Venom Alkaloid and Cuticular Hydrocarbon Profiles Are Associated with Social Organization, Queen Fertility Status, and Queen Genotype in the Fire Ant Solenopsis invicta

Abstract

Queens in social insect colonies advertise their presence in the colony to: a) attract workers’ attention and care; b) gain acceptance by workers as replacement or supplemental reproductives; c) prevent reproductive development in nestmates. We analyzed the chemical content of whole body surface extracts of adult queens of different developmental and reproductive stages, and of adult workers from monogyne (single colony queen) and polygyne (multiple colony queens) forms of the fire ant Solenopsis invicta. We found that the composition of the most abundant components, venom alkaloids, differed between queens and workers, as well as between reproductive and non-reproductive queens. Additionally, workers of the two forms could be distinguished by alkaloid composition. Finally, sexually mature, non-reproductive queens from polygyne colonies differed in their proportions of cis-piperidine alkaloids, depending on their Gp-9 genotype, although the difference disappeared once they became functional reproductives. Among the unsaturated cuticular hydrocarbons characteristic of queens, there were differences in amounts of alkenes/alkadienes between non-reproductive polygyne queens of different Gp-9 genotypes, between non-reproductive and reproductive queens, and between polygyne and monogyne reproductive queens, with the amounts increasing at a relatively higher rate through reproductive ontogeny in queens bearing the Gp-9 b allele. Given that the genotype-specific piperidine differences reflect differences in rates of reproductive maturation between queens, we speculate that these abundant and unique compounds have been co-opted to serve in fertility signaling, while the cuticular hydrocarbons now play a complementary role in regulation of social organization by signaling queen Gp-9 genotype.

Intraspecific variations in the venom peptidome of the ant Odontomachus haematodus (Formicidae: Ponerinae) from French Guiana

“…Interestingly, these results contrast with the case of fire ants whose alkaloid venom composition changes with the size and age of the workers (Deslippe and Guo 2000;Haight and Tschinkel 2003). The venom composition of all fire ant queens is also presumably different from workers which assumes different biological effects (Eliyahu et al 2011;Fox et al 2012). Also, Neoponera commutata (Ponerinae) and Pogonomyrmex spp.…”

Workers and alate queens of Solenopsis geminata share qualitatively similar but quantitatively different venom alkaloid chemistry

“…Workers inject venom directly into other animals for defense and predation, or spray it throughout the nest environment, presumably for protection against microbial pathogens (Chen, 2007). The proportion of cis piperidines was found to gradually increase in the venom of queens as they became fully reproductive (Eliyahu et al, 2011). Queens apply their venoms over eggs as they are laid, presumably for protecting eggs from entomopathogenic fungi (Vander Meer and Morel, 1995;Tschinkel, 2006).…”

“…These alkaloids in queens may not necessarily function as defensive compounds as in workers (Blum et al, 1958;Javors et al, 1993), but conceivably as queen pheromones. Venom alkaloids on the surface of eggs may play a role in advertising the presence and fertility status of queens (Vander Meer and Morel, 1995;Eliyahu et al, 2011). The workers are aggressive defenders against nest disturbance; however, queens move away from disturbances and seldom attempt to sting.…”

“…For each colony, ant workers, or alate queens (1 g) were killed by freezing and extracted with hexane (enough hexane to cover ant bodies, ∼3.5 mL) for 24 h. The whole body extraction proved to adequately represent the gland extractions (data not shown) and have been widely used for fire ant venom alkaloid analysis (For example, Deslippe and Guo, 2000;Eliyahu et al, 2011). The extract was dried over anhydrous sodium sulfate and concentrated to 0.5 mL under a mild stream of N 2 , and then loaded onto a 17 mm (o.d.)…”

Communication and Social Regulation in Termites

“…If, upon contact, the hydrocarbon blend is not recognized as a signal coming from a nestmate, aggressive behavior follows. The various information that is conveyed by hydrocarbons in social Hymenoptera has been well described in recent literature (e.g., Greene and Gordon 2003;Châline et al 2005;Smith et al 2009;Eliyahu et al 2011;Bonckaert et al 2012;Bos et al 2012;Van Oystaeyen et al 2014). Cuticular hydrocarbons play a prominent role in nestmate recognition in both ants (D'Ettore and Lenoir 2010) and termites .…”