Termite colonies are typically founded by a pair of sexually reproducing dispersers, which can sometimes be replaced by some of their offspring. Some Reticulitermes and Embiratermes species routinely practice asexual queen succession (AQS): the queen is replaced by neotenic daughters produced by parthenogenesis, which mate with the primary king. Here, to cast light on the evolution of AQS, we investigated another candidate species, Cavitermes tuberosus (Termitinae). Of 95 nests, 39 contained a primary queen and 28 contained neotenic females (2-667 individuals), usually with the primary king. Microsatellite analyses confirmed that colonies were initiated by single pairs after large dispersal flights. More than 80% of the neotenic females were of exclusively maternal origin and completely homozygous, suggesting automictic parthenogenesis with gamete duplication. Conversely, workers, soldiers, and most alates and primary reproductives were produced sexually. AQS often occurs late, after colonies have reached maturity, whereas early AQS in other species may boost the young colony's growth rate. We suggest additional benefits of AQS in C. tuberosus, related with a smaller size, lesser stability and higher mobility of colonies. Our data add to the phylogenetical dispersion and diversity of modalities of AQS in termites, supporting a multiple evolutionary origin of this process.
Termites are social cockroaches distributed throughout warm temperate and tropical ecosystems. The ancestor of modern termites roamed the earth during the early Cretaceous, suggesting that both vicariance and overseas dispersal may have shaped the distribution of early diverging termites. We investigate the historical biogeography of three early diverging termite families –Stolotermitidae, Hodotermitidae and Archotermopsidae (clade Teletisoptera) – using the nuclear rRNA genes and mitochondrial genomes of 27 samples. Our analyses confirm the monophyly of Teletisoptera, with Stolotermitidae diverging from Hodotermitidae + Archotermopsidae approximately 100 Ma. Although Hodotermitidae are monophyletic, our results demonstrate the paraphyly of Archotermopsidae. Phylogenetic analyses indicate that the timing of divergence among the main lineages of Hodotermitidae + Archotermopsidae are compatible with vicariance. In the Stolotermitidae, however, the common ancestors of modern Porotermes Hagen and Stolotermes Hagen are roughly as old as 20 and 35 Ma, respectively, indicating that the presence of these genera in South America, Africa and Australia involved over‐water dispersals. Overall, 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 Desneux and Zootermopsis Emerson and elevating Hodotermopsinae (Hodotermopsis Holmgren) as Hodotermopsidae (status novum).
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.
Background 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. Results 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. Conclusions 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. Electronic supplementary material The online version of this article (10.1186/s12862-019-1459-3) contains supplementary material, which is available to authorized users.
One sentence summary: The parthenogenetic termite Cavitermes tuberosus and the reproductive parasite Wolbachia are partners that likely engage in an intimate insect-bacteria nutritional partnership. † These authors contributed equally to this study. ‡ Simon Hellemans, http://orcid.org/0000-0003-1266-9134 § Nicolas Kaczmarek, ABSTRACTWolbachia has deeply shaped the ecology and evolution of many arthropods, and interactions between the two partners are a continuum ranging from parasitism to mutualism. Non-dispersing queens of the termite Cavitermes tuberosus are parthenogenetically produced through gamete duplication, a mode of ploidy restoration generally induced by Wolbachia. These queens display a bacteriome-like structure in the anterior part of the mesenteron. Our study explores the possibility of a nutritional mutualistic, rather than a parasitic, association between Wolbachia and C. tuberosus. We found a unique strain (wCtub), nested in the supergroup F, in 28 nests collected in French Guiana, the island of Trinidad and the state of Paraíba, Brazil (over 3500 km). wCtub infects individuals regardless of caste, sex or reproductive (sexual versus parthenogenetic) origin. qPCR assays reveal that Wolbachia densities are higher in the bacteriome-like structure and in the surrounding gut compared to other somatic tissues. High-throughput 16S rRNA gene amplicon sequencing reveals that Wolbachia represents over 97% of bacterial reads present in the bacteriome structure. BLAST analyses of 16S rRNA, bioA (a gene of the biosynthetic pathway of B vitamins) and five multilocus sequence typing genes indicated that wCtub shares 99% identity with wCle, an obligate nutritional mutualist of the bedbug Cimex lectularius.
In termite species with asexual queen succession (AQS), parthenogenetically produced immatures mostly differentiate into secondary queens, called "neotenics." In order to elucidate the ontogenetic origin of neotenics in Cavitermes tuberosus (Termitidae: Termitinae), a neotropical termite with AQS, we investigated developmental pathways of offspring according to their sex and genetic origin using both morphometric and genetic tools. The caste system of C. tuberosus follows the classical pathway of Termitidae. After the first larval instar, there is a bifurcation between two developmental lines. The apterous line is composed of a second larval instar, several worker instars, presoldiers, and soldiers. Workers display a consistent male bias and soldiers are female-only. The nymphal line is composed of five nymphal instars and the imago stage. We highlight that neotenic queens derive from third and fourth instar nymphs displaying peculiar morphological traits, here termed "aspirants," most of which are produced by parthenogenesis. Aspirants are present in all nests and perform worker tasks while waiting for the queen's death to differentiate into neotenic queens. Aspirants can successfully be used to demonstrate the occurrence of parthenogenesis in termite species whose reproductive cores are difficult to access.
Termites are major decomposers in terrestrial ecosystems and the second most diverse lineage of social insects. The Kalotermitidae form the second-largest termite family and are distributed across tropical and subtropical ecosystems, where they typically live in small colonies confined to single wood items inhabited by individuals with no foraging abilities. How the Kalotermitidae have acquired their global distribution patterns remains unresolved. Similarly, it is unclear whether foraging is ancestral to Kalotermitidae or was secondarily acquired in a few species. These questions can be addressed in a phylogenetic framework. We inferred time-calibrated phylogenetic trees of Kalotermitidae using mitochondrial genomes of ∼120 species, about 27% of kalotermitid diversity, including representatives of 21 of the 23 kalotermitid genera. Our mitochondrial genome phylogenetic trees were corroborated by phylogenies inferred from nuclear ultraconserved elements derived from a subset of 28 species. We found that extant kalotermitids shared a common ancestor 84 Mya (75–93 Mya 95% HPD), indicating that a few disjunctions among early-diverging kalotermitid lineages may predate Gondwana breakup. However, most of the ∼40 disjunctions among biogeographic realms were dated at less than 50 Mya, indicating that transoceanic dispersals, and more recently human-mediated dispersals, have been the major drivers of the global distribution of Kalotermitidae. Our phylogeny also revealed that the capacity to forage is often found in early-diverging kalotermitid lineages, implying the ancestors of Kalotermitidae were able to forage among multiple wood pieces. Our phylogenetic estimates provide a platform for critical taxonomic revision and future comparative analyses of Kalotermitidae.
Some species of termites evolved an outstanding reproductive strategy called asexual queen succession (AQS), in which the primary queen is replaced by multiple parthenogenetically produced daughters (neotenics) that mate with the primary king. When the primary king is eventually replaced, this time by sexually produced neotenic king(s), sex-asymmetric inbreeding occurs and the queen's genome is more transmitted than that of the king, thereby increasing the reproductive value of female dispersers, and female-biased population sex ratio is expected. Yet, the life cycle, the breeding system dynamics and AQS modalities differ between AQS species, thereby modifying the relative genetic contribution of primary reproductives in the colony and thus also the equilibrium sex ratio. We estimated colonial and population sex ratio over two consecutive dispersal periods in a French Guiana population of Cavitermes tuberosus (Termitinae) in which the founding queen may be replaced only after colony maturity, some neotenic females may be sexually produced, and some female dispersers arise through parthenogenesis. Colonial sex ratio varied among colonies: primary-headed nests with higher within-nest relatedness produced more females than neotenic-headed nests with lower relatedness among individuals. Over the two dispersal periods, the population investment sex ratio fluctuated around 1:1, thereby confirming that AQS breeding system is not necessarily linked with female-biased sex ratio. The balanced alate sex ratio, combined with the occurrence of sexually produced neotenic queens, is possibly the outcome of a queen-king conflict between the primary reproductives.
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