Abstract
Social insects have developed sophisticated recognition skills to defend their nests against intruders. They do this by aggressively discriminating against non-nestmates with deviant cuticular hydrocarbon (CHC) signatures. Studying nestmate recognition can be challenging as individual insects do not only vary in their discriminatory abilities, but also in their motivation to behave aggressively. To disentangle the influence of signaling and behavioral motivation on nestmate recognition, we investigated the ant Temnothorax nylanderi, where the presence of tapeworm-infected nestmates leads to reduced nestmate recognition among uninfected workers. The parasite-induced decline in nestmate recognition could be caused by higher intra-colonial cue diversity as tapeworm-infected workers are known to exhibit a modified hydrocarbon signature. This in turn may broaden the neuronal template of their nestmates, leading to a higher tolerance towards alien conspecifics. To test this hypothesis, we exchanged infected ants between colonies and analyzed their impact on CHC profiles of uninfected workers. We demonstrate that despite frequent grooming, which should promote the transfer of recognition cues, CHC profiles of uninfected workers neither changed in the presence of tapeworm-infected ants, nor did it increase cue diversity among uninfected nestmates within or between colonies. However, CHC profiles were systematically affected by the removal of nestmates and addition of non-nestmates, independently from the ants’ infection status. For example, when non-nestmates were present workers expressed more dimethyl alkanes and higher overall CHC quantities, possibly to achieve a better distinction from non-nestmates. Workers showed clear task-specific profiles with tapeworm-infected workers resembling more closely young nurses than older foragers. Our results show that the parasite-induced decline in nestmate recognition is not due to increased recognition cue diversity or altered CHC profiles of uninfected workers, but behavioral changes might explain tolerance towards intruders.
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References
Akino T, Yamamura K, Wakamura S, Yamaoka R (2004) Direct behavioral evidence for hydrocarbons as nestmate recognition cues in Formica japonica (Hymenoptera: Formicidae). Appl Entomol Zool 39(3):381–387. doi:10.1303/aez.2004.381/10.1303/ae
Aubert A, Richard FJ (2008) Social management of LPS-induced inflammation in Formica polyctena ants. Brain Behav Immun 22(6):833–837. doi:10.1016/j.bbi.2008.01.010
Baracchi D, Fadda A, Turillazzi S (2012) Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J Insect Physiol 58(12):1589–1596. doi:10.1016/j.jinsphys.2012.09.014
Bauer S, Böhm M, Witte V, Foitzik S (2010) An ant social parasite in-between two chemical disparate host species. BMC Evol Biol 24(2):317–332. doi:10.1007/s10682-009-9308-2
Beros S, Jongepier E, Hagemeier F, Foitzik S (2015) The parasite’s long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host. P Roy Soc B-Biol Sci 282 (1819): 1473. doi: 10.1098/rspb.2015.1473
Beye M, Neumann P, Chapuisat M, Pamilo P, Moritz RFA (1998) Nestmate recognition and the genetic relatedness of nests in the ant Formica pratensis. Behav Ecol Sociobiol 43(1):67–72. doi:10.1007/s002650050467
Bonavita-Cougourdan A, Clement JL, Lange C (1993) Functional subcaste discrimination (foragers and brood-tenders) in the ant Camponotus vagus scop: polymorphism of cuticular hydrocarbon patterns. J Chem Ecol 19(7):1461–1477. doi:10.1007/BF00984890
Bos N, Lefevre T, Jensen AB, d’Ettorre P (2012) Sick ants become unsociable. J Evol Biol 25(2):342–351. doi:10.1111/j.1420-9101.2011.02425.x
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(3):576–586. doi:10.1111/j.1420-9101.2004.00867.x
Cini A, Gioli L, Cervo R (2009) A quantitative threshold for nest-mate recognition in a paper social wasp. Biol Lett 5(4):459–461. doi:10.1098/rsbl.2009.0140
Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:693–702. doi:10.1016/j.cub.2007.06.008
Crozier R, Dix MW (1979) Analysis of two genetic models for the innate components of colony odor in social hymenoptera. Behav Ecol Sociobiol 4(3):217–224. doi:10.1007/BF00297645
Csata E, Timus N, Witek M, Casacci LP, Lucas C, Bagnères AG, Sztencel-Jablonka A, Barbero F, Bonelli S, Rákosy L, Markó B (2017) Lock-picks: fungal infection facilitates the intrusion of strangers into ant colonies. Sci Rep UK 7:46323. doi:10.1038/srep46323
Cuvillier-Hot V, Cobb M, Malosse C, Peeters C (2001) Sex, age and ovarian activity affect cuticular hydrocarbons in Diacamma ceylonense, a queenless ant. J Insect Physiol 47(4):485–493. doi:10.1016/S0022-1910(00)00137-2
Dani FR, Jones GR, Destri S, Spencer SH, Turillazzi S (2001) Deciphering the recognition signature within the cuticular chemical profile of paper wasps. Anim Behav 62(1):165–171. doi:10.1006/anbe.2001.1714
Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazzi S (2005) Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 30(6):477–489. doi:10.1093/chemse/bji040
Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39(7):840–859. doi:10.1007/s10886-013-0306-z
De Moraes CM, Stanczyk NM, Betz HS, Pulido H, Sim DG, Read AF, Mescher MC (2014) Malaria-induced changes in host odors enhance mosquito attraction. Proc Natl Acad Sci U S A 111:11079–11084. doi:10.1073/pnas.1405617111
Di Mauro G, Perez M, Lorenzi MC, Guerrieri FJ, Millar JG, d’Ettorre P (2015) Ants discriminate between different hydrocarbon concentrations. Front Evol Ecol 3:133. doi:10.3389/fevo.2015.00133
Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci U S A 100(18):10341–10346. doi:10.1073/pnas.1834281100
Errard C (1994) Development of interspecific recognition behavior in the ants Manica rubida and Formica selysi (Hymenoptera: Formicidae) reared in mixed-species groups. J Insect Behav 7(1):83–99. doi:10.1007/BF01989829
Errard C, Hefetz A, Jaisson P (2006) Social discrimination tuning in ants: template formation and chemical similarity. Behav Ecol Sociobiol 59(3):353–363. doi:10.1007/s00265-005-0058-z
Esponda F, Gordon DM (2015) Distributed nestmate recognition in ants. Proc R Soc B 282:20142838. doi:10.1098/rspb.2014.2838
Feldmeyer B, Mazur J, Beros S, Lerp H, Binder H, Foitzik S (2016) Gene expression patterns underlying parasite-induced alterations in host behaviour and life history. Mol Ecol 25(2):648–660. doi:10.1111/mec.13498
Foitzik S, Heinze J (1998) Nest site limitation and colony takeover in the ant Leptothorax nylanderi. Behav Ecol 9(4):367–375. doi:10.1093/beheco/9.4.367
Foitzik S, Heinze J (2001) Microgeographic genetic structure and intraspecific parasitism in the ant Leptothorax nylanderi. Ecol Entomol 26(5):449–456. doi:10.1046/j.1365-2311.2001.00354.x
Foitzik S, Sturm H, Pusch K, d’Ettorre P, Heinze J (2007) Nestmate recognition and intraspecific chemical and genetic variation in Temnothorax ants. Anim Behav 73(6):999–1007. doi:10.1016/j.anbehav.2006.07.017
Gibbs A (1995) Physical properties of insect cuticular hydrocarbons: model mixtures and lipid interactions. Comp Biochem Physiol B 112(4):667–672. doi:10.1016/0305-0491(95)00119-0
Gibbs A, Pomonis JG (1995) Physical properties of insect cuticular hydrocarbons: the effects of chain length, methyl-branching and unsaturation. Comp Biochem Physiol B 112(2):243–249. doi:10.1016/0305-0491(95)00081-X
Greene MJ, Gordon DM (2003) Social insects: cuticular hydrocarbons inform task decisions. Nature 423(6935):32–32. doi:10.1038/423032a
Guerrieri FJ, Nehring V, Jørgensen JG, Nielsen J, Galizia CG, d’Ettorre P (2009) Ants recognize foes and not friends. Proc R Soc B 276:2461–2468. doi:10.1098/rspb.2008.1860
Heinze J, Walter B (2010) Moribund ants leave their nests to die in social isolation. Curr Biol 20(3):249–252. doi:10.1016/j.cub.2009.12.031
Heinze J, Foitzik S, Hippert A, Hölldobler B (1996) Apparent dear-enemy phenomenon and environment-based recognition cues in the ant Leptothorax nylanderi. Ethology 102(3):510–522. doi:10.1111/j.1439-0310.1996.tb01143.x
Jongepier E, Foitzik S (2016) Ant recognition cue diversity is higher in the presence of slavemaker ants. Behav Ecol 27(1):304–311. doi:10.1093/beheco/arv153
Kather R, Drijfhout FP, Martin SJ (2011) Task group differences in cuticular lipids in the honey bee Apis mellifera. J Chem Ecol 37(2):205–212. doi:10.1007/s10886-011-9909-4
Katzav-Gozansky T, Boulay R, Ionescu-Hirsh A, Hefetz A (2008) Nest volatiles as modulators of nestmate recognition in the ant Camponotus fellah. J Insect Physiol 54:378–385. doi:10.1016/j.jinsphys.2007.10.008
Kleeberg I, Menzel F, Foitzik S (2017) The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons. P Roy Soc B-Biol Sci 284(1850):20162249. doi:10.1098/rspb.2016.2249
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 immunization in ant colonies. PLoS Biol 10(4):e1001300. doi:10.1371/journal.pbio.1001300
Lahav S, Soroker V, Hefetz A, Vander Meer RK (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86(5):246–249. doi:10.1007/s001140050609
Larsen J, Fouks B, Bos N, d’Ettorre P, Nehring V (2014) Variation in nestmate recognition ability among polymorphic leaf-cutting ant workers. J Insect Physiol 70:59–66. doi:10.1016/j.jinsphys.2014.09.002
Lenoir A, d’Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599. doi:10.1146/annurev.ento.46.1.573
Leonhardt SD, Brandstaetter AS, Kleineidam CJ (2007) Reformation process of the neuronal template for nestmate-recognition cues in the carpenter ant Camponotus floridanus. J Comp Physiol 193(9):993–1000. doi:10.1007/s00359-007-0252-8
Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164(6):1277–1287. doi:10.1016/j.cell.2016.01.035
Liang D, Silverman J (2000) “You are what you eat”: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87(9):412–416. doi:10.1007/s001140050752
López JH, Riessberger-Gallé U, Crailsheim K, Schuehly W (2017) Cuticular hydrocarbon cues of immune-challenged workers elicit immune activation in honeybee queens. Mol Ecol 26(11):3062–3073. doi:10.1111/mec.14086
Martin SJ, Drijfhout FP (2009) Nestmate and task cues are influenced and encoded differently within ant cuticular hydrocarbon profiles. J Chem Ecol 35(3):368–374. doi:10.1007/s10886-009-9612-x
Mas F, Haynes KF, Kölliker M (2009) A chemical signal of offspring quality affects maternal care in a social insect. P Roy Soc B-Biol Sci 276(1668):2847–2853. doi:10.1098/rspb.2009.0498
McDonnell CM, Alaux C, Parrinello H, Desvignes JP, Crauser D, Durbesson E, Beslay D, Le Conte Y (2013) Ecto- and endoparasite induce similar chemical and brain neurogenomic responses in the honey bee (Apis mellifera). BMC Ecol 13(1):1. doi:10.1186/1472-6785-13-25
Mersch DP, Crespi A, Keller L (2013) Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340(6136):1090–1093. doi:10.1126/science.1234316
Modlmeier AP, Pamminger T, Foitzik S, Scharf I (2012) Cold resistance depends on acclimation and behavioral caste in a temperate ant. Naturwissenschaften 99(10):811–819. doi:10.1007/s00114-012-0963-8
Morel L, Vander Meer RK, Lofgren CS (1990) Comparison of nestmate recognition between monogyne and polygyne populations of Solenopsis invicta (hymenoptera: Formicidae). Ann Entomol Soc A 83(3):642–647. doi:10.1093/aesa/83.3.642
Newey P (2011) Not one odour but two: a new model for nestmate recognition. J Theor Biol 270(1):7–12. doi:10.1016/j.jtbi.2010.10.029
Newey PS, Robson SK, Crozier RH (2010) Know thine enemy: why some weaver ants do but others do not. Behav Ecol 21(2):381–386. doi:10.1093/beheco/arp201
Pamminger T, Foitzik S, Kaufmann KC, Schützler N, Menzel F (2014) Worker personality and its association with spatially structured division of labor. PLoS One 9(1):e79616. doi:10.1371/journal.pone.0079616
R Core Team (2012) R: a language and environment for statistical computing. R Found. Stat. Comput, Vienna, Austria. isbn:3-900051-07-0
Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435
Richard FJ, Aubert A, Grozinger CM (2008) Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 6(1):1. doi:10.1186/1741-7007-6-50
Roulston TH, Buczkowski G, Silverman J (2003) Nestmate discrimination in ants: effect of bioassay on aggressive behavior. Insect Soc 50(2):151–159. doi:10.1007/s00040-003-0624-1
Rueppell O, Hayworth MK, Ross NP (2010) Altruistic self-removal of health-comprised honey bee workers from their hive. J Evol Biol 23(7):1538–1546. doi:10.1111/j.1420-9101.2010.02022.x
Salvy M, Martin C, Bagneres AG, Provost E, Roux M, Le Conte Y, Clement JL (2001) Modifications of the cuticular hydrocarbon profile of Apis mellifera worker bees in the presence of the ectoparasitic mite Varroa jacobsoni in brood cells. Parasitology 122(02):145–159. doi:10.1017/S0031182001007181
Scharf I, Modlmeier AP, Beros S, Foitzik S (2012) Ant societies buffer individual-level effects of parasite infections. Am Nat 180:671–683. doi:10.1086/667894
Soroker V, Vienne C, Hefetz A (1995) Hydrocarbon dynamics within and between nestmates in Cataglyphis niger (Hymenoptera: Formicidae). J Chem Ecol 21(3):365–378. doi:10.1007/BF02036724
Stuart RJ (1988) Collective cues as a basis for nestmate recognition in polygynous leptothoracine ants. P Natl Acad Sci USA 85(12):4572–4575
Sturgis SJ, Gordon DM (2012) Aggression is task dependent in the red harvester ant (Pogonomyrmex barbatus). Behav Ecol 24(2):532–539. doi:10.1093/beheco/ars194
Tanner CJ, Adler FR (2009) To fight or not to fight: context-dependent interspecific aggression in competing ants. Anim Behav 77(2):297–305. doi:10.1016/j.anbehav.2008.10.016
Trabalon M, Plateaux L, Péru L, Bagnères AG, Hartmann N (2000) Modification of morphological characters and cuticular compounds in worker ants Leptothorax nylanderi induced by endoparasite Anomotaenia brevis. J Insect Physiol 46:169–178. doi:10.1016/S0022-1910(99)00113-4
van Wilgenburg E, Felden A, Choe DH, Sulc R, Luo J, Shea KJ, Elgar MA, Tsutsui ND (2011) Learning and discrimination of cuticular hydrocarbons in a social insect. Biol Lett. doi:10.1098/rsbl.2011.0643
van Zweden JS, d'Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge University Press, Cambridge, pp 222–243
Vienne NC, Soroker V, Hefetz A (1995) Congruency of hydrocarbon patterns in heterospecific groups of ants: transfer and/or biosynthesis? Insect Soc 42(3):267–277. doi:10.1007/BF01240421
Wagner D, Brown MJ, Broun P, Cuevas W, Moses LE, Chao DL, Gordon DM (1998) Task-related differences in the cuticular hydrocarbon composition of harvester ants. Pogonomyrmex barbatus. J Chem Ecol 24(12):2021–2037. doi:10.1023/A:1020781508889
Wagner D, Tissot M, Cuevas W, Gordon DM (2000) Harvester ants utilize cuticular hydrocarbons in nestmate recognition. J Chem Ecol 26(10):2245–2257. doi:10.1023/A:1005529224856
Wakonigg G, Eveleigh L, Arnold G, Crailsheim K (2000) Cuticular hydrocarbon profiles reveal age-related changes in honey bee drones (Apis mellifera carnica). J Apic Res 39(4–3):137–141. doi:10.1080/00218839.2000.11101033
Walker TN, Hughes WHO (2009) Adaptive social immunity in leaf-cutting ants. Biol Lett 5:446–448. doi:10.1098/rsbl.2009.0107
Acknowledgements
We thank Cecilia Felicia Gall for data collection and Inon Scharf for helpful comments on the manuscript.
Funding
This work was funded by the German Research Foundation (DFG; grant numbers: FO 298/15–1 and ME 2842/3–1).
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Beros, S., Foitzik, S. & Menzel, F. What are the Mechanisms Behind a Parasite-Induced Decline in Nestmate Recognition in Ants?. J Chem Ecol 43, 869–880 (2017). https://doi.org/10.1007/s10886-017-0880-6
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DOI: https://doi.org/10.1007/s10886-017-0880-6