Biology subjects

Hellemans, S.

Publications and source records attributed to Hellemans, S..

15 recordsLinked to original sources

bioRxiv2026

High-fidelity long-read metagenomics reveals the metabolic functions of dominant termite gut bacteria

Many termites digest lignocellulosic wood using diverse gut microbiota, yet functions are rarely linked to specific symbionts because complete genomes are scarce. We used PacBio HiFi long reads to reconstruct circular single-contig bacterial metagenome-assembled genomes (MAGs) from the gut microbiota of the wood-feeding termite Nasutitermes takasagoensis. From 13.9 Gb of HiFi data, we obtained highly contiguous assemblies, including 11 Breznakiellaceae (Spirochaetota), two Candidatus Fibrimonas (Fibrobacterota), and one Chitinispirillaceae genome, three dominant lineages in this gut ecosystem. The reconstructed genomes encoded extensive carbohydrate-active enzyme repertoires and anaerobic fermentation pathways consistent with lignocellulose degradation. They also carried genes for essential amino acid biosynthesis, while nitrogen-fixation capacity was present in representatives of all three lineages but varied among closely related strains. One Breznakiellaceae genome possessed a complete Wood-Ljungdahl pathway potentially supporting reductive acetogenesis in the presence of external formate, whereas related strains carried incomplete variants likely involved in anabolic C1 metabolism. Differences in CAZymes, C1 metabolism, and nitrogen fixation among closely related strains reveal functional diversification that fragmented MAGs would not resolve. The mapping of metatranscriptomic reads from three biological replicates of the fiber-associated community to the reconstructed genomes provided independent evidence that key predicted metabolic functions are transcriptionally active. Our results demonstrate the power of HiFi metagenomics to recover highly contiguous genomes from complex insect microbiomes and uncover lineage-specific metabolic roles of dominant termite gut symbionts.

microbiology↗

bioRxiv2026

Genome size, rather than sociality, predicts the turnover of duplicated genes in termites and hymenopterans

Gene duplication is a major source of genetic variation and is considered as an important driver of evolutionary novelties, including eusociality in insects, such as ants, wasps, bees, and termites. However, it remains unclear whether selection acts to increase gene copy number in social insects. Here, we studied the paranomes, namely, the whole set of paralogous genes in a genome, of Blattodea and Hymenoptera. We estimated the rates of gene duplication and loss using the distribution of synonymous substitution rate of paralogous genes and showed that regardless of sociality, duplicated genes were lost more rapidly than expected under random drift, indicating that negative selection on duplicated genes is prevalent across Blattodea and Hymenoptera. The rates of gene duplication and loss varied independently of sociality levels, but were positively related to genome size, suggesting the expansion/contraction of gene families can be a side effect of genome expansion/contraction. These results call for a reevaluation of adaptative gene duplications.

genomics↗

bioRxiv2026

Social caste switching triggers emergence of novel cellular identities in Zootermopsis termites

A hallmark of eusocial insects is the specialisation of individuals into castes that share the same genome but present distinct phenotypes. Caste switching can affect gene expression1,2, but can it give rise to entirely new cell types? Here, we generated single-cell transcriptomic atlases of a king, a queen, a soldier, and six workers of the termite Zootermopsis nevadensis to understand whether caste differentiation is accompanied by the emergence of novel cellular identities. Out of 24 annotated termite cell types, 18 of which mirrored homologous Drosophila cell types, one was unique for king, one was almost entirely restricted to the queen, and none were exclusive to nonreproductives. Instead, nonreproductive termites possessed more muscle and neuronal cells and less fat cells than reproductives. Caste-linked transcriptional signatures were detected in most cell types, including rare genes expressed with dual specificity for both cell type and caste. Despite the emergence of new cell types in reproductives, expression of hormones, immune genes, carbohydrate-active enzymes3, and rapidly adapting genes4 were only weakly altered by caste. These findings show that cellular differentiation can be induced anew in adult organisms without dysregulating their key physiologic pathways.

evolutionary biology↗

bioRxiv2026

Rapid termite diversification is associated with increased transposable element activity

Termites are a lineage of social insects that originated during the Early Cretaceous [~]150 million years ago. They are the dominant decomposers in modern tropical and subtropical terrestrial ecosystems, a role they achieved through several phases of rapid diversification facilitated by unknown genetic mechanisms. Here, we investigated the link between termite diversification and the activity of transposable elements (TEs). We reconstructed the evolutionary history of TE replications using the genomes of 45 termite species and identified two waves of TE expansion that involved all major TE classes and superfamilies and took place synchronously across termite lineages. The first wave occurred around the end of the Cretaceous, and the second wave occurred during the Oligocene and Miocene, coinciding with the two major phases of termite diversification. We further estimated TE insertion/deletion rates along the species tree and showed that TE activity is positively correlated with termite diversification during the last [~]150 million years of evolution, providing evidence for a link between TE activity and diversification over a macroevolutionary timescale.

evolutionary biology↗

bioRxiv2026

Evolutionary origin of terpenoid biosynthesis in termites

Termites produce the most diverse array of terpenoids among metazoans, comprising over 200 structures. However, their biosynthesis has not yet been elucidated. Here, we identify a gene family which arose through the duplication of geranylgeranyl pyrophosphate synthase in the common ancestor of Neoisoptera, the terpene-producing termite lineage. We functionally characterized several proteins from this family as terpene synthases generating biologically relevant sesqui-and diterpenes. These include the queen pheromone (3R,6E)-nerolidol in Embiratermes neotenicus and the precursor of polycyclic defensive diterpenes (E,E,E)-neocembrene in Nasutitermes takasagoensis. We explore transposable element-mediated genomic mechanisms and selection pressures acting in the evolution of this gene family and report an amino acid site crucial for cyclization capacity as well as the enantiospecificity of the characterized enzymes. We conclude that we have identified an enzyme family underlying the remarkable richness of termite terpenoids, which likely contributed to the ecological success of Neoisoptera.

biochemistry↗

bioRxiv2025

Deciphering the evolution of sex determination across the termite tree of life using high-quality genome assemblies

Most termites exhibit a unique sex-determining system, featuring multiple X and Y chromosomes that fuse into large complexes during male meiosis. The evolutionary origins of such complexes remain largely unknown. Using the genomes of 45 termites and two cockroaches, we investigated the evolution of sex determination systems in an entire insect lineage. We found that termite sex chromosomes are largely undifferentiated, likely reflecting extensive ongoing recombination. Evolving from the X0 system of cockroaches, most early-diverging termites exhibit a Y chromosome bearing the sex-determining gene doublesex, whereas doublesex is autosomal in most other termites. In contrast, other species exhibit multiple sex chromosomes that have undergone frequent turnover, except for Termitidae, which harbor conserved sex chromosomes. Our findings reveal important reworkings of the ancestral transformer-doublesex pathway in termites and suggest a potential role of doublesex in the formation of meiotic chromosomal complexes and caste differentiation.

evolutionary biology↗

bioRxiv2025

Convergent genetic rewiring of the brain underlies termite sociality

How genomes encode major transitions in social evolution is unclear. We use 29 near-chromosome-quality genomes across a spectrum of social complexity to explore the genomic basis of termite sociality. We show that shifts in selection and gene family evolution preceded the emergence of sociality, pointing to subtler genetic causes of this major evolutionary transition (MET). In comparisons of convergent societal forms, we find that a subset of Odorant Receptors (ORs) underwent parallel expansions in independent advanced termite societies displaying true worker phenotypes. The identified OR genes play caste-differentiated roles in termite but not nearest roach brains and are especially elaborated in true workers. Together with evidence of co-opted nutritional signaling and behavioral genes at different levels of social complexity, our study illuminates the rewiring of the molecular machinery underlying this MET.

genomics↗

bioRxiv2025

Termites became the dominant decomposers of the tropics after two diversification pulses

Insects have the highest species richness among animals, but the extent of their diversity and the timing of their diversification remain unclear. Insect diversification is difficult to infer due to the incompleteness of the fossil record. Phylogenetic trees of extant species reconstructed from an exhaustive sampling can be useful to address major evolutionary questions. Here, we investigated the diversification of termites, which comprise 2,995 described species, using estimates of speciation, extinction, and net diversification rates inferred from molecular phylogenies including 2,800 samples representing 1,377 putative species. Termites originated in the Early Cretaceous [~]132 million years ago. Estimated extinction rates were close to zero despite fossil evidence of extinction; therefore, we focused our interpretations on the net diversification rates. Our analyses detected two significant rate shifts. The first shift occurred at the end of the Cretaceous, initially in the Kalotermitidae, then in the Neoisoptera as they started outcompeting Kalotermitidae. The second shift involved multiple lineages of Neoisoptera, especially Termitidae, which diversified as they colonized the world after the global cooling initiated at the Eocene-Oligocene transition. Our results indicate that termites became the dominant insect decomposers of tropical ecosystems as global climate change impacted ecosystems.

evolutionary biology↗

bioRxiv2025

Horizontal gene transfers are widespread across termite genomes but do not confer metabolic innovations

Horizontal gene transfer (HGT), the transmission of genetic material across species, is an important innovation source in prokaryotes. In contrast, its significance is unclear in many eukaryotes, including insects. Here, we used high-quality genomes of 45 termites and two cockroaches to investigate HGTs across blattodean genomes. We identified 289 genes and 2,494 pseudogenes classified into 168 orthologous groups originating from an estimated 281 HGT events. Wolbachia represented the primary HGT source, while termite gut bacteria and the cockroach endosymbiont Blattabacterium did not contribute meaningfully to HGTs. Most horizontally acquired genes descended from recent and species-specific HGTs, experienced frequent duplications and pseudogenizations, and accumulated substitutions faster than synonymous sites of native protein-coding genes. Genes frequently transferred horizontally to termite genomes included mobile genetic elements and genetic information processing genes. Our results indicate that termites continuously acquired genes through HGT, which they soon lost, leaving few horizontally acquired genes conserved across lineages.

genomics↗

bioRxiv2025

Unravelling termite evolution with 47 high-resolution genome assemblies

Termites are a lineage of social cockroaches abundant in tropical ecosystems where they are key decomposers of organic matter from wood to soil. Despite their ecological significance, only a handful of reference-quality termite genomes have been sequenced, which is insufficient to unravel the genetic mechanisms that have contributed to their ecological success. Here, we performed sequencing and hybrid assembly of 45 taxonomically and ecologically diverse termites and two cockroaches, resulting in haplotype-merged genome assemblies of 47 species, 22 of which were near-chromosome level. Next, we examined the link between termite dietary evolution and major genomic events. We found that Termitidae, which include [~]80% of described termite species, have larger genomes with more genes and a higher proportion of transposons than other termites. Our analyses identified a gene number expansion early in the evolution of Termitidae, including an expansion of the repertoire of CAZymes, the genes involved in lignocellulose degradation. Notably, this expansion of genomes and gene repertoires coincided with the origin of soil-feeding in Termitidae and remained unchanged in lineages that secondarily reverted to a wood-based diet. Overall, our sequencing effort multiplied the number of available termite genomes by six and provided unprecedented insights into the genome evolution of the most ancient lineage of social insects.

genomics↗

bioRxiv2023

Extinct and extant termites reveal the fidelity of behavior fossilization in amber

Fossils encompassing multiple individuals provide rare direct evidence of behavioral interactions among extinct organisms. However, the fossilization process can alter the spatial relationship between individuals and hinder behavioral reconstruction. Here, we report a Baltic amber inclusion preserving a female-male pair of the extinct termite species Electrotermes affinis. The head-to-abdomen contact in the fossilized pair resembles the tandem courtship behavior of extant termites, although their parallel body alignment differs from the linear alignment typical of tandem runs. To solve this inconsistency, we simulated the first stage of amber formation, the immobilization of captured organisms, by exposing living termite tandems to sticky surfaces. We found that the posture of the fossilized pair matches trapped tandems and differs from untrapped tandems. Thus, the fossilized pair likely is a tandem running pair, representing the first direct evidence of the mating behavior of extinct termites. Furthermore, by comparing the positions of partners on a sticky surface and in the amber inclusion, we estimated to 67% the probability that the leader role in the fossilized tandem was performed by a male. Our results demonstrate that past behavioral interactions can be reconstructed despite the spatial distortion of body poses during fossilization. Our taphonomic approach clarifies how certain behaviors can be inferred from fossil occurrences.

evolutionary biology↗

bioRxiv2023

Dating in the Dark: Elevated Substitution Rates in Cave Cockroaches (Blattodea: Nocticolidae) Have Negative Impacts on Molecular Date Estimates

Rates of nucleotide substitution vary substantially across the Tree of Life, with potentially confounding effects on phylogenetic and evolutionary analyses. A large acceleration in mitochondrial substitution rate occurs in the cockroach family Nocticolidae, which predominantly inhabit subterranean environments. To evaluate the impacts of this among-lineage rate heterogeneity on estimates of phylogenetic relationships and evolutionary timescales, we analysed nuclear ultraconserved elements (UCEs) and mitochondrial genomes from nocticolids and other cockroaches. Substitution rates were substantially elevated in nocticolid lineages compared with other cockroaches, especially in mitochondrial protein-coding genes. This disparity in evolutionary rates is likely to have led to different evolutionary relationships being supported by phylogenetic analyses of mitochondrial genomes and UCE loci. Furthermore, Bayesian dating analyses using relaxed-clock models inferred much deeper divergence times compared with a flexible local clock. Our phylogenetic analysis of UCEs, which is the first genome-scale study to include all ten major cockroach families, unites Corydiidae and Nocticolidae and places Anaplectidae as the sister lineage to the rest of Blattoidea. We uncover an extraordinary level of genetic divergence in Nocticolidae, including two highly distinct clades that separated [~]115 million years ago despite both containing representatives of the genus Nocticola. The results of our study highlight the potential impacts of high among-lineage rate variation on estimates of phylogenetic relationships and evolutionary timescales.

evolutionary biology↗

bioRxiv2021

Using ultraconserved elements to reconstruct the termite tree of life

The phylogenetic history of termites has been investigated using mitochondrial genomes and transcriptomes. However, both sets of markers have specific limitations. Mitochondrial genomes represent a single genetic marker likely to yield phylogenetic trees presenting incongruences with species trees, and transcriptomes can only be obtained from well-preserved samples. In contrast, ultraconserved elements (UCEs) include a great many independent markers that can be retrieved from poorly preserved samples. Here, we designed termite-specific baits targeting 50,616 UCE loci. We tested our UCE bait set on 42 samples of termites and three samples of Cryptocercus, for which we generated low-coverage highly-fragmented genome assemblies and successfully extracted in silico between 3,426 to 42,860 non-duplicated UCEs per sample. Our maximum likelihood phylogenetic tree, reconstructed using the 5,934 UCE loci retrieved from upward of 75% of samples, was congruent with transcriptome-based phylogenies, demonstrating that our UCE bait set is reliable and phylogenetically informative. Combined with non-destructive DNA extraction protocols, our UCE bait set provides the tool needed to carry out a global taxonomic revision of termites based on poorly preserved specimens such as old museum samples. The Termite UCE database is maintained at: https://github.com/oist/TER-UCE-DB/.

evolutionary biology↗

bioRxiv2021

Neoisoptera repetitively colonised Madagascar after the Middle Miocene climatic optimum

Madagascar is home to many endemic plant and animal species owing to its ancient isolation from other landmasses. This unique fauna includes several lineages of termites, a group of insects known for their key role in organic matter decomposition in many terrestrial ecosystems. How and when termites colonised Madagascar remains unknown. In this study, we used 601 mitochondrial genomes, 93 of which were generated from Madagascan samples, to infer the global historical biogeography of Neoisoptera, a lineage containing upwards of 80% of described termite species. Our results indicate that Neoisoptera colonised Madagascar between seven to ten times independently during the Miocene, between 8.4-16.6 Ma (95% HPD: 6.1-19.9 Ma). This timing matches that of the colonization of Australia by Neoisoptera. Furthermore, the taxonomic composition of the Neoisopteran fauna of Madagascar and Australia are strikingly similar, with Madagascar harbouring an additional two lineages absent from Australia. Therefore, akin to Australia, Neoisoptera colonised Madagascar during the global expansion of grasslands, possibly helped by the ecological opportunities arising from the spread of this new biome.

ecology↗

bioRxiv2021

Historical biogeography of early diverging termite lineages (Isoptera: Teletisoptera)

Termites are social cockroaches distributed throughout warm temperate and tropical ecosystems. The ancestor of modern termites (crown-Isoptera) occurred during the earliest Cretaceous, approximately 140 million years ago, suggesting that both vicariance through continental drift and overseas dispersal may have shaped the distribution of early diverging termite lineages. We reconstruct the historical biogeography of three early diverging termite families - Stolotermitidae, Hodotermitidae, and Archotermopsidae - using the nuclear rRNA genes and mitochondrial genomes of 27 samples. Our analyses confirmed the monophyly of Stolotermitidae + Hodotermitidae + Archotermopsidae (clade Teletisoptera), with Stolotermitidae diverging from a monophyletic Hodotermitidae + Archotermopsidae approximately 100.3 Ma (94.3-110.4 Ma, 95% HPD), and with Archotermopsidae paraphyletic to a monophyletic Hodotermitidae. The Oriental Archotermopsis and the Nearctic Zootermopsis diverged 50.8 Ma (40.7-61.4 Ma, 95% HPD) before land connections between the Palearctic region and North America ceased to exist. The African Hodotermes + Microhodotermes diverged from Anacanthotermes, a genus found in Africa and Asia, 32.1 Ma (24.8-39.9 Ma, 95% HPD), and the most recent common ancestor of Anacanthotermes lived 10.7 Ma (7.3-14.3 Ma, 95% HPD), suggesting that Anacanthotermes dispersed to Asia using the land bridge connecting Africa and Eurasia [~]18-20 Ma. In contrast, the common ancestors of modern Porotermes and Stolotermes lived 20.2 Ma (15.7-25.1 Ma, 95% HPD) and 26.6 Ma (18.3-35.6 Ma, 95% HPD), respectively, indicating that the presence of these genera in South America, Africa, and Australia involved over-water dispersals. Our results suggest that early diverging termite lineages acquired their current distribution through a combination of over-water dispersals and dispersal via land bridges. We clarify the classification by resolving the paraphyly of Archotermopsidae, restricting the family to Archotermopsis and Zootermopsis, and elevating Hodotermopsinae (Hodotermopsis) as Hodotermopsidae (status novum).

evolutionary biology↗