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

Abstract

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.

Bacteriome-associatedWolbachiaof the parthenogenetic termiteCavitermes tuberosus

“…Alates initiate new colonies after a nuptial flight and become primary reproductives while neotenics stay in the nest to replace primaries upon their death. Adapted from Hellemans et al (2017b). To enhance its own transmission, Wolbachia could induce thelytokous parthenogenesis in C. tuberosus.…”

“…In C. tuberosus, neotenic queens display an empty digestive tube and receive nutriments through mouthto-mouth exchanges (i.e. trophallaxis) with workers (Hellemans et al 2017b). Composition of the gut community of workers shows a potential capacity allowing to feed on diverse lignocellulose rich biomass (Fig.…”

Nest composition, stable isotope ratios and microbiota unravel the feeding behaviour of an inquiline termite

“…Cavitermes tuberosus (Emerson 1925) is a broad-spectrum inquiline colonizing arboreal nests built by other species, with a large neotropical distribution (Mathews 1977;Constantino 1991;Martius 1997;Apolinário and Martius 2004;Krishna et al 2013b). This species was demonstrated to undergo asexual queen succession: queens sexually produce several generations of winged reproductives that disperse and colonize new nests, while they parthenogenetically produce numerous secondary queens that reproduce within their mother's nest, thereby increasing the colony reproductive output (Fournier et al 2016;Hellemans et al 2017bHellemans et al , 2019a. Also, these secondary reproductives are small, which may present the advantage of remaining able to circulate through the small galleries at the margins of the host's nest-a probable constraint for physogastric queens.…”

Widespread occurrence of asexual reproduction in higher termites of the Termes group (Termitidae: Termitinae)

“…The majority of these neotenic queens (82%) bear only maternal alleles and are homozygous at all loci, which suggests their origin through thelytokous parthenogenesis via automixis with gamete duplication [13]. They develop from nymphs of the third and fourth stage through a transitional subfertile stage of “aspirants” [17] and reproduce with the founding primary king. In comparison with AQS cases in Syntermitinae, the replacement of the foundress by parthenogens in C. tuberosus takes place rather late in the colony life cycle.…”