Loss of males from mixed-sex societies in termites

Abstract

BackgroundSexual reproduction is the norm in almost all animal species, and in many advanced animal societies, both males and females participate in social activities. To date, the complete loss of males from advanced social animal lineages has been reported only in ants and honey bees (Hymenoptera), whose workers are always female and whose males display no helping behaviors even in normal sexual species. Asexuality has not previously been observed in colonies of another major group of social insects, the termites, where the ubiquitous presence of both male and female workers and soldiers indicate that males play a critical role beyond that of reproduction.ResultsHere, we report asexual societies in a lineage of the termite Glyptotermes nakajimai. We investigated the composition of mature colonies from ten distinct populations in Japan, finding six asexual populations characterized by a lack of any males in the reproductive, soldier, and worker castes of their colonies, an absence of sperm in the spermathecae of their queens, and the development of unfertilized eggs at a level comparable to that for the development of fertilized eggs in sexual populations of this species. Phylogenetic analyses indicated a single evolutionary origin of the asexual populations, with divergence from sampled sexual populations occurring about 14 million years ago. Asexual colonies differ from sexual colonies in having a more uniform head size in their all-female soldier caste, and fewer soldiers in proportion to other individuals, suggesting increased defensive efficiencies arising from uniform soldier morphology. Such efficiencies may have contributed to the persistence and spread of the asexual lineage. Cooperative colony foundation by multiple queens, the single-site nesting life history common to both the asexual and sexual lineages, and the occasional development of eggs without fertilization even in the sexual lineage are traits likely to have been present in the ancestors of the asexual lineage that may have facilitated the transition to asexuality.ConclusionsOur findings demonstrate that completely asexual social lineages can evolve from mixed-sex termite societies, providing evidence that males are dispensable for the maintenance of advanced animal societies in which they previously played an active social role.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0563-y) contains supplementary material, which is available to authorized users.

Comparative screening of endosymbiotic bacteria associated with the asexual and sexual lineages of the termiteGlyptotermes nakajimai

“…We have recently reported asexual societies in a lineage of the termite Glyptotermes nakajimai (Isoptera: Kalotermitidae)a dramatic transition from mixed-sex to all-female asexual societies. This finding provides evidence that males are not indispensable in advanced animal societies, regardless of whether males engage in social activities or not [7].…”

“…Lack of endosymbiotic bacteria in the asexual lineage of G. nakajimai (Table 1 and Figure 1) is suggestive of another selective force in the evolution of asexuality in the lineage. Indeed, Yashiro et al [7] have demonstrated that asexual colonies of G. nakajimai have a more uniform head size in their all-female soldier caste and fewer soldiers in proportion to other individuals compared with sexual colonies, indicating increased defensive efficiencies arising from asexuality. However, we are unable to rule out the possibility that endosymbiont DNA that causes parthenogenesis was integrated into the host genome, followed by the loss of the donor endosymbiont [14,15].…”

“…Further work is required to investigate the possibility that Wolbachia-induced CI contribute to the maintenance of asexuality in the lineage. Yashiro et al [7] have illustrated that the two lineages containing different chromosome profiles (2n = 35 in the asexual lineage vs 2n = 34 in the sexual lineage), which might also act as a reproductive barrier between the two lineages.…”

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

“…The independent evolution of thelytokous parthenogenesis (TP) in major clades is supported by different modalities of automixis: central fusion (CF), terminal fusion (TF) and gamete duplication (GD). Recently, the complete loss of males was reported in some populations of the Kalotermitidae Glyptotermes nakajimai , in which the mode of thelytoky, either automixis or apomixis, remains to be firmly demonstrated [44]…”

Asexual Queen Succession in Termites

“…Thelytoky can occur via two principal modes: apomixis through which ploidy is maintained by mitosis and the resulting offspring are true clones of their mothers, and automixis which involves meiosis followed by ploidy restoration. In termites, apomixis was suggested in G. nakajimai (Yashiro et al 2018), while species with AQS use automixis. Furthermore, ploidy restoration under automixis occurs through different modalities among AQS species: terminal fusion in species of Reticulitermes, central fusion in Syntermitinae, and gamete duplication in Termitinae (Table 1).…”