Simon Hellemans

Facultative asexual reproduction and genetic diversity of populations in the humivorous termite Cavitermes tuberosus.

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 colonys 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.

Mitochondrial and chemical profiles reveal a new genus and species of Neotropical termite with snapping soldiers, Palmitermes impostor (Termitidae : Termitinae)

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.

Secondary queens in the parthenogenetic termite Cavitermes tuberosus develop through a transitional helper stage

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 queens 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.

Sex ratio variations among years and breeding systems in a facultatively parthenogenetic termite

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.