Preadaptation for parthenogenetic colony foundation in subterranean termites Reticulitermes spp. (Isoptera: Rhinotermitidae)

Abstract

Thelytokous (all-female producing) parthenogenesis, in some cases, involves reproductive advantages against obligate sexual reproduction. However, the completion of parthenogenesis takes multiple steps without the help of males, and thus preadaptation that meets those requirements will be an important factor for the evolution of parthenogenesis. The Japanese subterranean termite, Reticulitermes speratus, is known to have the ability of parthenogenetic colony foundation, where females that failed to mate with males found colonies cooperatively with partner females and reproduce by parthenogenesis. In this study, we compared the parthenogenetic ability and the colony initiation behavior among six Reticulitermes species in Japan. All species other than R. speratus were not able to reproduce parthenogenetically. Nevertheless, females of these species without the parthenogenetic ability performed homosexual female-female colony initiation and produced eggs without fertilization. In addition, in one species without parthenogenetic reproduction, R. kanmonensis, female-female pair initiated founding behavior as quickly as a heterosexual pair. These results suggest that female-female colony initiation and virgin egg-laying are predominant characters among the genus Reticulitermes and provide a preadaptive condition for parthenogenetic colony foundation in R. speratus.

Parthenogenesis in Hexapoda: Entognatha and non-holometabolous insects

“…More about R. speratus reproduction and cytogenetics can be found in Matsuura et al. () and also in Kawatsu and Matsuura (). Experimental data about rearing of parthenogenetic termites also exist (Howard et al.…”

“…Yet, both parthenogenetic and bisexual colonies are infested with Wolbachia, suggesting the absence of correlation between infection and reproductive mode. More about R. speratus reproduction and cytogenetics can be found in Matsuura et al (2004) and also in Kawatsu and Matsuura (2013). Experimental data about rearing of parthenogenetic termites also exist (Howard et al 1981;Hayashi et al 2003;Matsuura and Kobayashi 2007).…”

Loss of males from mixed-sex societies in termites

“…Termite parthenogenesis is expected to be thelytokous rather than arrhenotokous because of the XY sex determination system found in most species [ 16 ]. Although thelytokous parthenogenesis has been reported in some termites, this is restricted to the production of neotenic (secondary) reproductives in nature [ 16 , 17 ] (but see also [ 18 , 19 ] for the ability of parthenogenetic colony foundation of these “asexual queen succession (AQS)” termites in the laboratory). Importantly, both male and female workers and soldiers continue to be produced sexually in natural AQS colonies [ 16 , 17 ], indicating that males play a critical role beyond that of reproduction in termite societies.…”

Physiological profiles associated with ceasing growth of unfertilized eggs produced by unmated queens in the subterranean termite Reticulitermes chinensis

“…This AQS system enables the primary queen to maintain her full genetic contribution to the next generation while avoiding any loss of genetic diversity from inbreeding ( Matsuura, 2011 ). Most of the work conducted on the AQS system in termites has focused on the discovery of new AQS species and the mechanism of facultative parthenogenesis ( Fougeyrollas et al, 2015 ; Kawatsu and Matsuura, 2013 ; Luchetti et al, 2013 ; Roisin et al, 2014 ; Vargo et al, 2012 ; Yashiro and Matsuura, 2014 ). Some termite species that are evolutionally related to AQS species of termites have been demonstrated to exhibit neither AQS nor parthenogenesis ( Kawatsu and Matsuura, 2013 ; Luchetti et al, 2013 ); however little is known about why these termite species have no AQS and specifically why unfertilized eggs produced by unmated queens of these species are unable to hatch.…”