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  • Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae
    Cellular and Molecular Life Sciences, 2021
    Co-Authors: Thomas Chouvenc, Jan Sobotnik, Michael S. Engel, Thomas Bourguignon
    Abstract:

    Termites are a clade of eusocial wood-feeding roaches with > 3000 described species. Eusociality emerged ~ 150 million years ago in the ancestor of modern termites, which, since then, have acquired and sometimes lost a series of adaptive traits defining of their evolution. Termites primarily feed on wood, and digest cellulose in association with their obligatory nutritional mutualistic gut microbes. Recent advances in our understanding of termite phylogenetic relationships have served to provide a tentative timeline for the emergence of innovative traits and their consequences on the ecological success of termites. While all “lower” termites rely on cellulolytic protists to digest wood, “higher” termites (Termitidae), which comprise ~ 70% of termite species, do not rely on protists for digestion. The loss of protists in Termitidae was a critical evolutionary step that fostered the emergence of novel traits, resulting in a diversification of morphology, diets, and niches to an extent unattained by “lower” termites. However, the mechanisms that led to the initial loss of protists and the succession of events that took place in the termite gut remain speculative. In this review, we provide an overview of the key innovative traits acquired by termites during their evolution, which ultimately set the stage for the emergence of “higher” termites. We then discuss two hypotheses concerning the loss of protists in Termitidae, either through an externalization of the digestion or a dietary transition. Finally, we argue that many aspects of termite evolution remain speculative, as most termite biological diversity and evolutionary trajectories have yet to be explored.

  • trail following pheromones in the termite subfamily syntermitinae blattodea termitoidae Termitidae
    Journal of Chemical Ecology, 2020
    Co-Authors: David Sillamdusses, Alain Robert, Etienne Sémon, Thomas Bourguignon, Eliana M. Cancello, Jan Sobotnik, Chloe Leroy, Michael J Lacey
    Abstract:

    Trail-following behavior is a key to ecological success of termites, allowing them to orient themselves between the nesting and foraging sites. This behavior is controlled by specific trail-following pheromones produced by the abdominal sternal gland occurring in all termite species and developmental stages. Trail-following communication has been studied in a broad spectrum of species, but the “higher” termites (i.e. Termitidae) from the subfamily Syntermitinae remain surprisingly neglected. To fill this gap, we studied the trail-following pheromone in six genera and nine species of Syntermitinae. Our chemical and behavioral experiments showed that (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol is the single component of the pheromone of all the termite species studied, except for Silvestritermes euamignathus. This species produces both (3Z,6Z)-dodeca-3,6-dien-1-ol and neocembrene, but only (3Z,6Z)-dodeca-3,6-dien-1-ol elicits trail-following behavior. Our results indicate the importance of (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol, the most widespread communication compound in termites, but also the repeated switches to other common pheromones as exemplified by S. euamignathus.

  • Evolution of Termite Symbiosis Informed by Transcriptome-Based Phylogenies
    'Elsevier BV', 2019
    Co-Authors: Ales Bucek, Yves Roisin, Jan Sobotnik, Mang Shi, Dino P. Mcmahon, Edward C. Holmes, Thomas Bourguignon
    Abstract:

    Termitidae comprises approximately 80% of all termite species [1] that play dominant decomposer roles in tropical ecosystems [2, 3]. Two major events during termite evolution were the loss of cellulolytic gut protozoans in the ancestor of Termitidae and the subsequent gain in the termitid subfamily Macrotermitinae of fungal symbionts cultivated externally in "combs" constructed within the nest [4, 5]. How these symbiotic transitions occurred remains unresolved. Phylogenetic analyses of mitochondrial data previously suggested that Macrotermitinae is the earliest branching termitid lineage, followed soon after by Sphaerotermitinae [6], which cultivates bacterial symbionts on combs inside its nests [7]. This has led to the hypothesis that comb building was an important evolutionary step in the loss of gut protozoa in ancestral termitids [8]. We sequenced genomes and transcriptomes of 55 termite species and reconstructed phylogenetic trees from up to 4,065 orthologous genes of 68 species. We found strong support for a novel sister-group relationship between the bacterial comb-building Sphaerotermitinae and fungus comb-building Macrotermitinae. This key finding indicates that comb building is a derived trait within Termitidae and that the creation of a comb-like "external rumen" involving bacteria or fungi may not have driven the loss of protozoa from ancestral termitids, as previously hypothesized. Instead, associations with gut prokaryotic symbionts, combined with dietary shifts from wood to other plant-based substrates, may have played a more important role in this symbiotic transition. Our phylogenetic tree provides a platform for future studies of comparative termite evolution and the evolution of symbiosis in this taxon

  • mitochondrial and chemical profiles reveal a new genus and species of neotropical termite with snapping soldiers palmitermes impostor Termitidae termitinae
    Invertebrate Systematics, 2017
    Co-Authors: Simon Hellemans, Robert Hanus, Thomas Bourguignon, Pavlína Kyjaková, Yves Roisin
    Abstract:

    Since the inception of Linnaean taxonomy, termite species and genus descriptions have been mostly based on the morphology of soldiers, sometimes complemented by alate characters, though these are seldom discriminant. However, narrowly soldier-based descriptions may overemphasise ancestral characters and lead to the establishment of non-monophyletic taxa. In this paper, we used an integrative taxonomic approach that incorporates the morphology of all castes, including workers, as well as molecular and chemical data, to describe Palmitermes impostor Hellemans & Roisin, 2017 (Termitidae:Termitinae), a new termite genus and species from French Guiana. Although the soldiers of P. impostor resemble those of Termes Linnaeus, 1758, the digestive tract and mandibles of workers suggest that Palmitermes is closely related to Cavitermes Emerson, 1925. The sister-group relationship between Palmitermes and Cavitermes was confirmed by a phylogenetic reconstruction based on full mitochondrial genome sequences as well as by the comparison of the profiles of cuticular hydrocarbons of workers with those of related taxa. Our study illustrates the benefits of using an integrative taxonomic approach to describe new taxa and the pitfalls of using soldier morphology as the exclusive set of characters in termite systematics.

  • Nutrient Recycling Starts in the Canopy: The Secretive Action of Termites
    Treetops at Risk, 2013
    Co-Authors: Yves Roisin, Thomas Bourguignon, Maurice Leponce
    Abstract:

    The role of termites as decomposers is undisputed at the level of the tropical forest floor (Martius 1994; Bignell and Eggleton 2000). The family Termitidae is especially diverse, with many taxa, collectively considered as soil feeders, feeding at a definite level in the humification gradient. Yet, the fundamental source of food for termites is wood, which can be exploited in several ways. Two extreme strategies are illustrated by small-colony dry-wood termites (family KaloTermitidae) and large-colony Nasutitermes (family Termitidae).

Yves Roisin - One of the best experts on this subject based on the ideXlab platform.

  • Widespread occurrence of asexual reproduction in higher termites of the Termes group (Termitidae: Termitinae).
    BMC Evolutionary Biology, 2019
    Co-Authors: Simon Hellemans, Klára Dolejšová, Jan Křivánek, Denis Fournier, Robert Hanus, Yves Roisin
    Abstract:

    A decade ago, the mixed reproductive strategy Asexual Queen Succession (AQS) was first described in termites. In AQS species, the workers, soldiers and dispersing reproductives are produced through sexual reproduction, while non-dispersing (neotenic) queens arise through automictic thelytokous parthenogenesis, replace the founding queen and mate with the founding king. As yet, AQS has been documented in six species from three lineages of lower (RhinoTermitidae) and higher (Termitinae: Termes group and Syntermitinae) termites. Independent evolution of the capacity of thelytoky as a preadaptation to AQS is supported by different mechanisms of automixis in each of the three clades. These pioneering discoveries prompt the question on the extent of thelytoky and AQS in the diversified family of higher termites. Here, we investigated the capacity of thelytoky and occurrence of AQS in three species from the phylogenetic proximity of the neotropical AQS species Cavitermes tuberosus (Termitinae: Termes group): Palmitermes impostor, Spinitermes trispinosus, and Inquilinitermes inquilinus. We show that queens of all three species are able to lay unfertilized eggs, which undergo thelytokous parthenogenesis (via gamete duplication as in C. tuberosus) and develop through the transitional stage of aspirants into replacement neotenic queens. The breeding system in P. impostor is very reminiscent of that described in C. tuberosus and can be characterized as AQS. In the remaining two species, our limited data do not allow classifying the breeding system as AQS; yet, also in these species the thelytokous production of neotenic females appears to be a systematic element of reproductive strategies. It appears likely that the capacity of thelytokous parthenogenesis evolved once in the Termes group, and may ultimately be found more widely, well beyond these Neotropical species.

  • Evolution of Termite Symbiosis Informed by Transcriptome-Based Phylogenies
    'Elsevier BV', 2019
    Co-Authors: Ales Bucek, Yves Roisin, Jan Sobotnik, Mang Shi, Dino P. Mcmahon, Edward C. Holmes, Thomas Bourguignon
    Abstract:

    Termitidae comprises approximately 80% of all termite species [1] that play dominant decomposer roles in tropical ecosystems [2, 3]. Two major events during termite evolution were the loss of cellulolytic gut protozoans in the ancestor of Termitidae and the subsequent gain in the termitid subfamily Macrotermitinae of fungal symbionts cultivated externally in "combs" constructed within the nest [4, 5]. How these symbiotic transitions occurred remains unresolved. Phylogenetic analyses of mitochondrial data previously suggested that Macrotermitinae is the earliest branching termitid lineage, followed soon after by Sphaerotermitinae [6], which cultivates bacterial symbionts on combs inside its nests [7]. This has led to the hypothesis that comb building was an important evolutionary step in the loss of gut protozoa in ancestral termitids [8]. We sequenced genomes and transcriptomes of 55 termite species and reconstructed phylogenetic trees from up to 4,065 orthologous genes of 68 species. We found strong support for a novel sister-group relationship between the bacterial comb-building Sphaerotermitinae and fungus comb-building Macrotermitinae. This key finding indicates that comb building is a derived trait within Termitidae and that the creation of a comb-like "external rumen" involving bacteria or fungi may not have driven the loss of protozoa from ancestral termitids, as previously hypothesized. Instead, associations with gut prokaryotic symbionts, combined with dietary shifts from wood to other plant-based substrates, may have played a more important role in this symbiotic transition. Our phylogenetic tree provides a platform for future studies of comparative termite evolution and the evolution of symbiosis in this taxon

  • mitochondrial and chemical profiles reveal a new genus and species of neotropical termite with snapping soldiers palmitermes impostor Termitidae termitinae
    Invertebrate Systematics, 2017
    Co-Authors: Simon Hellemans, Robert Hanus, Thomas Bourguignon, Pavlína Kyjaková, Yves Roisin
    Abstract:

    Since the inception of Linnaean taxonomy, termite species and genus descriptions have been mostly based on the morphology of soldiers, sometimes complemented by alate characters, though these are seldom discriminant. However, narrowly soldier-based descriptions may overemphasise ancestral characters and lead to the establishment of non-monophyletic taxa. In this paper, we used an integrative taxonomic approach that incorporates the morphology of all castes, including workers, as well as molecular and chemical data, to describe Palmitermes impostor Hellemans & Roisin, 2017 (Termitidae:Termitinae), a new termite genus and species from French Guiana. Although the soldiers of P. impostor resemble those of Termes Linnaeus, 1758, the digestive tract and mandibles of workers suggest that Palmitermes is closely related to Cavitermes Emerson, 1925. The sister-group relationship between Palmitermes and Cavitermes was confirmed by a phylogenetic reconstruction based on full mitochondrial genome sequences as well as by the comparison of the profiles of cuticular hydrocarbons of workers with those of related taxa. Our study illustrates the benefits of using an integrative taxonomic approach to describe new taxa and the pitfalls of using soldier morphology as the exclusive set of characters in termite systematics.

  • Chemical systematics of Neotropical termite genera with symmetrically snapping soldiers (Termitidae: Termitinae)
    Zoological Journal of the Linnean Society, 2016
    Co-Authors: Pavlína Kyjaková, Klára Dolejšová, Virginie Roy, Anna Jirošová, Jana Krasulová, Jan Křivánek, Romana Hadravová, Jiří Rybáček, Radek Pohl, Yves Roisin
    Abstract:

    Termite soldiers often combine mechanical adaptations with defensive chemicals secreted from the frontal gland. Amongst the most remarkable strategies for mechanical defence, symmetrical and asymmetrical snapping mandibles evolved in several lineages of the diversified subfamily Termitinae (Termitidae). The contribution of the frontal chemical weapon to defence in snapping soldiers has long been doubted and the subfamily Termitinae overlooked with respect to soldier-produced chemicals. We recently reported an active frontal gland secreting unique defensive chemicals in the symmetrically snapping soldiers of Cavitermes tuberosus. The aim of the present study was a larger-scale comparison of chemical defence in symmetrically snapping soldiers. We studied the anatomy of the frontal gland and the chemistry of its secretion in five additional Neotropical species and mapped our observations on a de novo constructed molecular phylogeny of the target group. We show that the soldiers of all studied species possess a functional frontal gland, housed in part in the frontal projections on their heads. Phylogenetic reconstruction groups the studied taxa into two well-defined clades, supported by fundamental differences in defensive chemicals, either arising exclusively from the lipogenic pathway or containing also the products of the isoprenoid pathway. Our results also identify a new genus of symmetrical snappers, related to the genus Cavitermes, incorrectly classified in several previous studies.

  • Nutrient Recycling Starts in the Canopy: The Secretive Action of Termites
    Treetops at Risk, 2013
    Co-Authors: Yves Roisin, Thomas Bourguignon, Maurice Leponce
    Abstract:

    The role of termites as decomposers is undisputed at the level of the tropical forest floor (Martius 1994; Bignell and Eggleton 2000). The family Termitidae is especially diverse, with many taxa, collectively considered as soil feeders, feeding at a definite level in the humification gradient. Yet, the fundamental source of food for termites is wood, which can be exploited in several ways. Two extreme strategies are illustrated by small-colony dry-wood termites (family KaloTermitidae) and large-colony Nasutitermes (family Termitidae).

Daouda Kone - One of the best experts on this subject based on the ideXlab platform.

Simon Hellemans - One of the best experts on this subject based on the ideXlab platform.

  • Widespread occurrence of asexual reproduction in higher termites of the Termes group (Termitidae: Termitinae).
    BMC Evolutionary Biology, 2019
    Co-Authors: Simon Hellemans, Klára Dolejšová, Jan Křivánek, Denis Fournier, Robert Hanus, Yves Roisin
    Abstract:

    A decade ago, the mixed reproductive strategy Asexual Queen Succession (AQS) was first described in termites. In AQS species, the workers, soldiers and dispersing reproductives are produced through sexual reproduction, while non-dispersing (neotenic) queens arise through automictic thelytokous parthenogenesis, replace the founding queen and mate with the founding king. As yet, AQS has been documented in six species from three lineages of lower (RhinoTermitidae) and higher (Termitinae: Termes group and Syntermitinae) termites. Independent evolution of the capacity of thelytoky as a preadaptation to AQS is supported by different mechanisms of automixis in each of the three clades. These pioneering discoveries prompt the question on the extent of thelytoky and AQS in the diversified family of higher termites. Here, we investigated the capacity of thelytoky and occurrence of AQS in three species from the phylogenetic proximity of the neotropical AQS species Cavitermes tuberosus (Termitinae: Termes group): Palmitermes impostor, Spinitermes trispinosus, and Inquilinitermes inquilinus. We show that queens of all three species are able to lay unfertilized eggs, which undergo thelytokous parthenogenesis (via gamete duplication as in C. tuberosus) and develop through the transitional stage of aspirants into replacement neotenic queens. The breeding system in P. impostor is very reminiscent of that described in C. tuberosus and can be characterized as AQS. In the remaining two species, our limited data do not allow classifying the breeding system as AQS; yet, also in these species the thelytokous production of neotenic females appears to be a systematic element of reproductive strategies. It appears likely that the capacity of thelytokous parthenogenesis evolved once in the Termes group, and may ultimately be found more widely, well beyond these Neotropical species.

  • mitochondrial and chemical profiles reveal a new genus and species of neotropical termite with snapping soldiers palmitermes impostor Termitidae termitinae
    Invertebrate Systematics, 2017
    Co-Authors: Simon Hellemans, Robert Hanus, Thomas Bourguignon, Pavlína Kyjaková, Yves Roisin
    Abstract:

    Since the inception of Linnaean taxonomy, termite species and genus descriptions have been mostly based on the morphology of soldiers, sometimes complemented by alate characters, though these are seldom discriminant. However, narrowly soldier-based descriptions may overemphasise ancestral characters and lead to the establishment of non-monophyletic taxa. In this paper, we used an integrative taxonomic approach that incorporates the morphology of all castes, including workers, as well as molecular and chemical data, to describe Palmitermes impostor Hellemans & Roisin, 2017 (Termitidae:Termitinae), a new termite genus and species from French Guiana. Although the soldiers of P. impostor resemble those of Termes Linnaeus, 1758, the digestive tract and mandibles of workers suggest that Palmitermes is closely related to Cavitermes Emerson, 1925. The sister-group relationship between Palmitermes and Cavitermes was confirmed by a phylogenetic reconstruction based on full mitochondrial genome sequences as well as by the comparison of the profiles of cuticular hydrocarbons of workers with those of related taxa. Our study illustrates the benefits of using an integrative taxonomic approach to describe new taxa and the pitfalls of using soldier morphology as the exclusive set of characters in termite systematics.

S. Takeichi - One of the best experts on this subject based on the ideXlab platform.

  • Confirmation of soil‐feeding termites (Isoptera; Termitidae; Termitinae) in Australia using stable isotope ratios
    Functional Ecology, 1998
    Co-Authors: Ichiro Tayasu, Tetsushi Inoue, Leigh R Miller, Atsuko Sugimoto, S. Takeichi
    Abstract:

    1. Carbon (δ13C) and nitrogen (δ15N) stable isotope ratios of termites (Isoptera) were examined in Darwin, northern Australia. It is suggested that the stable isotope technique, together with phylogenetics, is a useful tool to understand the evolution of functional groups in detritivores. 2. A high δ15N value was observed in the Termes-Capritermes branch of the subfamily Termitinae and the genus Amitermes, two distinct taxonomic groups that evolved from wood-feeding to soil-feeding in Australia. Among eight Termes-Capritermes branch species, only two species (Xylochomitermes melvillensis and Ephelotermes melachoma) were discernible as wood/soil interface feeders, the remaining six species analysed were soil-feeders, where the diet preference was identified by using δ15N of workers. 3. The Termes-Capritermes group in Australia contains both wood/soil interface feeders and soil-feeders, whereas wood/soil interface feeders in Cameroon are from the Termes-Capritermes branch while soil-feeders are from Cubitermes group. The result confirmed that soil-feeding forms evolved both in Australia and Africa, but from different phylogenetic groups.

  • confirmation of soil feeding termites isoptera Termitidae termitinae in australia using stable isotope ratios
    Functional Ecology, 1998
    Co-Authors: Ichiro Tayasu, Tetsushi Inoue, Leigh R Miller, Atsuko Sugimoto, S. Takeichi, Takuya Abe
    Abstract:

    1. Carbon (δ13C) and nitrogen (δ15N) stable isotope ratios of termites (Isoptera) were examined in Darwin, northern Australia. It is suggested that the stable isotope technique, together with phylogenetics, is a useful tool to understand the evolution of functional groups in detritivores. 2. A high δ15N value was observed in the Termes-Capritermes branch of the subfamily Termitinae and the genus Amitermes, two distinct taxonomic groups that evolved from wood-feeding to soil-feeding in Australia. Among eight Termes-Capritermes branch species, only two species (Xylochomitermes melvillensis and Ephelotermes melachoma) were discernible as wood/soil interface feeders, the remaining six species analysed were soil-feeders, where the diet preference was identified by using δ15N of workers. 3. The Termes-Capritermes group in Australia contains both wood/soil interface feeders and soil-feeders, whereas wood/soil interface feeders in Cameroon are from the Termes-Capritermes branch while soil-feeders are from Cubitermes group. The result confirmed that soil-feeding forms evolved both in Australia and Africa, but from different phylogenetic groups.