Evolution of Caste-Specific Chemical Profiles in Halictid Bees
Chemical communication is crucial for the maintenance of colony organization in eusocial insects and chemical signals are known to mediate important aspects of their social life, including the regulation of reproduction. Sociality is therefore hypothesized to be accompanied by an increase in the complexity of chemical communication. However, little is known about the evolution of odor signals at the transition from solitary living to eusociality. Halictid bees are especially suitable models to study this question as they exhibit considerable variability in social behavior. Here we investigated whether the dissimilarities in cuticle chemical signals in females of different castes and life stages reflect the level of social complexity across halictid bee species. Our hypothesis was that species with a higher social behavior ergo obligate eusocial species possess a more distinct chemical profile between castes or female life stages. We analyzed cuticular chemical profiles of foundresses, breeding females and workers of ancestrally solitary species, facultative and obligate eusocial halictid species. We also tested whether social complexity was associated with a higher investment in chemical signals. Our results revealed higher chemical dissimilarity between castes in obligate than in facultative eusocial species, especially regarding macrocyclic lactones, which were the single common compound class overproduced in queens compared with workers. Chemical dissimilarities were independent of differences in ovarian status in obligate eusocial species but were dependent on ovarian status in facultative eusocial species, which we discuss in an evolutionary framework.
KeywordsSweat bees Communication Social organization Eusociality Sociobiology Chemical distance Fertility signals Macrocyclic lactones
The authors thank Antonella Soro, Bill Wcislo and Beryl Jones for their helpful collaboration and collection of samples, Laura Campos for assistance in collecting and analyzing some of the data and Jonas Kuppler as well as two anonymous reviewers and Etya Ansalem for helpful comments on the manuscript. We acknowledge Stefan Schulz for his help in structure elucidation. Callum Kingwell was funded by scholarships from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Smithsonian Tropical Research Institute (STRI) and Iris Steitz by a scholarship from the Studienstiftung des Deutschen Volkes.
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Conflict of Interest
The authors declare that they have no conflict of interest.
- 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). Insect Soc 40:41–58. https://doi.org/10.1007/BF01338831 CrossRefGoogle Scholar
- 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 45:95–106. https://doi.org/10.1007/s002650050543 CrossRefGoogle Scholar
- Blum MS (1996) Semiochemical parsimony in the Arthropoda. Annu Rev Entomol 41:353–374. https://doi.org/10.1146/annurev.en.41.010196.002033 CrossRefPubMedGoogle Scholar
- Clarke KR, Gorley RN (2006) PRIMER V6: user manual-tutorial. Plymouth Marine Laboratory, PlymouthGoogle Scholar
- Duchateau MJ, Velthuis HHW (1989) Ovarian development and egg laying in workers of Bombus terrestris. Entomol Exp Appl 51:199–213. https://doi.org/10.1111/j.1570-7458.1989.tb01231.x CrossRefGoogle Scholar
- Hefetz A (1987) The role of Dufour's gland secretions in bees. Physiol Entomol 12:243–253. https://doi.org/10.1111/j.1365-3032.1987.tb00749.x CrossRefGoogle Scholar
- Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. https://doi.org/10.1146/annurev.ento.50.071803.130359 CrossRefPubMedGoogle Scholar
- Le Conte Y, Hefetz A (2008) Primer pheromones in social Hymenoptera. Annu Rev Entomol 53:523–542. https://doi.org/10.1146/annurev.ento.52.110405.091434 CrossRefPubMedGoogle Scholar
- Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530Google Scholar
- Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4–3. https://CRAN.R-project.org/package=vegan
- Peeters C, Liebig J (2009) Fertility signaling as a general mechanism of regulating reproductive division of labor in ants. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to socio-complexity. Harvard University Press, Cambridge, pp 220–242Google Scholar
- R Core Team (2016) R: a language and environment for statistical computing R Foundation for statistical computing, Vienna, Austria. URL https://www.R-project.org/
- Schwarz MP, Richards MH, Danforth BN (2007) Changing paradigms in insect social evolution: insights from Halictine and Allodapine bees. Annu Rev Entomol 52:127–150. https://doi.org/10.1146/annurev.ento.51.110104.150950 CrossRefPubMedGoogle Scholar
- Van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C, Oi CA, d'Ettorre P, Khalesi M, Billen J, Wäckers F, Millar JG, Wenseleers T (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290. https://doi.org/10.1126/science.1244899 CrossRefPubMedGoogle Scholar
- van Zweden J, d'Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ (ed) Insect hydrocarbons biology, biochemistry, and chemical ecology. Cambridge University Press, pp 222–243Google Scholar
- Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
- Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signatures. Cambridge University Press, CambridgeGoogle Scholar