Asexual queen succession in the subterranean termite Reticulitermes virginicus

Abstract

Termite colonies are founded by a pair of primary reproductives. In many species, including subterranean termites (family Rhinotermitidae), the primary king and queen can be succeeded by neotenic reproductives that are produced from workers or nymphs within the colony. It is generally believed that these neotenics inbreed within the colony, sometimes for many generations. Here, we show that primary queens of the North American subterranean termite, Reticulitermes virginicus, are replaced by numerous parthenogenetically produced female neotenics. We collected functional female neotenics from five colonies of R. virginicus in North Carolina and Texas, USA. Genetic analysis at eight microsatellite loci showed that 91 -100% of the neotenics present within a colony were homozygous at all loci, indicating that they were produced through automictic parthenogenesis with terminal fusion. In contrast, workers, soldiers and alates were almost exclusively sexually produced by mating between the female neotenics and a single king. This is the second termite species shown to undergo asexual queen succession, a system first described in the Japanese species, Reticulitermes speratus. Thus, the conditional use of sexual and asexual reproduction to produce members of different castes may be widespread within Reticulitermes and possibly other subterranean termites.

Sex ratio biases in termites provide evidence for kin selection

“…In contrast, previous studies indicate that R. virginicus appears to experience king replacement in an earlier stage of colony establishment, so that 40% of colonies are estimated to have a primary king and 60% a secondary king 20 . We can therefore make the following two predictions concerning the sex allocation in Reticulitermes species: sex allocation in species with AQS will be significantly female biased, whereas sex allocation in species without AQS will not be biased; sex allocation in R. virginicus should be more female biased than in R. speratus.…”

“…On the other hand, primary kings live much longer than primary queens. This AQS system enables founding queens to increase their reproductive output while retaining the same transmission rate of their genes to future generations 19,20,23 (Fig. 3b).…”

“…Recently, a novel breeding system called AQS has been described in two species of subterranean termites-Reticulitermes speratus 19 and Reticulitermes virginicus 20 -that meet all three of these conditions. Termite colonies are typically founded by a monogamous pair of primary reproductives (adult winged forms), one king and one queen.…”

“…In the subterranean termites R. speratus and R. virginicus, queens produce their neotenic replacement reproductives asexually but use normal sexual reproduction to produce other colony members 19,20 . These species undergo typical colony founding by a pair of primary reproductives.…”

Termite queens close the sperm gates of eggs to switch from sexual to asexual reproduction

“…S1) (18,19). In AQS species, queens produce their neotenic replacement queens asexually but use normal sexual reproduction to produce other colony members (14)(15)(16). Because sex determination in Reticulitermes termites is male heterogamy (20), queens cannot produce secondary kings by parthenogenesis (17).…”