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

Abstract

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.

Evolution of the asexual queen succession system and its underlying mechanisms in termites

“…Therefore, it was astonishing that the mode of thelytoky in a higher termite, E. neotenicus, was found to be most like automixis with central fusion (Fougeyrollas et al, 2015). This is not the case for thelytoky of another higher termite, C. tuberosus, where parthenogens are completely homozygous, suggesting gamete duplication (Fournier et al, 2016). thelytokous parthenogenesis and eventually replace the old queens (Fig.…”

“…AQS was first identified in a lower termite species, R. speratus (Matsuura et al, 2009), and later confirmed in two other species of the same genus, R. virginicus (Vargo et al, 2012) and R. lucifugus (Luchetti et al, 2013), and was recently identified in two species of higher termite (Termitidae), E. neotenicus (Fougeyrollas et al, 2015) and C. tuberosus (Fournier et al, 2016) (Table 1).…”

“…However, the actual mechanism of ploidy restoration in C. tuberosus remains to be identified by cytological observation because complete homozygosity of the offspring can also be explained by terminal fusion without recombination. Regardless, as the mechanism of parthenogenesis is different in the two AQS higher termites, it is likely that AQS evolved independently in Embiratermes and Cavitermes (Fournier et al, 2016). To date, five independent origins of AQS have been suggested, including three independent origins in Reticulitermes termites.…”

“…In the soil-feeding higher termite C. tuberosus (Termitidae, Termitinae), colonies frequently contain numerous neotenic females (2-667 individuals, n=28 colonies) usually with a single primary king (Fournier et al, 2016), suggesting a high probability of AQS. This species is ecologically close to the AQS higher termite E. neotenicus, but belongs to a different subfamily of the Termitidae.…”

“…Unusual modes of reproduction, in which queens use sex for somatic growth but use parthenogenesis for germline production, have been uncovered both in the ants Cataglyphis cursor (Pearcy et al, 2004), Wasmannia auropunctata (Fournier et al, 2005), Vollenhovia emeryi (Ohkawara et al, 2006), Paratrechina longicornis , Cataglyphis hispanica (Leniaud et al, 2012), Cataglyphis velox, Cataglyphis mauritanica (Eyer et al, 2013) and Cardiocondyla kagutsuchi (Okita and Tsuchida, 2016), and in the termites Reticulitermes speratus (Matsuura et al, 2009), Reticulitermes virginicus (Vargo et al, 2012), Reticulitermes lucifugus (Luchetti et al, 2013), Embiratermes neotenicus (Fougeyrollas et al, 2015) and Cavitermes tuberosus (Fournier et al, 2016).…”