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

Abstract

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.

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

“…We conducted a meta‐analysis of classical nymphs N3 and N4, and aspirants from all nests presented in Fournier et al (): (i) the sex ratio of classical nymphs N4 is balanced (205 individuals, 12 nests, sex ratio = 0.376 ± 0.270; one sample t ‐test; t = −1.595, df = 11, p = 0.139) in accordance with the sex ratio in alates (Hellemans, Fournier, Hanus, & Roisin in prep), while the sex ratio in aspirants is highly female‐biased (990 individuals, 40 nests, sex ratio = 0.835 ± 0.294; Wilcoxon rank sum test, W = 690.5, p < 0.001); (ii) female aspirants were mainly of parthenogenetic origin (92.2%, n = 193); and (iii) aspirants were found in almost all nests, including those containing alates (13 out of 17 nests), indicating that they develop independently of the massive nymphal production prior to dispersal. At several occasions, we observed directly aspirants molting into neotenics (Figure d–f).…”

“…Nymphoid neotenics were frequently found in nests of C. tuberosus , and their occurrence is most likely a normal step in the colony's life cycle (Fournier et al, ). Neotenics have been reported from several species in the clade comprising Cavitermes, its close relative Spinitermes , Palmitermes impostor , (see Hellemans et al, , ; Kyjaková et al, , for recent phylogenies): Spinitermes brevicornutus, S. nigrostomus (review in Noirot, ), S. robustus , S. trispinosus (Carrijo, ), Termes hospes (Noirot, ), T. laticornis , T. riograndensis (as T. saltans ; Noirot, ), and several Australian taxa probably part of the same clade: Xylochomitermes (as Termes ) occidualis , X. reductus , Hesperotermes infrequens (Gay, ), and Cristatitermes pineaformis , in which Miller () mentions two occurrences of multiple neotenic females with an imaginal king. Although the reports of neotenics are few, the ability to produce nymphoid neotenics, sometimes in the pattern very reminiscent of the AQS breeding system, appears widespread in this clade.…”

“…Furthermore, nymphs of the same morphology as aspirants in C. tuberosus were determined to be parthenogenetically produced also in Palmitermes impostor , the sister genus of Cavitermes (Hellemans et al, , ). Therefore, aspirants can be a useful clue for the detection of parthenogenesis (and AQS) in other species since the actual breeding system is often masked by the genetic uniformity of the sterile castes and reproductive cores are not always easy to find, while aspirants can be found throughout the nest.…”

Asexual Queen Succession in Termites

“…AQS was initially described from the Japanese Rhinotermitidae Reticulitermes speratus (Matsuura et al 2009), and later found in two additional species of Reticulitermes (Vargo et al Asexual queen succession in termites (A29115) 8 2012; Luchetti et al 2013). More recently, it was reported in several species of Termitidae belonging to Syntermitinae and Termitinae subfamilies (Fougeyrollas et al 2015;Fournier et al 2016;Fougeyrollas et al 2017;Hellemans et al 2019a). Because AQS occurs in phylogenetically distant taxa, in contrasted ecological contexts -in temperate wood-feeding subterranean Rhinotermitidae and in neotropical soil-feeding Termitidae-and under different modalities of ploidy restoration (see Genetic consequences of Asexual Queen Succession below), it appears clear that this breeding system evolved independently several times (Dedeine et al 2016;Matsuura 2017;Hellemans et al 2019a).…”

Genomic imprinting and evolution of insect societies

“…10–5 million years ago) and in North America (less than 14.1 million years ago) (Dedeine et al, ). Recent surveys of the breeding systems of higher termites (Termitidae) in French Guiana have repeatedly identified AQS in Neotropical termitids including Embiratermes neotenicus (Syntermitinae) (Fougeyrollas et al, ), the humivorous termite Cavitermes tuberosus (Termitinae) (Fournier, Hellemans, Hanus, & Roisin, ), Silvestritermes minutus (Syntermitinae) (Fougeyrollas et al, ) and Palmitermes impostor (Termitinae) (Hellemans et al, ). In all of these seven AQS species, the asexual neotenic queens derive from nymphs, that is, the sexual pathway.…”