Effects of Soldier-Derived Terpenes on Soldier Caste Differentiation in the Termite Reticulitermes flavipes

Abstract

-Primer pheromones play key roles in regulating division of labor, which is one of the most fundamental and defining aspects of insect sociality. Primer pheromones are chemical messengers that transmit hormone-like messages among colony members; in recipients these messages can either induce or suppress phenotypic caste differentiation. Here, we investigated soldier-caste-derived chemicals as possible primer pheromones in the lower termite Reticulitermes flavipes, a species for which no primer pheromones have yet been identified. We determined that soldier head extracts (SHE), when provided to totipotent workers along with the insect morphogenetic juvenile hormone (JH), significantly enhanced soldier caste differentiation. When applied alone, however, SHE had no impacts on caste differentiation, survivorship, or any other aspect of worker biology. These findings support that soldier-derived chemicals serve as primer pheromones which enhance the action of the endogenous morphogenetic hormone JH.Thus, SHE chemicals apparently have no effect when received under natural conditions by non-receptive individuals with presumably low JH titers. Gas chromatography-mass spectrometry analysis identified two terpenes as the most plentiful components of R.flavipes SHE. Through GC-MS and NMR analyses, these terpenes were identified as γ-cadinene and its corresponding aldehyde, γ-cadinenal. Validative bioassays with commercially available cadinene confirmed its activity. However, several other previously identified terpenes were also significantly active. These findings reveal a novel primer pheromone-like function for soldier-derived terpenes in termites, and further suggest convergent evolution of terpene functions in enhancing JH-dependent soldier caste differentiation.

Communication and Social Regulation in Termites

“…It has also been shown that the terpenoids released by Reticulitermes soldiers have a regulatory effect on the differentiation of soldiers as seen in Coptotermes Raina 2003, 2005). This primer effect (which is distinct from the different releaser effects described at the beginning of the paragraph) is attributed to two sesquiterpenes, namely γ-cadinene and its aldehyde, which enhance the effect of the juvenile hormone (JH) on R. flavipes soldiers (Tarver et al 2009(Tarver et al , 2011. Two hexamerin proteins, which are controlled by two genes (Hex-1 and Hex-2), suppress JH-mediated differentiation of workers into soldiers (Zhou et al 2006); JH and soldier head extracts have opposing effects on several regulatory genes but have few regulatory effects on the gut microbiome (Sen et al 2013).…”

“…This primer effect produced by the soldiers requires direct contact between the soldiers and the undifferentiated individuals (Dong et al 2009). Interspecific variation in the terpenoid content of Reticulitermes frontal gland secretions was observed by Quintana et al (2003), and the chemical components present in R. flavipes frontal gland secretions have been particularly well described (Zalkow et al 1981;Bagnères et al 1990a;Tarver et al 2009). It has also been shown that the terpenoids released by Reticulitermes soldiers have a regulatory effect on the differentiation of soldiers as seen in Coptotermes Raina 2003, 2005).…”

Characterization of four esterase genes and esterase activity from the gut of the termite Reticulitermes flavipes

“…Previous studies have shown that JH can act exogenously to induce soldier caste differentiation in workers via feeding on treated substrates (e.g., Scharf et al, 2005). Other caste-regulatory terpenes that are active via feeding are produced by termite soldiers (Tarver et al, 2009), some of which are derived from the same biosynthetic pathways as JH (Bellés et al, 2005). Finally, sequencing from the endogenous (host) gut transcriptome in R. flavipes has revealed a number of genes encoding members of JH biosynthetic and degradative pathways, including two putative JH esterases (Tartar et al, 2009;M.…”

Variations in Worker Cuticular Hydrocarbons and Soldier Isoprenoid Defensive Secretions Within and Among Introduced and Native Populations of the Subterranean Termite, Reticulitermes flavipes

“…Juvenile hormone III (JH III) could play a role in regulating the soldier and reproductive castes, with a high concentration of JH III inducing the differentiation of workers into secondary reproductives and a higher concentration inducing differentiation into soldiers (Scharf et al, 2003;Park and Raina, 2004;Elliott and Stay, 2007;Leniaud, 2008). Recent research also has revealed that γ-cadinene and the cadinene aldehyde, two isopreonid SDS components in R. flavipes, act in synergy with juvenile hormone in inducing differentiation of workers in soldiers (Tarver et al, 2009). It also has been suggested that soldiers may intervene in worker differentiation in other castes (Henderson, 1998).…”

“…These soldier defensive secretions (SDSs) are believed to play a role in defending colonies against predators and competitors (Zalkow et al, 1981), and they also may play a role in the production of primer pheromones in Reticulitermes (Henderson, 1998;Tarver et al, 2009). SDSs can be composed of alkanes, aldehydes, ketones, and terpenes, as well as more complex compounds (Quintana et al, 2003;Piskorski et al, 2007).…”