Behavioral Ecology and Sociobiology

, Volume 65, Issue 4, pp 641–653 | Cite as

Kin discriminators in the eusocial sweat bee Lasioglossum malachurum: the reliability of cuticular and Dufour’s gland odours

  • Antonella Soro
  • Manfred Ayasse
  • Marion U. Zobel
  • Robert J. Paxton
Original Paper


The ability to discriminate degrees of relatedness may be expected to evolve if it allows unreciprocated altruism to be preferentially directed towards kin (Hamilton in J Theor Biol 7:1–16, 1964). We explored the possibility of kin recognition in the primitively eusocial halictid bee Lasioglossum malachurum by investigating the reliability of worker odour cues that can be perceived by workers to act as indicators of either nest membership or kinship. Cuticular and Dufour’s gland compounds varied significantly among colonies of L. malachurum, providing the potential for nestmate discrimination. A significant, though weak, negative correlation between chemical distance and genetic relatedness (r = −0.055, p < 0.001) suggests a genetic component to variation in cuticular bouquet, but odour cues were not informative enough to discriminate between different degrees of relatedness within nests. This pattern of variation was similar for Dufour’s gland bouquets. The presence of unrelated individuals within nests that are not chemically different from their nestmates suggests that the discrimination system of L. malachurum is prone to acceptance errors. Compounds produced by colony members are likely combined to generate a gestalt colony chemical signature such that all nestmates have a similar smell. The correlation between odour cues and nest membership was greater for perceived compounds than for non-perceived compounds, suggesting that variability in perceived compounds is a result of positive selection for nestmate recognition despite potentially stabilising selection to reduce variability in odour differences and thereby to reduce costs derived from excessive intracolony nepotistic behaviour.


Recognition Nestmate Halictidae Gas chromatography Electro-antennal detection 

Supplementary material

265_2010_1066_MOESM1_ESM.doc (160 kb)
ESM 1 Online Supplementary Material (DOC 160 kb)


  1. Aitchinson J (1986) The statistical analysis of compositional data. Chapman & Hall, LondonGoogle Scholar
  2. Akino T, Yamamura K, Wakamura S, Yamaoka R (2004) Direct behavioural evidence for hydrocarbons as nestmate recognition cues in Formica japonica (Hymenoptera; Formicidae). Appl Entomol Zool 39:381–387CrossRefGoogle Scholar
  3. Arnold G, Quenet B, Cornuet JM, Masson C, De Schepper B, Estoup A, Gasqui P (1996) Kin recognition in honeybees. Nature 379:498CrossRefGoogle Scholar
  4. Arnold G, Quenet B, Masson C (2000) Influence of social environment on genetically based subfamily signature in the honeybee. J Chem Ecol 26:2321–2333CrossRefGoogle Scholar
  5. Ayasse M (1990a) Odor based interindividual and nest recognition in the sweat bee Lasioglossum malachurum (Hymenoptera: Halictidae). In: Veeresh GK et al (eds) Social insects and the environment. Oxford & IBH, New Delhi, pp 511–512Google Scholar
  6. Ayasse M (1990b) Visuelle und olfatorische Orientierung in der Nestfindung bei Lasioglossum malachurum (Hymenoptera: Halictidae). Apidologie 21:349–351Google Scholar
  7. Ayasse M (1991) Chemische Kommunikation bei der primitiv eusozialen Furchenbiene Lasioglossum malachurum (Halictidae): Ontogenese kastenspezifischer Duftstoffbouquets, Paarungsbiologie und Nesterkennung. Eberhard-Karls-Universität Tübingen, TübingenGoogle Scholar
  8. Ayasse M, Engels W, Hefetz A, Lübke G, Francke W (1990) Ontogenetic patterns in amounts and proportions of Dufour gland volatile secretions in virgin and nesting queens of Lasioglossum malachurum (Hymenoptera, Halictidae). Z Naturforsch 45:709–714Google Scholar
  9. Ayasse M, Engels W, Hefetz A, Tengö J, Lübke G, Francke W (1993) Ontogenetic patterns of volatiles identified in Dufour’s gland extracts from queens and workers of the primitively eusocial halictine bee, Lasioglossum malachurum (Hymenoptera: Halictidae). Insectes Soc 40:41–58CrossRefGoogle Scholar
  10. Ayasse M, Engels W, Lübke G, Taghizadeh T, Francke W (1999) Mating expenditures reduced via female sex pheromone modulation in the primitively eusocial halictine bee, Lasioglossum (Evylaeus) malachurum (Hymenoptera: Halictidae). Behav Ecol Sociobiol 45:95–106CrossRefGoogle Scholar
  11. Ayasse M, Paxton RJ, Tengö J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78PubMedCrossRefGoogle Scholar
  12. Boomsma JJ, Nielsen J, Sundström L, Oldham NJ, Tentschert J, Petersen HC, Morgan D (2003) Informational constrains on optimal sex allocation in ants. Proc Natl Acad Sci USA 100:8799–8804PubMedCrossRefGoogle Scholar
  13. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  14. Breed MD (1998) Chemical cues in kin recognition: criteria for identification, experimental approaches, and the honey bee as an example. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview, Boulder, pp 56–78Google Scholar
  15. Breed MD, Bennet B (1987) Kin recognition in highly eusocial insects. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, Chichester, pp 243–285Google Scholar
  16. Brooks RW, Cane JH (1984) Origin and chemistry of the secreted nest entrance lining of Halictus hesperus (Hymenoptera: Apoidea). J Kansas Entomol Soc 57:161–165Google Scholar
  17. Buchwald R, Breed MD (2005) Nestmate recognition cues in a stingless bee, Trigona fulviventris. Anim Behav 70:1331–1337CrossRefGoogle Scholar
  18. Buckle GR, Greenberg L (1981) Nestmate recognition in sweat bees (Lasioglossum zephyrum): does an individual recognize its own odours or only odours of its nestmates? Anim Behav 29:802–809CrossRefGoogle Scholar
  19. Carlin NF, Hölldobler B (1983) Nestmate and kin recognition in interspecific mixed colonies of ants. Science 222:1027–1029PubMedCrossRefGoogle Scholar
  20. Carlin NF, Hölldobler B (1986) The kin recognition system of carpenter ants (Camponotus spp.). I. Hierarchical cues in small colonies. Behav Ecol Sociobiol 19:123–134CrossRefGoogle Scholar
  21. Cornwallis CK, West SA, Griffin AS (2009) Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. J Evol Biol 22:2445–2457PubMedCrossRefGoogle Scholar
  22. Couvillon MJ, Ratnieks FLW (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable–absent” recognition system. Behav Ecol Sociobiol 62:1099–1105CrossRefGoogle Scholar
  23. Crozier RH (1987) Genetic aspects of kin recognition. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, New York, pp 55–73Google Scholar
  24. Crozier RH, Dix MW (1979) Analysis of two genetic models for the innate components of colony odor in social Hymenoptera. Behav Ecol Sociobiol 4:217–224CrossRefGoogle Scholar
  25. Dani FR, Foster KF, Zacchi F, Seppä P, Massolo A, Carelli A, Arévalo E, Queller DC, Strassmann J, Turillazzi S (2004) Can cuticular lipids provide sufficient information for within-colony nepotism in wasps. Proc R Soc B 271:745–753PubMedCrossRefGoogle Scholar
  26. 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 30:477–489PubMedCrossRefGoogle Scholar
  27. 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 62:165–171CrossRefGoogle Scholar
  28. Fletcher DJC, Michener CD (1987) Kin recognition in animals. Wiley, Chichester, p 465Google Scholar
  29. Grafen A (1990) Do animals really recognize kin? Anim Behav 39:42–54CrossRefGoogle Scholar
  30. Greenberg L (1979) Genetic component of bee odor in kin recognition. Science 206:1095–1097PubMedCrossRefGoogle Scholar
  31. Guerrieri FJ, Nehring V, Jørgensen CG, Nielsen J, Galizia CG, D’Ettorre P (2009) Ants recognize foes and not friends. Proc R Soc B 276:2461–2468PubMedCrossRefGoogle Scholar
  32. Hamilton WD (1964) The genetical evolution of social behaviour I. & II. J Theor Biol 7:1–16, 17–52PubMedCrossRefGoogle Scholar
  33. Hamilton WD (1987) Discrimination nepotism: expectable, common, overlooked. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, New York, pp 417–437Google Scholar
  34. Hefetz A (1987) The role of Dufour’s gland secretions in bees. Physiol Entomol 12:243–253CrossRefGoogle Scholar
  35. Hefetz A (1998) Exocrine glands and their products in non-Apis bees: chemical, functional and evolutionary perspectives. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview, BoulderGoogle Scholar
  36. Hefetz A, Bergström G, Tengo J (1986) Species, individual and kin specific blends in Dufour’s gland secretions of halictine bees—chemical evidence. J Chem Ecol 12:197–208CrossRefGoogle Scholar
  37. Howard RW, Blomquist GJ (2005) Ecological, behavioral and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393PubMedCrossRefGoogle Scholar
  38. Hölldobler B, Wilson EO (1990) The ants. Springer, BerlinGoogle Scholar
  39. Jackson LL, Blomquist GJ (1976) Insect waxes. In: Kolattukudy PE (ed) Chemistry and biochemistry of natural waxes. Elsevier, Amsterdam, pp 201–203Google Scholar
  40. Kaminski G, Dridi S, Graff C, Gentaz E (2009) Human ability to detect kinship in strangers’ faces: effects of the degree of relatedness. Proc R Soc B 1670:3193–3200. doi: 10.1098/rspb.2009.0677 CrossRefGoogle Scholar
  41. Keller L (1997) Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol Evol 12:99–103PubMedCrossRefGoogle Scholar
  42. Keller L, Reeve HK (1999) Dynamics of conflicts within insect societies. In: Keller L (ed) Levels of selections in evolution. Princeton University Press, Princeton, pp 153–175Google Scholar
  43. Knerer G (1992) The biology and social behaviour of Evylaeus malachurus (K.) (Hymenoptera; Halictidae) in different climatic conditions of Europe. Zoologishes Jahrbuch für Systematik 119:261–290Google Scholar
  44. Kukuk PF, Crozier RH (1990) Trophallaxis in a communal halictine bee Lasioglossum (Chilalictus) erythrurum. Proc Natl Acad Sci USA 87:5402–5404PubMedCrossRefGoogle Scholar
  45. Lahav S, Soroker V, Hefetz A, Vander Meer RK (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminator. Naturwissenschaften 86:246–249CrossRefGoogle Scholar
  46. Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants: the emergence of the social representation concept. In: Detrain C, Deneubourg J-L, Pasteels JM (eds) Information processing in social insects. Birkhäuser, BaselGoogle Scholar
  47. Liebig J, Peeters C, Oldham NJ, Markstädter C, Hölldobler B (2000) Are variation in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc Natl Acad Sci USA 97:4124–4131PubMedCrossRefGoogle Scholar
  48. Lihoreau M, Rivault C (2008) Kin recognition via cuticular hydrocarbons shapes cockroach social life. Behav Ecol 20:46–53CrossRefGoogle Scholar
  49. Lorenzi M-C, Bagnères A-G, Clément J-L (1996) The role of cuticular hydrocarbons in social insects: is it the same in paper-wasps? In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper-wasps. Oxford University Press, Oxford, pp 178–189Google Scholar
  50. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  51. Martin SJ, Vitikainen E, Helanterä H, Drijfhout FP (2008) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc R Soc B 275:1271–1278PubMedCrossRefGoogle Scholar
  52. Martin SJ et al (2009) Polygyny reduces rather than increases nestmate discrimination cue diversity in Formica exsecta ants. Insectes Soc 56:375–383CrossRefGoogle Scholar
  53. Mas F, Hayne KF, Kölliker M (2009) A chemical signal of offspring quality affects maternal care in a social insect. Proc R Soc B 276:2847–2853. doi: 10.1098/rspb.2009.0498 PubMedCrossRefGoogle Scholar
  54. Michener CD (1974) The social behavior of the bees. A comparative study. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  55. Michener CD, Smith BH (1987) Kin recognition in primitively eusocial insects. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, Chichester, pp 209–242Google Scholar
  56. Nunes TM, Nascimento TM, Turatti IC, Lopes NP, Zucchi R (2008) Nestmate recognition in a stingless bee: does the similarity of chemical cues determine guard acceptance? Anim Behav 75:1165–1171CrossRefGoogle Scholar
  57. Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nest mate and non-nest mate discrimination by a chemosensory sensillium. Science 309:311–315PubMedCrossRefGoogle Scholar
  58. Packer L, Knerer G (1985) Social evolution and its correlates in bees of the subgenus Evylaeus (Hymenoptera; Halictidae). Behav Ecol Sociobiol 17:143–149Google Scholar
  59. Paxton RJ, Ayasse M, Field J, Soro A (2002) Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee, Lasioglossum malachurum, as revealed by microsatellites. Mol Ecol 11:2405–2416PubMedCrossRefGoogle Scholar
  60. Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlate with reproductive status in a queenless ant. Proc R Soc Lond B 266:1323–1327CrossRefGoogle Scholar
  61. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  62. Ratnieks FLW, Reeve HK (1992) Conflict in single-queen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J Theor Biol 158:33–65CrossRefGoogle Scholar
  63. Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435CrossRefGoogle Scholar
  64. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  65. Richards MH (2000) Evidence for geographic variation in colony social organization in an obligately social sweat bee, Lasioglossum malachurum Kirby (Hymenoptera; Halictidae). Can J Zool 78:1259–1266CrossRefGoogle Scholar
  66. Richards MH, French D, Paxton RJ (2005) It’s good to be queen: classically eusocial colony structure and low worker fitness in a obligately social sweat bee. Mol Ecol 14:4123–4133PubMedCrossRefGoogle Scholar
  67. Ryan PD, Harper DAT, Whalley JS (1995) PALSTAT, statistics for paleontologists. Chapman & Hall, LondonGoogle Scholar
  68. Schwarz MP, Richards MH, Danforth BN (2007) Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Ann Rev Entomol 52:127–150CrossRefGoogle Scholar
  69. Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson B, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–422CrossRefGoogle Scholar
  70. Segoli M, Keasar T, Harari AR, Bouskil A (2009) Limited kin discrimination abilities mediate tolerance toward relatives in polyembryonic parasitoid wasps. Behav Ecol 20:1262–1267CrossRefGoogle Scholar
  71. Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology. Blackwell Science, Oxford, pp 69–96Google Scholar
  72. Singer TL (1998) Roles of hydrocarbons in the recognition systems of insects. Am Zool 38:394–405Google Scholar
  73. Singer TL, Espelie KE, Gamboa GJ (1998) Nest and nestmate discrimination in independent-founding in paper wasps. In: Vander Meer RK, Breed MD, Winston ML, Espelie KE (eds) Pheromone communication in social insects: ants, wasps, bees, and termites. Westview, Boulder, pp 104–125Google Scholar
  74. Sledge MF, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409CrossRefGoogle Scholar
  75. Smith BH, Ayasse M (1987) Kin-based male mating preferences in two species of halictine bees. Behav Ecol Sociobiol 20:313–318CrossRefGoogle Scholar
  76. Smith BH, Breed MD (1995) The chemical basis for nest-mate recognition and mate discrimination in social insects. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects 2. Chapman & Hall, London, pp 287–317Google Scholar
  77. Smith BH, Weller C (1989) Social competition among gynes in halictine bees: the influence of bee size and pheromones on behavior. J Insect Behav 2:397–411CrossRefGoogle Scholar
  78. Smith BH, Wenzel JW (1988) Pheromonal covariation and kinship in social bee Lasioglossum zephyrum (Hymenoptera: Halictidae). J Chem Ecol 14:87–94CrossRefGoogle Scholar
  79. Smith AA, Hölldobler B, Liebig J (2009) Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol 19:78–81PubMedCrossRefGoogle Scholar
  80. Soro A, Ayasse M, Zobel MU, Paxton RJ (2009) Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum. Insectes Soc 56:55–63CrossRefGoogle Scholar
  81. Steiger S, Peschke K, Francke W, Müller JK (2007) The smell of parents: breeding status influences cuticular hydrocarbon pattern in the burying beetle Nicrophorus vespilloides. Proc R Soc B-274:2211–2220Google Scholar
  82. Toolson EC, Kuper-Simbrón R (1989) Laboratory evolution of epicuticular hydrocarbons composition and cuticular permeability in Drosophila pseudoobscura: effects on sexual dimorphism and thermal-acclimation ability. Evolution 43:468–473CrossRefGoogle Scholar
  83. Torres CW, Brandt M, Tsutsui ND (2007) The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (Linepithema humile). Insectes Soc 54:363–373CrossRefGoogle Scholar
  84. van Wilgenburg E, Sulc R, Shea KJ, Tsutsui ND (2010) Deciphering the chemical basis of nestmate recognition. J Chem Ecol 36:751–758PubMedCrossRefGoogle Scholar
  85. van Zweden JS, Dreier S, D’Ettorre P (2009) Disentangling environmental and heritable nestmate recognition cues in a carpenter ant. J Insect Physiol 55:159–164CrossRefGoogle Scholar
  86. Walker JT (1999) Statistics in criminal justice. Aspen, GaithersburgGoogle Scholar
  87. Weisfeld GE, Czilli T, Phillips KA, Gall JA, Lichtman CM (2003) Possible olfaction-based mechanisms in human kin recognition and inbreeding avoidance. J Experimental Child Psychology 85:279–295CrossRefGoogle Scholar
  88. Westrich P (1989) Die Wildbienen Baden Württembergs. Verlag Eugen Ulmer, StuttgartGoogle Scholar
  89. Wyman LM, Richards MH (2003) Colony social organisation of Lasioglossum malachurum Kirby (Hymenoptera, Halictidae) in southern Greece. Insectes Soc 50:1–12CrossRefGoogle Scholar
  90. Zimma BO, Ayasse M, Tengo J, Ibarra F, Schulz C, Francke W (2003) Do social parasitic bumblebees use chemical weapons? (Hymenoptera, Apidae). J Comp Physiol A 189:769–775CrossRefGoogle Scholar
  91. Zobel M, Paxton RJ (2007) Is big the best? Queen size, usurpation and nest closure of a primitively eusocial sweat bee (Lasioglossum malachurum). Behav Ecol Sociobiol 61:435–447CrossRefGoogle Scholar
  92. van Zweden JS, Brask JB, Christensen JH, Boomsma JJ, Linksvayer TA, d’Ettorre P (2010) Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism. J Evol Biol 23:1498–1508PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Antonella Soro
    • 1
    • 2
    • 4
  • Manfred Ayasse
    • 3
  • Marion U. Zobel
    • 1
  • Robert J. Paxton
    • 2
    • 4
  1. 1.Animal Physiological EcologyUniversity of TübingenTübingenGermany
  2. 2.School of Biological SciencesQueen’s University BelfastBelfastUK
  3. 3.Institute of Experimental EcologyUniversity of UlmUlmGermany
  4. 4.Institute for BiologyMartin-Luther-University Halle-WittenbergHalleGermany

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