Klára Dolejšová

Asexual queen succession in the higher termite Embiratermes neotenicus

Asexual queen succession (AQS), in which workers, soldiers and dispersing reproductives are produced sexually while numerous non-dispersing queens arise through thelytokous parthenogenesis, has recently been described in three species of lower termites of the genus Reticulitermes. Here, we show that AQS is not an oddity restricted to a single genus of lower termites, but a more widespread strategy occurring also in the most advanced termite group, the higher termites (Termitidae). We analysed the genetic structure in 10 colonies of the Neotropical higher termite Embiratermes neotenicus (Syntermitinae) using five newly developed polymorphic microsatellite loci. The colonies contained one primary king accompanied either by a single primary queen or by up to almost 200 neotenic queens. While the workers, the soldiers and most future dispersing reproductives were produced sexually, the non-dispersing neotenic queens originated through thelytokous parthenogenesis of the founding primary queen. Surprisingly, the mode of thelytoky observed in E. neotenicus is most probably automixis with central fusion, contrasting with the automixis with terminal fusion documented in Reticulitermes. The occurrence of AQS based on different mechanisms of ploidy restoration raises the hypothesis of an independent evolutionary origin of this unique reproductive strategy in individual lineages of lower and higher termites.

Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus

Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so‐called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2 years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3 years. We conclude that S. minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.

Nonadecadienone, a New Termite Trail-Following Pheromone Identified in Glossotermes oculatus (Serritermitidae)

Within the multitude of chemical signals used by termites, the trail marking by means of pheromones is ubiquitous. Chemistry and biology of the trail-following communication have been described in more than 60 species from all families except for the Neotropical Serritermitidae. The chemical ecology of Serritermitidae is of special interest not only as a missing piece of knowledge on the diversity and evolution of isopteran pheromones but also because it may contribute to the debate on the phylogenetic position of this family, which is still unresolved. Therefore, we aimed in this study to identify the trail-following pheromone of the serritermitid Glossotermes oculatus. Based on a combined approach of analytical chemistry, electrophysiology, and behavioral bioassays, we propose (10Z,13Z)-nonadeca-10,13-dien-2-one to be the trail-following pheromone of G. oculatus, secreted by the sternal gland of pseudergates. Thus, we report on a new termite trail-following pheromone of an unexpected chemical structure, a ketone with 19 carbons, contrasting with unsaturated alcohols containing 12 carbons as trail-following pheromones in other advanced termite families. In addition to this unique trail-following pheromone, we also describe the sternal gland in pseudergates as an organ of unusual shape, size, and structure when compared with other isopteran species. These results underline the peculiarity of the family Serritermitidae and prompt our interest in the chemistry of pheromones in the other genus of the family, Serritermes.

Smells Like Home: Chemically Mediated Co-Habitation of Two Termite Species in a Single Nest

Termite nests often are referred to as the most elaborate constructions of animals. However, some termite species do not build a nest at all and instead found colonies inside the nests of other termites. Since these so-called inquilines do not need to be in direct contact with the host population, the two colonies usually live in separate parts of the nest. Adaptations of both the inquiline and its host are likely to occur to maintain the spatial exclusion and reduce the costs of potential conflicts. Among them, mutual avoidance, based on chemical cues, is expected. We investigated chemical aspects of cohabitation between Constrictotermes cavifrons (Nasutitermitinae) and its obligatory inquiline Inquilinitermes inquilinus (Termitinae). Inquiline soldiers produce in their frontal glands a blend of wax esters, consisting of the C12 alcohols (3Z)-dodec enol, (3Z,6Z)-dodecadienol, and dodecanol, esterified with different fatty acids. The C12 alcohols appear to be cleaved gradually from the wax esters, and they occur in the frontal gland, in soldier headspace, and in the walls of the inquiline part of the nest. Electrophysiological experiments revealed that (3Z)-dodecenol and (3Z,6Z)-dodecadienol are perceived by workers of both species. Bioassays indicated that inquiline soldier heads, as well as the two synthetic compounds, are attractive to conspecific workers and elicit an arresting behavior, while host soldiers and workers avoid these chemicals at biologically relevant amounts. These observations support the hypothesis that chemically mediated spatial separation of the host and the inquiline is an element of a conflict-avoidance strategy in these species.

Sphinganine-Like Biogenesis of (E)-1-Nitropentadec-1-ene in Termite Soldiers of the Genus Prorhinotermes

In 1974, (E)‐1‐nitropentadec‐1‐ene, a strong lipophilic contact poison of soldiers of the termite genus Prorhinotermes, was the first‐described insect‐produced nitro compound. However, its biosynthesis remained unknown. In the present study, we tested the hypothesis that (E)‐1‐nitropentadec‐1‐ene biosynthesis originates with condensation of amino acids with tetradecanoic acid. By using in vivo experiments with radiolabeled and deuterium‐labeled putative precursors, we show that (E)‐1‐nitropentadec‐1‐ene is synthesized by the soldiers from glycine or L‐serine and tetradecanoic acid. We propose and discuss three possible biosynthetic pathways.

Identification and Enantiodivergent Synthesis of (5Z,9S)-Tetradec-5-en-9-olide, a Queen-Specific Volatile of the Termite Silvestritermes minutus

The queens of social insects differ from sterile colony members in many aspects of their physiology. Besides adaptations linked with their specialization for reproduction and extended lifespan, the queens also invest in the maintenance of their reproductive dominance by producing exocrine chemicals signaling their presence to the nestmates. The knowledge of the chemistry of queen-specific cues in termites is scarce. In addition to the contact recognition based on cuticular hydrocarbons, long-range signals mediated by volatiles are expected to participate in queen signaling, especially in populous colonies of higher termites (Termitidae). In queens of the higher termite Silvestritermes minutus (Syntermitinae), we have detected a previously undescribed volatile. It is present in important quantities on the body surface and in the headspace, ovaries, and body cavity. MS and GC-FTIR data analyses led us to propose the structure of the compound to be a macrolide 10-pentyl-3,4,5,8,9,10-hexahydro-2 H-oxecin-2-one. We performed enantiodivergent syntheses of two possible enantiomers starting from enantiopure ( S)-glycidyl tosylate. The synthetic sequence involved macrolide-closing metathesis quenched with a ruthenium scavenging agent. The absolute and relative configuration of the compound was assigned to be (5 Z,9 S)-tetradec-5-en-9-olide. Identification and preparation of the compound allow for investigation of its biological significance.

Metabolomic and transcriptomic data on major metabolic/biosynthetic pathways in workers and soldiers of the termite Prorhinotermes simplex (Isoptera: Rhinotermitidae) and chemical synthesis of intermediates of defensive ( E )-nitropentadec-1-ene biosynthesis

Production of nitro compounds has only seldom been recorded in arthropods. The aliphatic nitroalkene (E)-nitropentadec-1-ene (NPD), identified in soldiers of the termite genus Prorhinotermes, was the first case documented in insects in early seventies. Yet, the biosynthetic origin of NPD has long remained unknown. We previously proposed that NPD arises through the condensation of amino acids glycine and/or l-serine with tetradecanoic acid along a biosynthetic pathway analogous to the formation of sphingolipids. Here, we provide a metabolomics and transcriptomic data of the Prorhinotermes simplex termite workers and soldiers. Data are related to NPD biosynthesis in P. simplex soldiers. Original metabolomics data were deposited in MetaboLights metabolomics database and are become publicly available after publishing the original article. Additionally, chemical synthesis of biosynthetic intermediates of NPD in nonlabeled and stable labeled forms are reported. Data extend our poor knowledge of arthropod metabolome and transcriptome and would be useful for comparative study in termites or other arthropods. The data were used for de-replication of NPD biosynthesis and published separately (Jirošová et al., 2017) [1].