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bourguignon, t.

Publications and source records attributed to bourguignon, t..

8 recordsLinked to original sources

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↗

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↗

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↗

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↗

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↗

The functional evolution of termite gut microbiota

Termites primarily feed on lignocellulose or soil in association with specific gut microbes. The functioning of the termite gut microbiota is partly understood in a handful of wood-feeding pest species, but remains largely unknown in other taxa. We intend to feel this gap and provide a global understanding of the functional evolution of termite gut microbiota. We sequenced the gut metagenomes of 145 samples representative of the termite diversity. We show that the prokaryotic fraction of the gut microbiota of all termites possesses similar genes for carbohydrate and nitrogen metabolisms, in proportions varying with termite phylogenetic position and diet. The presence of a conserved set of gut prokaryotic genes implies that key nutritional functions were present in the ancestor of modern termites. Furthermore, the abundance of these genes largely correlated with the host phylogeny. Finally, we found that the adaptation to a diet of soil by some termite lineages was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes and pathways. Our results reveal that the composition and function of termite gut prokaryotic communities have been remarkably conserved since termites first appeared [~]150 million years ago. Therefore, the "world smallest bioreactor" has been operating as a multipartite symbiosis composed of termites, archaea, bacteria, and cellulolytic flagellates since its inception.

evolutionary biology↗

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↗

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↗