). Ethology. 105:553-568.
7. Costa J T. 2006. The other insect societies. Cambridge (MA): Harvard University Press. p. 49-80.
8. Cotter SC, Kilner RM. 2010a. Personal immunity versus social immunity. Behav Ecol. 21:663-668.
9. Cotter SC, Kilner RM. 2010b. Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides. J Anim Ecol. 79:35-43.
10. Cremer S, Armitage SA, Schmid-Hempel P. 2007. Social immunity. Curr Biol. 17:R693-R702.
11. Cremer S, Sixt M. 2009. Analogies in the evolution of individual and social immunity. Phil Trans R Soc Lond B. 364:129-142.
12. Dobler R, Kölliker M. 2010. Kin-selected siblicide and cannibalism in the European earwig. Behav Ecol. 21:257-263.
13. Dobler R, Kölliker M. 2011. Infuence of weight asymmetry and kinship on siblicidal and cannibalistic behaviour in earwigs. Anim Behav. 82:667-672.
14. Eisner T. 1960. Defense mechanisms of arthropods. II. The chemical and mechanical weapons of an earwig. Psyche. 67:62-70.
15. Eisner T, Rossini C, Eisner M. 2000. Chemical defense of an earwig (Doru taeniatum). Chemoecology. 10:81-87.
16. Gasch T, Schott M, Wehrenfennig C, Düring RA, Vilcinskas A. 2013. Multifunctional weaponry: the chemical defenses of earwigs. J Insect Physiol. 59:1186-1193.
17. Gherbawy Y, Mach RL, Rai M. 2009. Current advances in molecular mycology. New York: Nova Science Publishers, Inc.
18. Grindstaf JL, Brodie ED, Ketterson ED. 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc R Soc Lond B. 270:2309-2319.
19. Herzner G, Strohm E. 2007. Fighting fungi with physics: food wrapping by a solitary wasp prevents water condensation. Curr Biol. 17:R46-R47.
20. Jayaprakash A, Ebenezer P. 2010. A new report on mycobiota associated with Ropalidia marginata paper nests. Indian J Sci Technol. 3:6-8.
21. Klostermeyer EC. 1942. The life history and habits of the ringlegged earwig, Euborellia annulipes (Lucus) (Order Dermaptera). J Kansas Entomol Soc. 15:13-18.
22. Kölliker M. 2007. Benefts and costs of earwig (Forfcula auricularia) family life. Behav Ecol Sociobiol. 61:1489-1497.
23. Konrad M, Vyleta ML, Theis FJ, Stock M, Tragust S, Klatt M, Drescher V, Marr C, Ugelvig LV, Cremer S. 2012. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biol. 10:e1001300.
24. Kroiss J, Kaltenpoth M, Schneider B, Schwinger MG, Hertweck C, Maddula RK, Strohm E, Svatos A. 2010. Symbiotic Streptomycetes provide antibiotic combination prophylaxis for wasp ofspring. Nat Chem Biol. 6:261-263.
25. Lamb RJ. 1976. Parental behaviour in the Dermaptera with special reference to Forfcula auricularia (Dermaptera: Forfculidae). Can Entomol. 108:609-619.
26. Lamb RJ, Wellington WG. 1975. Life history and population characteristics of the European earwig, Forfcula auricularia, (Dermaptera: Forfculidae), at Vancouver, British Columbia. Can Entomol. 107:819-824.
27. Lessells CM, Boag P T. 1987. Unrepeatable repeatabilities: a common mistake. Auk. 2:116-121.
28. Machado G, Oliveira PS. 2002. Maternal care in the neotropical harvestman Bourguyia albiornata (Arachnida: Opiliones): Oviposition site selection and egg protection. Behaviour. 139:1509-1524.
29. Madden AA, Stchigel AM, Guarro J, Sutton D, Starks PT. 2012. Mucor nidi-cola sp. nov., a fungal species isolated from an invasive paper wasp nest. Int J Syst Evol Microbiol. 62:1710-1714.
30. Mari M, Cembali T, Casalini L, Pratella GC. 2000. Mucor species in orchard soil-population dynamics and pathogenicity on pear fruit. Eur J Plant Pathol. 106:449-454.
31. Matsuura K, Tamura T, Kobayashi N, Yashiro T, Tatsumi S. 2007. The antibacterial protein lysozyme identifed as the termite egg recognition pheromone. PLoS One. 2:e813.
32. Meunier J, Kölliker M. 2012. Parental antagonism and parent-of-spring co-adaptation interact to shape family life. Proc R Soc Lond B. 279:3981-3988.
33. Meunier J, Wong JWY, Gómez Y, Kuttler S, Röllin L, Stucki D, Kölliker M. 2012. One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig. Evol Ecol. 26:669-682.
34. Miller JS, Rudolph L, Zink AG. 2011. Maternal nest defense reduces egg cannibalism by conspecifc females in the maritime earwig Anisolabis mari-tima. Behav Ecol Sociobiol. 65:1873-1879.
35. Miller JS, Zink AG. 2012. Parental care trade-ofs and the role of flial cannibalism in the maritime earwig, Anisolabis maritima. Anim Behav. 83:1387-1394.
36. Pollard SD. 1984. Egg guarding by Clubiona cambridgei (Araneae, Clubionidae) against conspecifc predators. Am Arachnol Soc. 11:323-326.
37. Reber A, Chapuisat M. 2012. Diversity, prevalence and virulence of fungal entomopathogens in colonies of the ant Formica selysi. Insectes Soc. 59:231-239.
38. Reber A, Purcell J, Buechel SD, Buri P, Chapuisat M. 2011. The expression and impact of antifungal grooming in ants. J Evol Biol. 24:954-964.
39. Rosengaus RB, Traniello JFA, Chen T, Brown JJ, Karp RD. 1999. Immunity in a social insect. Naturwissenschaften 86:588-591.
40. Royle NJ, Smiseth P, Kölliker M. 2012. The evolution of parental care. Oxford: Oxford University Press.
41. Rozen DE, Engelmoer DJ, Smiseth P T. 2008. Antimicrobial strategies in burying beetles breeding on carrion. Proc Natl Acad Sci USA. 105:17890-17895.
42. Schmid-Hempel P. 2003. Variation in immune defence as a question of evolutionary ecology. Proc Biol Sci. 270:357-366.
43. Schmid-Hempel P, Ebert D. 2003. On the evolutionary ecology of specifc immune defence. Trends Ecol Evol. 18:27-32.
44. Smiseth P T, Royle NJ, Kölliker M. 2012. What is parental care? In: Royle NJ, Smiseth P T, Kölliker M, editors. The evolution of parental care. Oxford: Oxford University Press.
45. Strohm E, Linsenmair KE. 2001. Females of the European beewolf preserve their honeybee prey against competing fungi. Ecol Entomol. 26:198-203.
46. Tallamy DW. 1984. Insect parental care. Bioscience. 34:20-24.
47. Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S. 2013. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Curr Biol. 23:76-82.
48. Traniello JF, Rosengaus RB, Savoie K. 2002. The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc Natl Acad Sci USA. 99:6838-6842.
49. Trumbo S T. 2012. Patterns of parental care in invertebrates. In: Royle NJ, Smiseth P T, Kölliker M, editors. The evolution of parental care. 1st ed. Oxford: Oxford University Press. p. 81-93.
50. Ugelvig L V, Cremer S. 2007. Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr Biol. 17:1967-1971.
51. Ugelvig L V, Kronauer DJ, Schrempf A, Heinze J, Cremer S. 2010. Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc R Soc Lond B. 277:2821-2828.
52. Wong JWY, Kölliker M. 2012. The efect of female condition on maternal care in the European earwig. Ethology. 118:450-459.
53. Wong JWY, Meunier J, Kölliker M. 2013. The evolution of parental care in insects: the roles of ecology, life history and the social environment. Ecol Entomol. 38:123-137.
54. Worthington EB. 1926. The life-cycle of Forfcula auricularia L. The Entomologist. 39:138-142.
55. Zeh DW, Zeh JA, Smith RL. 1989. Ovipositors, amnions and eggshell architecture in the diversifcation of terrestrial arthropods. Q Rev Biol. 64:147-168.
56. Zink AG. 2003. Quantifying the costs and benefts of parental care in female treehoppers. Behav Ecol. 14:687-693.