The lose-to-win strategy of the weak: intraspecific parasitism via egg abduction in a termite

Predation by larger conspecifics poses a major threat to small juveniles in many animal species. However, in social insects, raids perpetrated by large colonies may provide smaller colonies with opportunities for parasitization. Herein, in the termite Reticulitermes speratus , we demonstrate that small incipient colonies parasitize large mature colonies through egg abduction when attacked by raiding conspecifics. We observed that the eggs of incipient colonies were brought into raiding colonies while their parents were killed during the attack. In this species, unmated females found new colonies with female–female (FF) cooperation, in addition to the typical monogamous colony foundation. Interestingly, the abducted eggs of FF pairs developed into nymphs (reproductive caste) in the raiding colonies, whereas the eggs of male–female (MF) pairs developed into workers (non-reproductive caste). Parthenogenetic eggs are known to be developmentally predisposed to becoming female reproductives owing to genomic imprinting in termites. This study demonstrates that the plundering of small colonies by larger conspecific colonies not only results in the extinction of the weaker colonies, but also serves as a strategy that incipient colonies use to obtain the reproductive position in large colonies by stealth. The results elucidate the diversity and complexity of inter-colonial interactions in social insects.

Genomic and transcriptomic analyses of the subterranean termite Reticulitermes speratus: gene duplication facilitates social evolution

Termites are model social organisms characterized by a polyphenic caste system. Subterranean termites (Rhinotermitidae) are ecologically and economically important species, including acting as destructive pests. Rhinotermitidae occupies an important evolutionary position within the clade representing an intermediate taxon between the higher (Termitidae) and lower (other families) termites. Here, we report the genome, transcriptome and methylome of the Japanese subterranean termite Reticulitermes speratus. The analyses highlight the significance of gene duplication in social evolution in this termite. Gene duplication associated with caste-biased gene expression is prevalent in the R. speratus genome. Such duplicated genes encompass diverse categories related to social functions, including lipocalins (chemical communication), cellulases (wood digestion and social interaction), lysozymes (social immunity), geranylgeranyl diphosphate synthase (social defense) and a novel class of termite lineage-specific genes with unknown functions. Paralogous genes were often observed in tandem in the genome, but the expression patterns were highly variable, exhibiting caste biases. Some duplicated genes assayed were expressed in caste-specific organs, such as the accessory glands of the queen ovary and frontal glands in soldier heads. We propose that gene duplication facilitates social evolution through regulatory diversification leading to caste-biased expression and subfunctionalization and/or neofunctionalization that confers caste-specialized functions.

Cuticular hydrocarbon profile for queen recognition in the termite Reticulitermes speratus

Chemical communication underlies the sophisticated colony organization of social insects. In these insects, cuticular hydrocarbons (CHCs) play central roles in nestmate, task, and caste recognition, which contribute to maintenance of the social and reproductive division of labor. Queen-specific CHCs reflect queen fertility status and function as a queen recognition pheromone, triggering aggregation responses around the queens. However, there are only a few studies about the royal recognition mechanism in termites, and particularly, no study has reported about queen-specific CHCs in the species using asexual queen succession (AQS) system, in which the primary queen is replaced by neotenic queens produced parthenogenetically. In this study, we identified the CHC pheromone for neotenic queen recognition in the AQS termite species Reticulitermes speratus. Gas chromatography-mass spectrometry analyses revealed that the relative amount of n-pentacosane was disproportionately greater in the CHC profiles of queens than in the CHC profiles of kings, soldiers, and workers. Furthermore, we investigated the cuticular chemicals of the queen aggregate workers; bioassays demonstrated that n-pentacosane shows a worker arrestant activity in the presence of workers’ cuticular extract. These results suggest that R. speratus workers identify whether each individual is a neotenic queen by recognizing the relatively higher ratio of n-pentacosane in the conspecific CHC background. Moreover, they suggest that termites have evolved queen recognition behavior, independently of social hymenopterans.

Colony Suppression and Possible Colony Elimination of the Subterranean Termites Coptotermes formosanus and Reticulitermes speratus by Discontinuous Soil Treatment Using a Diluent of Fipronil Suspension Concentrate

We assessed the efficacy of a discontinuous soil treatment using a diluent of fipronil suspension concentrate in controlling colonies of Coptotermes formosanus and Reticulitermes speratus. In-ground monitoring stations were installed at Isogi Park and Kindai University, and individual termites inhabiting the stations were collected for four or six years to determine the numbers and locations of colonies present in test areas before and after the discontinuous soil treatment. Microsatellite genotyping indicated that two C. formosanus and two R. speratus colonies in the test area at Isogi Park and five R. speratus colonies in the test area at Kindai University were active and that their territories fluctuated every year. One of the two C. formosanus colonies at Isogi Park and one of the five R. speratus colonies at Kindai University were subjected to discontinuous soil treatments with fipronil and were strongly affected by the treatment at the colony level, resulting in the suppression and possible elimination of colonies. Termite activity of the fipronil-treated colony of C. formosanus was detected within one week after the discontinuous soil treatment and was not found for more than two years (28 months), while termite activity of the fipronil-treated colony of R. speratus was detected within four days and three weeks after the discontinuous soil treatment and was not detected thereafter for three years. Fipronil residue analysis showed that workers of C. formosanus moved at least 28 m and that workers of R. speratus moved 6 m from the treated soil locations for up to three weeks.

Reduction in Toxicity of Tectoquinone against Reticulitermes speratus Kolbe termites

The cause of low toxicity against Reticulitermes speratusKolbe termite species of teakwood under natural condition was investigated. Anti-termite test was conducted to evaluate the effectivity of four major components (tectoquinone, deoxylapachol, tecomaquinone, and squalene) of ethanol-benzene extracts in the teak heartwood. Tectoquinone exhibited both strong toxicity and antifeedancy as well as it was far superior to other components. The strength reduction of tectoquinone bioactivity is assumed due to interaction with other major components. As squalene was found in considerable amounts or 1.8 to 13.1 times as high as the tectoquinone concentration in woods, termite feeding was set to the mixtures of tectoquinone and squalene in various ratios (1:1, 1:5, 1:10, and 1:20). It was revealed that squalene addition could decrease the termite mortality 15% to 44% from its initial value (tectoquinone only). On the other hand, the mixtures reduced mass loss due to termite attacks only to a small degree.