Background Territorial boundaries between conspecific social insect colonies are maintained through nestmate recognition systems. However, in supercolony-forming ants, which have developed an extraordinary social organization style known as unicoloniality, a single supercolony extends across large geographic distance. The underlying mechanism is considered to involve less frequent occurrence of intraspecific aggressive behaviors, while maintaining interspecific competition. Thus, we examined whether the supercolony-forming species, Formica yessensis has a nestmate recognition system similar to that of the multicolonial species, Camponotus japonicus with respect to the cuticular hydrocarbon-sensitive sensillum (CHC sensillum), which responds only to non-nestmate CHCs. We further investigated whether the sensory system reflects on the apparent reduced aggression between non-nestmates typical to unicolonial species. Methodology/Principal Findings F. yessensis constructs supercolonies comprising numerous nests and constitutes the largest supercolonies in Japan. We compared the within-colony or between-colonies’ (1) similarity in CHC profiles, the nestmate recognition cues, (2) levels of the CHC sensillar response, (3) levels of aggression between workers, as correlated with geographic distances between nests, and (4) their genetic relatedness. Workers from nests within the supercolony revealed a greater similarity of CHC profiles compared to workers from colonies outside it. Total response of the active CHC sensilla stimulated with conspecific alien CHCs did not increase as much as in case of C. japonicus, suggesting that discrimination of conspecific workers at the peripheral system is limited. It was particularly limited among workers within a supercolony, but was fully expressed for allospecific workers. Conclusions/Significance We demonstrate that chemical discrimination between nestmates and non-nestmates in F. yessensis was not clear cut, probably because this species has only subtle intraspecific differences in the CHC pattern that typify within a supercolony. Such an incomplete chemical discrimination via the CHC sensilla is thus an important factor contributing to decreased occurrence of intraspecific aggressive behavior especially within a supercolony.
References
[1]
Price WP (1975) Insect ecology: New York: Wiley. 514 p.
[2]
H?lldobler B, Wilson OE (1990) The ants. Cambridge: Belknap Press of Harvard University Press. 732 p.
[3]
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: 381–387.
[4]
Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, et al. (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309: 311–314.
[5]
Martin SJ, Vitikainen E, Helanter? H, Drijfhout FP (2008) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc R Soc B 275: 1271–1278.
[6]
Holway AD, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Ann Rev Ecol Syst 33: 181–233.
[7]
Holway AD, Suarez VA, Case JT (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282: 949–952.
[8]
Tsutsui DN, Suarez VA, Holway AD, Case JT (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97: 5948–5953.
[9]
Giraud T, Pedersen SJ, Keller L (2002) Evolution of supercolonies: The Argentine ants of southern Europe. Proc Natl Acad Sci USA 99: 6075–6079.
[10]
Pedersen SJ, Krieger JBM, Vogel V, Giraud TV, Keller L (2006) Native supercolonies of unrelated individuals in the invasive Argentine ant. Evolution 60: 782–791.
[11]
Wetterer JK, Walsh PD, White LJT (1999) Wasmannia auropunctata (Roger) (Hymenoptera: Formicidae), a destructive tramp-ant, in wildlife refuges of Gabon. African Entomol 7: 292–294.
[12]
Jourdan H, Sadlier RA, Bauer AM (2001) Little fire ant invasion (Wasmannia auropunctata) as a threat to New Caledonian lizards: Evidences from a sclerophyll forest (Hymenoptera: Formicidae). Sociobiology 38: 283–301.
[13]
Vonshak M, Dayan T, Foucaud J, Estoup A, Hefetz A (2009) The interplay between genetic and environmental effects on colony insularity in the clonal invasive little fire ant Wasmannia auropunctata. Behav Ecol Sociobiol 63: 1667–1677.
[14]
Vonshak M, Dayan T, Ionescu-Hirsh A, Freidberg A, Hefetz A (2010) The little fire ant Wasmannia auropunctata: a new invasive species in the Middle East and its impact on the local arthropod fauna. Biol Invasions 10.1007/s10530–009–9593–2.
[15]
Silverman J, Liang D (2001) Colony disassociation following diet partitioning in a unicolonial ant. Naturwissenshaften 88: 73–77.
[16]
Torres WC, Brandt M, Tsutsui DN (2007) The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (Linepithema humile). Insect Soc 54: 363–373.
[17]
Higashi S (1976) Nest proliferation by budding and nest growth pattern in Formica (Formica) yessensis in Ishikari shore. Jour Fac Sci Hokkaido Univ Ser VI Zool 20: 359–389.
[18]
Higashi S, Yamauchi K (1979) Influence of a supercolonial ant Formica (Formica) yessensis Forel on the distribution of other ants in Ishikari coast. Jap J Ecol 29: 257–264.
[19]
Cherix D (1980) Note preliminaire sur la structure, la phenologie et le regime alimentaire d’une super-colonie de Formica lugubris Zett. Insectes Soc 27: 226–236.
[20]
Holzer B, Chapuisat M, Kremer N, Finet C, Keller L (2006) Unicoloniality, recognition and genetic differentiation in a native Formica ant. Euro Soc Evol Biol 19: 2031–2039.
[21]
Buczkowski G (2010) Extreme life history plasticity and the evolution of invasive characteristics in a native ant. Biolo Invasions 12: 3343–3349.
[22]
Leniaud L, Hefetz A, Grumiau L, Aron S (2011) Multiple mating and supercoloniality in Cataglyphis desert ants. Biol J Linean Soc 104: 866–876.
[23]
Bonavita-Cougourdan A, Clément LJ, Lange C (1986) Nestmate recognition: the role of cuticular hydrocarbons in the ant Camponotus vagus scop. J Entomol Soc 22: 1–10.
[24]
De Maesschalck R, Jouan-Rimbaud D, Massart LD (2000) The Mahalanobis distance. Chemometr Intell Lab 50: 1–18.
[25]
Ugelvig VL, Drijfhout PF, Kronauer JCD, Boomsma JJ, Pedersen SJ, et al.. (2008) The introduction history of invasive garden ants in Europe: Integrating genetic, chemical and behavioral approaches. BMC Biol 10.1186/1741-7007-6-11.
[26]
Higashi S (1978) Task and areal conservatism and internest drifting in a red wood ant Formica (Formica) yessensis Forel. Jpn J Ecol 28: 307–317.
[27]
Brandt M, van Wilgenburg E, Sulc R, Shea JK, Tsutsui DN (2009) The scent of supercolonies: the discovery, synthesis and behavioral verification of ant colony recognition cues. BMC Biol 10.1186/1741-7007/7/71.
[28]
Guerrieri FJ, Nehring V, J?rgensen CG, Nielsen J, Galizia CG, et al. (2009) Ants recognize foes and not friends. Proc Biol Sci 276: 2461–2468.
[29]
Dahbi A, Cerda X, Hefetz A, Lenoir A (1997) Adult transport in the ant Cataglyphis iberica: a means to maintain a uniform colonial odour in a species with multiple nests. Physiol Entomol 22: 13–19.
[30]
Dahbi A, Lenoir A (1998) Nest separation and the dynamics of the Gestalt odor in the polydomous ant Cataglyphis iberica (Hymenoptera, Formicidae). Behav Ecol Sociobiol 42: 349–355.
[31]
Martin SJ, Helanter? H, Kiss K, Lee YR, Drijfhout FP (2009) Polygyny reduces rather than increases nestmate discrimination cue diversity in Formica exsecta ants. Insect Soc 56: 375–383.
[32]
Brandstaetter AS, R?sser W, Kleinaidam CJ (2011) Friends and foes from an ant brain’s point of view-Neronal correlations of colony odors in a social insect. PloS ONE 6: e21383.
[33]
Vander Meer RK, Saliwanchik D, Lavine B (1989) Temporal changes in colony cuticular hydrocarbon patterns of Solenopsis invicta. J Chem Ecol 15: 2115–2125.
[34]
Provost E, Riviere G, Roux M, Morgan DE, Bagneres GA (1993) Change in the chemical signature of the ant Leptothorax lichtensteini bondroit with time. Insect Biochem Mol Biol 23: 945–957.
[35]
Boulay R, Hefetz A, Soroker V, Lenoir A (2000) Camponotus fellah colony integration: worker individuality necessitates frequent hydrocarbon exchanges. Anim Behav 59: 1127–1133.
[36]
Lahav S, Soroker V, Vander Meer RK, Hefetz A (2001) Segregation of Colony Odor in the Desert Ant Cataglyphis niger. J Chem Ecol 27: 927–943.
[37]
Hildebrand GJ, Shepherd MG (1997) Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Ann Rev Neurosci 20: 595–631.
[38]
Boulay R, Katzav-Gozansky T, Vander Meer RK, Hefets A (2003) Colony insularity through queen social motivation in ants. Proc R Soc Lond, Ser B: Biol Sci 270: 971–977.
[39]
Roeder T (2005) Tyramine and octopamine: Ruling behavior and metabolism. Ann Rev Entomol 50: 447–477.
[40]
Knaden M, Wehner R (2003) Nest Defense and Conspecific Enemy Recognition in the Desert Ant Cataglyphis fortis. J Insect Behav 16: 717–730.
[41]
Sanada-Morimura S, Minai M, Yokoyama M, Hirota T, Satoh T, Obara Y (2003) Encounter-induced hostility to neighbors in the ant Pristomyrmex pungens. Behav Ecol 14: 713–718.
[42]
Leonhardt SD, Brandstaetter AS, Kleineidam CJ (2007) Reformation process of the neural template for nestmate-recognition cues in the carpenter ant Camponotus floridanus. J Comp Physiol A 193: 993–1000.
[43]
Aitchinson J (1986) The statistical analysis of compositional data: Blackburn Press.
[44]
Goodwyn PP, Wada-Katsumata A, Okada K (2009) Morphology and neurophysiology of tarsal vibration receptors in the water strider Aquarius paludum (Heteroptera: Gerridae). J Insect Physiol 55: 855–861.
[45]
Hasegawa E, Imai S (2004) Characterization of microsatellite loci in red wood ants Formica (s. str) spp. and the related genus Polyergus. Mol Ecol Notes 4: 200–203.
[46]
Chapuisat M (1996) Characterization of microsatellite loci in Formica lugubris B and their variability in other at species. Mol Ecol 5: 599–601.
[47]
Gyllenstrand N, Gertsch PJ, Pamilo P (2002) Polymorphic microsatellite DNA markers in the ant Formica excecta. Mol Ecol Notes 2: 67–69.
[48]
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.
[49]
Goudet (2001) FASTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). 42. Raymond F, Rousset M (1995) Testing heterozygote excess and deficiency. Genetics 140: 1413–1419.
Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4: 779–782.