Sex ratio variations among years and breeding systems in a facultatively parthenogenetic termite

Abstract

Some species of termites evolved an outstanding reproductive strategy called asexual queen succession (AQS), in which the primary queen is replaced by multiple parthenogenetically produced daughters (neotenics) that mate with the primary king. When the primary king is eventually replaced, this time by sexually produced neotenic king(s), sex-asymmetric inbreeding occurs and the queen's genome is more transmitted than that of the king, thereby increasing the reproductive value of female dispersers, and female-biased population sex ratio is expected. Yet, the life cycle, the breeding system dynamics and AQS modalities differ between AQS species, thereby modifying the relative genetic contribution of primary reproductives in the colony and thus also the equilibrium sex ratio. We estimated colonial and population sex ratio over two consecutive dispersal periods in a French Guiana population of Cavitermes tuberosus (Termitinae) in which the founding queen may be replaced only after colony maturity, some neotenic females may be sexually produced, and some female dispersers arise through parthenogenesis. Colonial sex ratio varied among colonies: primary-headed nests with higher within-nest relatedness produced more females than neotenic-headed nests with lower relatedness among individuals. Over the two dispersal periods, the population investment sex ratio fluctuated around 1:1, thereby confirming that AQS breeding system is not necessarily linked with female-biased sex ratio. The balanced alate sex ratio, combined with the occurrence of sexually produced neotenic queens, is possibly the outcome of a queen-king conflict between the primary reproductives.

Asexual Queen Succession in Termites

“…Accordingly, species of the genus Reticulitermes without AQS exhibit a balanced sex ratio, while it is female-biased in species with AQS (Kobayashi et al 2013;Luchetti et al 2013). This is, however, not the case in AQS species from the Termitidae, whose sex ratio is balanced (Fougeyrollas et al 2017;Hellemans et al 2019b). Interestingly, the differentiation of parthenogens into neotenic queens is not perfectly hardwired in all species with AQS.…”

“…the proportion of generations during which mother-son or father-daughter inbreeding occurs relative to those in which both genomes are equally transmitted to the dispersers. In C. tuberosus, queen replacement seems to be facultative and take place after colony maturity, thus at a late stage in the life cycle of the colony compared to other species with AQS (Hellemans et al 2019b). It follows that the life expectancy of colonies may be short after queen replacement, and even shorter after queen and king replacement, so that the proportion of generations with dispersers arising from mother-son inbreeding might be low.…”

“…Conversely, some female dispersers may also be produced asexually and become successful foundresses, thereby raising the contribution of the founding queen to the next generation. Furthermore, it is hypothesized that conflict over reproduction and sex ratio may arise between parthenogenetically and sexually-produced neotenic queens as the former ones are less related to the offspring of the latter ones (Hellemans et al 2019b).…”

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)

“…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. While in the syntermitines E. neotenicus and S. minutus , the queen replacement is an obligatory event preceding the colony maturation and production of dispersers [10, 11], the primary queens of C. tuberosus are often replaced only after the colony reaches maturity and already produces dispersing reproductives [13, 18]. Therefore, the total incidence of the harem breeding structure is lower in C. tuberosus (44% of mature colonies) and the presence of AQS can be viewed as a tool to extend the colony’s reproductive potential and lifespan beyond those of the foundress in late stages of colony existence [13].…”