Research

Old arboreal nest of Labiotermes labralis (Syntermitinae) inhabited by the generalist inquiline Cavitermes tuberosus (French Guiana, 2014)

Research Interests

My research interest is centered around the evolution and ecology of termites, a clade of eusocial ecosystem engineers —more precisely on the modalities of their reproduction; their ecology and symbioses; and their phylogenetic history.

I investigate their reproductive evolutionary history (breeding system, mode of reproduction, sex ratio, sex determination) using empirical evidence and theoretical modelling in order to determine the consequences on their genetic and population features. Notably, my research participates in evidencing the widespread ability of queens to reproduce parthenogenetically and in deconstructing the paradigm of lifelong monogamy between termite royals.

I study their evolutionary history through their ecological attributes as well as population and phylogenetic prevalence of peculiar bacteria (some of which potentially involved in nutritional symbioses); with a focus at understanding whether these bacteria can explain the ecological success of inquilines —termites living and feeding on another one’s den.

Finally, I am also involved in the revision of their taxonomy, blurred by incomplete species descriptions which highly impedes the proper resolution of their phylogenesis.

A. Reproductive strategies in termites

AQS in the neotropical inquiline Cavitermes tuberosus. Primary-headed colony (above) with a primary king and a primary queen, and secondary colony (below) in which the primary queen was replaced by neotenic daughters (Pictures credits: R. Hanus).

Asexual Queen Succession

Typically, a termite colony is founded by an independent pair of adults, which become the new colony's primary queen and king. The primary queen dies systematically before the king in a few species: neotenic daughters produced by thelytokous parthenogenesis replace their mother and mate with the primary king in their natal nest, a process called asexual queen succession (AQS).

Focusing on the neotropical lineage of the Termes-group, we evidenced AQS for the first time in the Termitinae in Cavitermes tuberosus (Fournier, Hellemans et al. 2016 Proc. Royal Soc. B). Expanding beyond Cavitermes, we evidenced this reproductive strategy in an additional three species thereby suggesting that this strategy is more widespread than previously thought (Hellemans et al. 2019 BMC Evol. Biol.). In all investigated species of this lineage, automictic parthenogenesis occurs through gamete duplication (see section on Bacterial endosymbioses).

A decade after the discovery of AQS, we revisited the occurrence of parthenogenesis in termites, the phenomenon of AQS, the prerequisites to its evolution, its consequences on the genetic and population characteristics of species, as well as suggest future research directions (Hellemans & Roisin 2020 eLS).

Aspiring royals in the Termitinae

The evolution of the AQS breeding system requires both the ability of queens to lay viable unfertilized eggs and the propensity of parthenogenetic eggs to develop into neotenic queens.

Comparing the developmental pathways of parthenogenetically-produced females to that of sexually-produced ones, we found that neotenic queens develop from a newly described stage in the Termitinae, referred to as aspirants, that behave as helpers in the society as long as the primary queen stays alive (Hellemans et al. 2017 Evol. Dev.).

Alate-destined nymph (left) with normal wing pads, and aspirant (right) with soil-filled gut and regressed translucent wing pads (Pictures credits: R. Hanus).

Swarming event in the Petit Saut Research Station (French Guiana, 2015)

Breeding system and sex ratio

Sex allocation —the production of alates dispersers (future primary kings and queens) rather than sterile castes— is the ultimate goal of colonies. This allocation to reproduction is further categorized as the relative investment in males or females, i.e. the sex ratio.

In AQS species, while queen replacement does not modify the genetic architecture of the colony, this is not the case upon the death of the primary king in species with AQS. Due to asymmetric genetic contribution of the primary king and queen within the alate dispersers, a female-biased sex ratio is expected at the population level. Our results on C. tuberosus indicate that a female-biased sex ratio should not always be expected in AQS species and rather depends on their various life history traits (Hellemans et al. 2019 Insectes Soc.).

Habitat and breeding systems

Connectivity loss following habitat fragmentation depends notably on the dispersal ability and breeding systems of each species. Among termites, soil-feeding ones are most sensitive due to their ecological requirements.

We investigated the genetic diversity of a population of the AQS mound-building species Embiratermes neotenicus (Syntermitinae) about a century after fragmentation following sugarcane plantations in Northeast Brazil on a span 20 km. We showed that the population exhibits weak genetic structure which may be explained by the extraordinarily long lifespan of colonies which in turn begets several opportunities for dispersal events and patch colonisation (Couto, Hellemans et al. 2020 Insect Conserv. Divers.).

Impressive mound of E. neotenicus (French Guiana, 2015)

B. Ecology and symbioses

The biology of inquilinism

Termites are eusocial insects which evolved diverse feeding and nesting strategies. The one of inquiline termites is to live in nests built by other species. Obligatory inquilines are often associated with a single species and colonize host-inhabited nests, whereas facultative inquilines colonize nests not necessarily inhabited by their builder.

Our studies on the facultative inquiline termite Cavitermes tuberosus offered several insights into the biology of inquilinism by using an integrative framework combining classical ecological measurements and next generation sequencing. These results support the hypothesis that C. tuberosus feeds on nest material and is adapted to colonize nests built by various builders —features which would compensate for its inability to build its own nest and explain its ecological success (Hellemans et al. 2019 Oecologia).

Bacterial endosymbioses

In each species from the neotropical lineage of the Termes-group with demonstrated parthenogenetic ability, parthenogenesis occurs through gamete duplication, a ploidy restoration generally induced by Wolbachia, an endosymbiotic bacterium known to have profound impacts on the biology of arthropods.

We detected Wolbachia in C. tuberosus and I. inquilinus, two species referred to as inquiline termites for their habit to live and feed on arboreal nests built by other termite species. Focusing on C. tuberosus, our results revealed that Wolbachia is tightly associated to a bacteriome located in the midgut, suggesting a nutritional mutualistic association rather than parthenogenesis induction in this species (Hellemans, Kaczmarek et al. 2019 FEMS Microbiol. Ecol.).

In neotenic queens of C. tuberosus, the bacteriome is visible as a black dot through the cuticle (Picture credits: R. Hanus).

Soil-feeding termites sailed to new realms

Termites feed on vegetal matter at various stages of decomposition. While wood-feeding termites often live in the wood on which they feed and are efficient at dispersing across oceans by rafting, soil-feeders were believed to be poor dispersers.

Our phylogenetic and ancestral trait reconstructions indicate that despite their lower dispersive probability, soil-feeders experienced long-distance over-water dispersal events that contributed to their modern distribution (Hellemans et al. 2022 Proc. Royal Soc. B).

C. Phylogenetics and taxonomy

Since the inception of Linnaean taxonomy, termite descriptions have mostly been based on the morphology of soldiers which may overemphasise ancestral characters and lead to the establishment of non-monophyletic taxa.

Illustration by Tibo for a vulgarization article on Palmitermes impostor in Le Journal des Nouragues 2017 (1), p. 15

The impostor

During our studies on Termitinae species with AQS, we encountered an enigmatic and misleading taxon, Palmitermes impostor Hellemans & Roisin. While the soldiers of P. impostor resemble those of the Termes genus, worker anatomy suggest a close relationship to the genus Cavitermes. Using an integrative taxonomic approach combining the description of all castes, cuticular chemical profiles and mitochondrial phylogenomics, we uncovered the sister-group relationship between Palmitermes and Cavitermes (Hellemans et al. 2017 Invertebr. Syst.).

Palmitermes Hellemans & Roisin —whose name reflects initial frequent findings of their nests at the basis of spiky palm trees of the genus Astrocaryum— is yet a monotypic genus. Its type species' name, Palmitermes impostor Hellemans & Roisin, refers to frequent confusions with C. tuberosus and the T. fatalis species complex during field collections.

The emblematic African genus Cubitermes

Cubitermes is one of the most diverse and abundant genera of African termites, and play important ecological roles at the ecosystem level. However, their taxonomy is obscured by many inadequately detailed historical descriptions. In the context of this limited morphological background, we aimed at establishing a comprehensive phylogeny of the genus. Our results evidenced the paraphyly of Cubitermes whose species are distributed into five major clades —highly reflective of workers’ enteric valve armatures— and was divided into five monophyletic genera (Hellemans et al. 2021 Syst. Entomol.).

Of the five genera Cubitermes sensu lato's species were split between, two are nomina nova: Polyspathotermes Josens & Deligne refers to their spatulated enteric valve (Greek: 𝜋o𝜆𝜐𝜍, polus, many; 𝜎𝜋𝛼𝜃o𝜍, spathos, spatula), and Ternicubitermes Josens & Deligne to the triradial symmetry of their enteric valve (Latin: terni, triple; cubus, cube).

Phylogenies using genomic snapshots

Our current understanding of termites' phylogenetic history is mostly based on mitochondrial markers. However, they form a single marker with its genes linked and maternally inherited as a single package, and such phylogenies can sometimes not reflect species phylogenies.

We developped termite-specific baits tageting over 50k UltraConserved Elements (UCE) loci, enabling phylogenies from full genomic snapshots. With non-destructive DNA extraction protocols, this bait set will help to carry out a global taxonomic revision of termites based on (sometimes poorly preserved) old museum specimens (Hellemans et al. 2022 Mol. Phylogenet. Evol.). The termite UCE database is maintained on GitHub.

We later used UCE phylogenies to unravel the historic biogeography of Kalotermitidae (Bucek et al. 2022) and the intimate coevolution of termites and their bacteria (Arora et al. 2023).

The advent of a new termite classification

Using UCEs and a multitude of concatenation- and coalescence-based phylogenetic reconstructions, we proposed the revised modern classification of Isoptera (Hellemans et al. 2024 Nat. Comm.). Six new subfamilies were erected to accommodate the remaining monophyletic lineages of the polyphyletic "Termitinae": Crepititermitinae, Cylindrotermitinae, Forficulitermitinae, Neocapritermitinae, Promirotermitinae, Protohamitermitinae (all six by: Hellemans, Engel & Bourguignon).

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