Chemical Discrimination and Aggressiveness via Cuticular Hydrocarbons in a Supercolony-Forming Ant, Formica yessensis

Abstract

BackgroundTerritorial 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/SignificanceWe 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.

Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication

“…Discovering the molecular basis for hydrocarbon recognition has thus been a priority of the research community (4). Electrophysiological studies have pinpointed the neurons involved in hydrocarbon detection, showing that they are housed in female-specific basiconic sensilla (17)(18)(19). Meanwhile, 9-exon ORs have been proposed as candidate hydrocarbon receptors based on evolutionary studies (27)(28)(29)(30).…”

“…Renthal et al (16) posited that the basiconic sensilla detect low volatility pheromones such as the hydrocarbons used to discriminate nestmates and nonnestmates, based on the fact that they have an ultrastructure appropriate for contact chemosensation and are concentrated in the portion of the antennae used to antennate conspecifics in Solenopsis invicta. Now numerous studies have used electrophysiology to confirm that ant basiconic sensilla are responsive to hydrocarbons (17)(18)(19), as well as a broad range of other odorants (19). By pharmacologically blocking the obligate odorant receptor coreceptor ORCO, Sharma et al (19) were able to show that it is specifically odorant receptors in the basiconic sensilla that are sensitive to hydrocarbons.…”

At the brink of supercoloniality: genetic, behavioral, and chemical assessments of population structure of the desert ant Cataglyphis niger

“…Polydomy and supercoloniality can be detected genetically as well as behaviorally and chemically. Members of a supercolony are tolerant to each other even if they originate from different nests at the time of their testing, and exhibit chemical uniformity of cuticular hydrocarbon compositions (Errard et al, 2005;Brandt et al, 2009b;Vonshak et al, 2009;Blight et al, 2012;Kidokoro-Kobayashi et al, 2012). Therefore, assessing the population structure of an ant species is best done by encompassing all three parameters, genetic, behavior and recognition chemistry.…”

“…Ample evidence indicate that hydrocarbons constitute at least part of the recognition system (reviewed in Hefetz, 2007), and that there is high degree of congruency in the hydrocarbon recognition cues within a supercolony and distinct compositions between supercolonies (Errard et al, 2005;Brandt et al, 2009a). Recently, it was shown in the unicolonial ant Formica yessensis that profile similarity/disparity as well as incomplete chemical discrimination via the hydrocarbon sensilla (Kidokoro-Kobayashi et al, 2012) are important factors in the establishment of unicoloniality.…”

Cuticular Hydrocarbon Pheromones for Social Behavior and Their Coding in the Ant Antenna

“…Insect antennae express several Ors, each ORN usually expressing a single Or along with an obligate Orco coreceptor, which, together, form a functional receptor. These ORNs and their associated molecular receptors have been proposed to play a central role in detecting the queen CHCs that act as signature cues and are involved in regulating complex worker-specific behaviors and physiological effects such as suppressing ovarian function (Kidokoro-Kobayashi et al, 2012;Nakanishi et al, 2010;Nishikawa et al, 2012;Ozaki et al, 2005;Smith et al, 2013). In this study, we characterize the electrophysiological responses of a panel of cuticular hydrocarbons and non-cuticular hydrocarbons on the worker-specific basiconic sensilla of the antenna and find that they are broadspectrum detectors of hydrocarbons.…”