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.

Figure 1.

Proportions of individuals of different castes and developmental stages produced sexually and parthenogenetically in five colonies of R. virginicus based on their genotypes at eight microsatellite loci. Individuals homozygous at all loci were considered to be parthenogens, whereas those that were heterozygous at one or more loci were considered to be sexually produced. Open bars, sexually produced; filled bars, parthenogemetically produced. (a) Secondary queens; (b) workers; (c) alates.

Figure 2.

Degree of relatedness between the presumed primary queen founding a colony and the reigning king in five colonies of R. virginicus estimated from eight microsatellite loci. The genotypes of the primary queens were inferred from the genotypes of the parthenogenetically produced secondary queens within colonies. Genotypes of kings were inferred from a combination of the genotypes of their secondary queen mates and the genotypes of their worker offspring, except in colony 5, where the primary king was genotyped directly. Standard error bars were estimated by jack-knifing over loci.