Explore the vast range of titles available.

Division of labour in eusocial insects is characterized by efficient communication systems based on pheromones. Among such insects, termites have evolved specialized sterile defenders, called soldiers. Because they are incapable of feeding themselves, it has been suggested that soldiers are sustained by workers and emit the pheromone arresting workers. However, such a soldier pheromone has not been identified in any termite species, and the details of the soldier–worker interaction remain to be explored. Here, we identified a soldier-specific volatile sesquiterpene as a worker arrestant, which also acts as a primer pheromone regulating soldier differentiation and fungistatic agent in a termite Reticulitermes speratus. Chemical analyses revealed that (−)-β-elemene is the major component of soldier extract, and its authentic standard exhibited arrestant activity to workers and inhibited the differentiation from workers to soldiers. This compound also showed fungistatic activity against entomopathogenic fungi. These suggest that (−)-β-elemene secreted by soldiers acts not only as a worker arrestant but also as one component of inhibitory primer pheromone and an anti-pathogenic agent. Our study provides novel evidence supporting the multi-functionality of termite soldier pheromone and provides new insights into the role of soldiers and the evolutionary mechanisms of pheromone compounds.

The origin of complex worker-caste systems in ants perplexed Darwin 1 and has remained an enduring problem for evolutionary and developmental biology 2 – 6 . Ants originated approximately 150 million years ago, and produce colonies with winged queen and male castes as well as a wingless worker caste 7 . In the hyperdiverse genus Pheidole , the wingless worker caste has evolved into two morphologically distinct subcastes—small-headed minor workers and large-headed soldiers 8 . The wings of queens and males develop from populations of cells in larvae that are called wing imaginal discs 7 . Although minor workers and soldiers are wingless, vestiges or rudiments of wing imaginal discs appear transiently during soldier development 7 , 9 – 11 . Such rudimentary traits are phylogenetically widespread and are primarily used as evidence of common descent, yet their functional importance remains equivocal 1 , 12 – 14 . Here we show that the growth of rudimentary wing discs is necessary for regulating allometry—disproportionate scaling—between head and body size to generate large-headed soldiers in the genus Pheidole . We also show that Pheidole colonies have evolved the capacity to socially regulate the growth of rudimentary wing discs to control worker subcaste determination, which allows these colonies to maintain the ratio of minor workers to soldiers. Finally, we provide comparative and experimental evidence that suggests that rudimentary wing discs have facilitated the parallel evolution of complex worker-caste systems across the ants. More generally, rudimentary organs may unexpectedly acquire novel regulatory functions during development to facilitate adaptive evolution. In the ant genus Pheidole the growth of rudimentary wing discs—which influence developmental allometry to produce castes with distinct morphologies—is socially regulated to determine the worker-to-soldier ratio in Pheidole colonies.

Altruistic caste, including worker and soldier (derived from worker), plays a critical role in the ecological success of social insects. The proportion of soldiers, soldier sex ratios, and the number of workers vary significantly between species, and also within species, depending on colony developmental stage and environmental factors. However, it is unknown whether there are sex-linked effects from parents on controlling the caste fate or not. Here, we compared soldier sex ratios, soldier proportions, and population size among a four mating types of Reticulitermes amamianus (Ra) and R. speratus (Rs) (male x female, mRa x fRa, mRa x fRs, mRs x fRa, mRs x fRs) and demonstrate that the soldier sex ratio and worker population size of hybrid colonies skew to colonies of king's species, while the soldier proportion skew to queen's species. The survival rate of offspring resulting from interspecies hybridization was significantly higher for mRa x fRs than for mRs x fRa. The results of this study demonstrate the asymmetric influence of kings and queens on caste determination and colony growth, which can contribute to our better understanding of parental influence on the colony dynamics of social insects.

Polyphenisms in social insects arise from flexible developmental mechanisms that may produce behaviorally and morphologically specialized workers. The ant genus Pheidole is typically characterized by small minor worker and large soldier subcastes, but larger supersoldiers have evolved in several species, including the exceptionally polymorphic Pheidole rhea. To examine worker phenotype evolution in this socially complex ant, we tested the hypotheses that behavior, brain structure, and morphology are integrated within worker size classes due to selection for specialized social roles and that traits have been discretized among these groups. Our analyses revealed significant differences in brain structure and body shape between minor workers and the two soldier size classes. Behavioral repertoires of minors, soldiers, and supersoldiers were similar, but minors performed important tasks at higher frequencies than soldiers and supersoldiers. The extensive overlap in behavioral repertoire between soldier and supersoldier groups correlated with shared neuroanatomical and morphological traits. Although head and body size vary allometrically among P. rhea size classes, scaling analyses revealed little allometry in brain substructure. The covariation of behavior and brain organization between soldier size classes suggests that their functionality may be due to differences in task performance rate or efficiency rather than task repertoire. The early branching position of P. rhea in the phylogeny of Pheidole and patterns of worker phenotypic plasticity suggest this species exhibits an ancestral state of sociobiological and neurobiological organization that served as a ground plan for diversification in this ecologically dominant ant genus. Selection for divergent social roles may impact the degree to which behavioral, neuroanatomical, and morphological phenotypes are integrated within individuals and between specialized groups. Behavioral repertoire, neuroanatomy, and worker body shape in the strongly polymorphic P. rhea, a species of the hyperdiverse ant genus Pheidole that branched early in the phylogeny of the clade appear to show a relatively low degree of integration with worker head-body size. The putatively ancestral and developmentally plastic condition in which largerbodied soldier groups are not distinguishable in behavior, brain scaling relationships, and body shape suggests the advantage of worker head-body allometry may derive from variation in quantitative aspects of behavioral performance rather than specialization on qualitatively different tasks. This appears to be significant to social evolution in the genus.

Subterranean termites live in underground colonies with a division of labor among castes (i.e., queens and kings, workers, and soldiers). The function of social colonies relies on sophisticated chemical communication. Olfaction, the sense of smell from food, pathogens, and colony members, plays an important role in their social life. Olfactory plasticity in insects can be induced by long- and short-term environmental perturbations, allowing adaptive responses to the chemical environment according to their physiological and behavioral state. However, there is a paucity of information on the molecular basis of olfaction in termites. In this study, we identified an ortholog encoding the odorant receptor co-receptor (Orco) in the Formosan subterranean termite, Coptotermes formosanus , and examined its expression variation across developmental stages and in response to social conditions. We found that C . formosanus Orco showed conserved sequence and structure compared with other insects. Spatial and temporal analyses showed that the Orco gene was primarily expressed in the antennae, and it was expressed in eggs and all postembryonic developmental stages. The antennal expression of Orco was upregulated in alates (winged reproductives) compared with workers and soldiers. Further, the expression of Orco decreased in workers after starvation for seven days, but it was not affected by the absence of soldiers or different group sizes. Our study reveals the molecular characteristics of Orco in a termite, and the results suggest a link between olfactory sensitivity and nutritional status. Further studies are warranted to better understand the role of Orco in olfactory plasticity and behavioral response.

Pheromone communication is the cornerstone of eusocial insect societies since it mediates the social hierarchy, division of labor, and concerted activities of colony members. The current knowledge on molecular mechanisms of social insect pheromone detection by odorant receptors (ORs) is limited to bees and ants, while no OR was yet functionally characterized in termites, the oldest eusocial insect clade. Here, we present the first OR deorphanization in termites. We selected four OR sequences from the annotated antennal transcriptome of the termite Prorhinotermes simplex (Psammotermitidae), expressed them in Empty Neuron Drosophila , and functionally characterized them using single sensillum recording (SSR). For one of the selected ORs, PsimOR14, we obtained strong responses to the main component of P. simplex trail-following pheromone, the monocyclic diterpene neocembrene. PsimOR14 showed a narrow tuning to neocembrene with only one additional compound out of 67 tested generating non-negligible responses. We report on homology-based modeling and molecular dynamics simulations of ligand binding by PsimOR14. Subsequently, we used SSR in P. simplex workers and identified the olfactory sensillum responding to neocembrene, thus likely expressing PsimOR14 . Finally, we demonstrate that PsimOR14 is significantly more expressed in worker antennae compared to soldiers, which correlates with higher sensitivity of workers to neocembrene.

Background The insect cuticle is mainly composed of exocuticle and endocuticle layers that consist of a large number of structural proteins. The thickness and synthesis of the exocuticle depend on different castes that perform various functions in alates, workers and soldiers. However, it is not clear whether the soft endocuticle is involved in the division of labour in termite colonies. To reveal the structural characteristics of the endocuticle in different castes, we investigated the thickness of endocuticle layers in alates, workers and soldiers of the termite Reticulitermes aculabialis , and then we sequenced their transcriptome and detected the endocuticle protein genes. The differential expression levels of the endocuticular protein genes were confirmed in the three castes. Results We found that there was a great difference in the thickness of the endocuticle among the alates, soldiers and workers. The thickest endocuticle layers were found in the heads of the workers 7.88 ± 1.67 μm. The endocuticle layer in the head of the workers was approximately three-fold and nine-fold thicker than that in the heads of soldiers and alates, respectively. The thinnest endocuticle layers occurred in the head, thorax and abdomen of alates, which were 0.86 ± 0.15, 0.76 ± 0.24 and 0.52 ± 0.17 μm thick, respectively, and had no significant differences. A total of 43,531,650 clean sequencing reads was obtained, and 89,475 unigenes were assembled. Of the 70 identified cuticular protein genes, 10 endocuticular genes that belong to the RR-1 family were selected. qRT-PCR analysis of the five endocuticular genes (SgAbd-2, SgAbd-9, Abd-5, SgAbd-2-like and Abd-4-like) revealed that the endocuticle genes were more highly expressed in workers than in soldiers and alates. Conclusion These results suggest that SgAbd and Abd are the key components of the endocuticle. We infer that the thicker endocuticle in workers is helpful for them to perform their functions against environmental stress.

Comparing the size of functionally distinct brain regions across individuals with remarkable differences in sensory processing and cognitive demands provides important insights into the selective forces shaping animal nervous systems. We took advantage of the complex system of worker-to-soldier differentiation in the termitid Procornitermes araujoi , to investigate how a profound modification of body morphology followed by an irreversible shift in task performance are translated in terms of brain structure and size. This behavioural shift is characterised by a reduction of the once wide and complex behavioural repertoire of workers to one exclusively dedicated to nest defence (soldiers). In accordance with soldier’s reduced cognitive and sensory demands, we show here that differentiation of workers into soldiers is associated with a size reduction of the mushroom body (MB) compartments, higher-order brain regions responsible for multimodal processing and integration of sensory information, as well as learning, memory, and decision-making. Moreover, in soldiers, we found an apparent fusion of the medial and lateral MB calyces likely associated with its volume reduction. These results illustrate a functional neuroplasticity of the MB associated with division of labour, supporting the link between MB size and behavioural flexibility in social insect workers.

Termites are eusocial insects with functionally specialized workers and soldiers, both sharing the same genotype. Additionally, lower termites host flagellates in their hindguts that assist in wood digestion. However, worker-biased and soldier-biased gene expression patterns of the host–flagellate symbiotic system remain underexplored in most taxonomic groups. In this study, we sequenced high-depth transcriptomes from the workers and soldiers of a lower termite, Neotermes binovatus (Kalotermitidae), to investigate the differentially expressed termite transcripts, flagellate transcript abundance, and co-expression patterns of the host–flagellate transcript pairs in both castes. The worker-biased transcripts were enriched in functions related to cuticle development, nervous system regulation, pheromone biosynthesis, and metabolism, whereas the soldier-biased transcripts were predominantly involved in muscle development and kinesis, body morphogenesis, protein modification, and aggression. Flagellate transcripts from the orders Cristamonadida, Trichomonadida, Tritrichomonadida, and Oxymonadida were identified in both workers and soldiers, with the abundance of most flagellate transcripts tending to be higher in workers than in soldiers. Furthermore, we observed a much larger number of strong co-expression correlations between the termite and flagellate transcripts in workers than in soldiers, suggesting the possibility that soldiers depend more on food processed by worker holobionts than on their own symbiotic system. This research provides insights into the functional specialization of the host–flagellate symbiotic system in the worker and soldier castes of termites, supporting the workers’ roles in nest maintenance, preliminary food processing, and communication, while emphasizing the defensive role of soldiers. Additionally, it offers new perspectives on the potential termite-flagellate interactions and underscores the need for whole-genome data of termite flagellates in further studies.

The trade-off between reproduction and longevity is known in wide variety of animals. Social insect queens are rare organisms that can achieve a long lifespan without sacrificing fecundity. The extended longevity of social insect queens, which contradicts the trade-off, has attracted much attention because it implies the existence of an extraordinary anti-aging mechanism. Here, we show that queens of the termite Reticulitermes speratus incur significantly lower oxidative damage to DNA, protein and lipid and have higher activity of antioxidant enzymes than non-reproductive individuals (workers and soldiers). The levels of 8-hydroxy-2'-deoxyguanosine (oxidative damage marker of DNA) were lower in queens than in workers after UV irradiation. Queens also showed lower levels of protein carbonyls and malondialdehyde (oxidative damage markers of protein and lipid, respectively). The antioxidant enzymes of insects are generally composed of catalase (CAT) and peroxiredoxin (Prx). Queens showed more than two times higher CAT activity and more than seven times higher expression levels of the CAT gene RsCAT1 than workers. The CAT activity of termite queens was also markedly higher in comparison with other solitary insects and the queens of eusocial Hymenoptera. In addition, queens showed higher expression levels of the Prx gene RsPRX6. These results suggested that this efficient antioxidant system can partly explain why termite queens achieve long life. This study provides important insights into the evolutionary linkage of reproductive division of labor and the development of queens' oxidative stress resistance in social insects.