Collective defence portfolios of ant hosts shift with social parasite pressure

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1791, 2014, Pages

  Jongepier, Evelien ^a   Kleeberg, Isabelle ^a   Job, Sylwester ^a   Foitzik, Susanne ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Brood parasites; Defence portfolios; Frontline defences; Host parasite interaction; Social insects

Indexed keywords

AGGRESSION; ANT; ANTIPARASITE DEFENSE; ARMS RACE; BROOD PARASITISM; COEVOLUTION; COOPERATIVE BEHAVIOR; DEFENSE MECHANISM; HOST-PARASITE INTERACTION; PARASITE INTENSITY; PARASITE RESISTANCE; SOCIAL INSECT; SOCIAL PARASITISM;

AGGRESSION; ANIMAL; ANT; HOST PARASITE INTERACTION; PARASITOLOGY; PHYSIOLOGY; QUEBEC; SOCIAL BEHAVIOR; UNITED STATES;

AGGRESSION; ANIMALS; ANTS; HOST-PARASITE INTERACTIONS; QUEBEC; SOCIAL BEHAVIOR; UNITED STATES;

EID: 85003045343     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0225     Document Type: Article

References (50)

1. Planqué R, Britton NF, Franks NR, Peletier MA. 2002 The adaptiveness of defence strategies against cuckoo parasitism. Bull. Math. Biol. 64, 1045-1068. (doi: 10. 1006/bulm. 2002. 0311)
2. Britton NF, Planqué R, Franks NR. 2007 Evolution of defence portfolios in exploiter-victim systems. Bull. Math. Biol. 69, 957-988. (doi: 10. 1007/s11538-006-9178-5)
3. Kilner RM, Langmore NE. 2011 Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol. Rev. Camb. Phil. Soc. 86, 836-852. (doi: 10. 1111/j. 1469-185X. 2010. 00173. x)
4. Svennungsen TO, Holen ØH. 2010 Avian brood parasitism: information use and variation in eggrejection behavior. Evolution64, 1459-1469. (doi: 10. 1111/j. 1558-5646. 2009. 00919. x)
5. Langmore NE, Kilner RM. 2010 The coevolutionary arms race between Horsfield's Bronze-Cuckoos and Superb Fairy-wrens. Emu110, 32-38. (doi: 10. 1071/MU09032)
6. Gilman RT, Nuismer SL, Jhwueng D-C. 2012 Coevolution in multidimensional trait space favours escape from parasites and pathogens. Nature483, 328-330. (doi: 10. 1038/nature10853)
7. Feeney WE, Welbergen JA, Langmore NE. 2012 The frontline of avian brood parasite-host coevolution. Anim. Behav. 84, 3-12. (doi: 10. 1016/j. anbehav. 2012. 04. 011)
8. Spottiswoode CN, Kilner RM, Davies NB. 2012 Brood parasitism. In The evolution of parental care (eds NJ Royle, PT Smiseth, M Kölliker), pp. 226-239. Oxford, UK: Oxford University Press.
9. Alloway TM. 1990 Slave-species ant colonies recognize slavemakers as enemies. Anim. Behav. 39, 1218-1220. (doi: 10. 1016/S0003-3472(05)80797-3)
10. Foitzik S, DeHeer CJ, Hunjan DN, Herbers JM. 2001 Coevolution in host-parasite systems: behavioural strategies of slave-making ants and their hosts. Proc. R. Soc. Lond. B268, 1139-1146. (doi: 10. 1098/rspb. 2001. 1627)
11. Brandt M, Heinze J, Schmitt T, Foitzik S. 2005 A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. J. Evol. Biol. 18, 576-586. (doi: 10. 1111/j. 1420-9101. 2004. 00867. x)
12. Achenbach A, Foitzik S. 2009 First evidence for slave rebellion: enslaved ant workers systematically kill the brood of their social parasite Protomognathus americanus. Evolution63, 1068-1075. (doi: 10. 1111/j. 1558-5646. 2009. 00591. x)
13. Pamminger T, Scharf I, Pennings PS, Foitzik S. 2011 Increased host aggression as an induced defense against slave-making ants. Behav. Ecol. 22, 255-260. (doi: 10. 1093/beheco/arq191)
14. Hölldobler B, Wilson EO. 1990 The ants. Berlin, Germany: Springer.
15. Hermann HR. 1984 Defensive mechanisms in social insects. New York, NY: Praeger.
16. Wilson EO, Regnier FE. 1971 The evolution of the alarm-defense system in the formicine ants. Am. Nat. 105, 279-289. (doi: 10. 1086/282724)
17. Beibl J, Stuart RJ, Heinze J, Foitzik S. 2005 Six origins of slavery in formicoxenine ants. Insectes Soc. 52, 291-297. (doi: 10. 1007/s00040-005-0808-y)
18. Alloway TM. 1979 Raiding behaviour of two species of slave-making antsHarpagoxenus americanus (Emery) and Leptothorax duloticus Wesson (Hymenoptera: Formicidae). Anim. Behav. 27, 202-210. (doi: 10. 1016/0003-3472(79)90140-4)
19. Foitzik S, Herbers JM. 2001 Colony structure of a slavemaking ant. II. Frequency of slave raids and impact on the host population. Evolution55, 316-323. (doi: 10. 1111/j. 0014-3820. 2001. tb01296. x)
20. Blatrix R, Herbers JM. 2003 Coevolution between slave-making ants and their hosts: host specificity and geographical variation. Mol. Ecol. 12, 2809-2816. (doi: 10. 1046/j. 1365-294X. 2003. 01947. x)
21. Wesson LG. 1939 Contributions to the natural history ofHarpagoxenus americanusEmery (Hymenoptera?: Formicidae). Trans. Am. Entomol. Soc. 65, 97-122.
22. Keller L. 1998 Queen lifespan and colony characteristics in ants and termites. Insectes Soc. 45, 235-246. (doi: 10. 1007/s000400050084)
23. Herbers JM, Foitzik S. 2002 The ecology of slavemaking ants and their hosts in north temperate forests. Ecology83, 148-163. (doi: 10. 1890/0012-9658(2002)083[0148: TEOSAA] 2. 0. CO; 2)
24. Brandt M, Foitzik S. 2004 Community context and specialization influence coevolution between a slavemaking ant and its hosts. Ecology85, 2997-3009. (doi: 10. 1890/03-0778)
25. Foitzik S, Backus VL, Trindl A, Herbers JM. 2004 Ecology ofLeptothorax ants: impact of food nest sites and social parasites. Behav. Ecol. Sociobiol. 55, 484-493. (doi: 10. 1007/s00265-003-0718-9)
26. Foitzik S, Achenbach A, Brandt M. 2009 Locally adapted social parasite affects density social structure and life history of its ant hosts. Ecology 90, 1195-1206. (doi: 10. 1890/08-0520. 1)
27. Bates D, Maechler M, Bolker B. 2012 lme4: linear mixed-effects models using S4 classes. R package version 0. 999999-0. (http: //cran. r-project. org/ package=lme4)
28. R Core Team. 2013 R: a language and environment for statistical computing. Vienna, Austria: R Found. Stat. Comput. (http: //www. r-project. org/)
29. Herbers JM. 1986 Nest site limitation and facultative polygyny in the antLeptothorax longispinosus. Behav. Ecol. Sociobiol. 19, 115-122. (doi: 10. 1007/ BF00299946)
30. Robertson RJ, Norman RF. 1976 Behavioral defences to brood parasitism by potential hosts of the Brown-headed Cowbird. Condor 78166-173. (doi: 10. 2307/1366851)
31. Neudorf DL, Sealy SG. 1992 Reactions of four passerine species to threats of predation and Cowbird parasitism: enemy recognition or generalized responses? Behaviour12384-105. (doi: 10. 1163/156853992X00138)
32. Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HM, Pedersen HC. 1991 Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour11664-89. (doi: 10. 1163/ 156853990X00365)
33. Røskaft E, Moksnes A, Stokke BG, Bicík V, MoskátC. 2002 Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour139613-628. (doi: 10. 1163/15685390260136735)
34. Briskie JV, Sealy SG, Hobson KA. 1992 Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution 46334-340. (doi: 10. 2307/2409854)
35. Hale K, Briskie JV. 2007 Response of introduced European birds in New Zealand to experimental brood parasitism. J. Avian Biol. 38, 198-204. (doi: 10. 1111/j. 2007. 0908-8857. 03734. x)
36. Lindholm AK, Thomas RJ. 2000 Differences between populations of reed warblers in defences against brood parasitism. Behaviour137, 25-42. (doi: 10. 1163/156853900501854)
37. Welbergen JA, Davies NB. 2009 Strategic variation in mobbing as a front line of defense against brood parasitism. Curr. Biol. 19, 235-240. (doi: 10. 1016/j. cub. 2008. 12. 041)
38. Thorogood R, Davies NB. 2013 Reed warbler hosts fine-tune their defenses to track three decades of cuckoo decline. Evolution67, 3545-3555. (doi: 10. 1111/evo. 12213)
39. Kleeberg I, Jongepier E, Foitzik S. In preparation. What shapes collective behavior? Colony aggression depends on context and parasite pressure.
40. Zamora-Munoz C, Ruano F, Errard C, Lenoir A, Hefetz A, Tinaut A. 2003 Coevolution in the slaveparasite systemProformica longiseta-Rossomyrmex minuchae(Hymenoptera: Formicidae). Sociobiology 42, 299-317.
41. Savolainen R, Vepsäläinen K. 1988 A competition hierarchy among boreal ants: impact on resource partitioning and community structure. Oikos51, 135-155. (doi: 10. 2307/3565636)
42. Davies NB, Bourke AFG, Brooke MdeL. 1989 Cuckoos and parasitic ants: interspecific brood parasitism as an evolutionary arms race. Trends Ecol. Evol. 4, 274-278. (doi: 10. 1016/0169-5347(89)90202-4)
43. Moksnes A, Røskaft E, Braa AT. 1991 Rejection behavior by common cuckoo hosts towards artificial brood parasite eggs. Auk108, 348-354.
44. Hosoi S, Rothstein S. 2000 Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim. Behav. 59, 823-840. (doi: 10. 1006/anbe. 1999. 1370)
45. Peer BD, Sealy SG. 2004 Correlates of egg rejection in hosts of the brown-headed cowbird. Condor106, 580-599. (doi: 10. 1650/7412)
46. Mori A, Ettorre RD, Moli EL. 1995 Host nest usurpation and colony foundation in the European amazon antPolyergus rufescensLatr. (Hymenoptera: Formicidae). Insectes Soc. 286, 279-286.
47. Servedio MR, Hauber ME. 2006 To eject or to abandon? Life history traits of hosts and parasites interact to influence the fitness payoffs of alternative anti-parasite strategies. J. Evol. Biol. 19, 1585-1594. (doi: 10. 1111/j. 1420-9101. 2006. 01124. x)
48. Brodie ED, Ridenhour BJ, Brodie ED. 2002 The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution56, 2067-2082. (doi: 10. 1111/j. 0014-3820. 2002. tb00132. x)
49. Thompson JN, Cunningham BM. 2002 Geographic structure and dynamics of coevolutionary selection. Nature417, 735-738. (doi: 10. 1038/nature00810)
50. Gomulkiewicz R, Drown DM, Dybdahl MF, Godsoe W, Nuismer SL, Pepin KM, Ridenhour BJ, Smith CI, Yoder JB. 2007 Dos and don'ts of testing the geographic mosaic theory of coevolution. Heredity (Edinb.) 98, 249-258. (doi: 10. 1038/sj. hdy. 6800949)