Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus

Abstract

Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so-called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2 years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3 years. We conclude that S. minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.

A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate

“…Hence, our model matches well with the reproductive systems of a broad range of termite species. Note that recent studies identified three AQS species in higher termites(Termitidae), which arephylogeneticallydistant from the lower termite genus Reticulitermes (Fougeyrollas et al 2015(Fougeyrollas et al , 2017Fournier et al 2016). The termitid species with AQS exhibit different mechanisms of parthenogenesis: Cavitermes tuberosus uses automixis with terminal fusion (Fournier et al 2016), resulting in homozygous female parthenogens as in Reticulitermes, whereas Embiratermes neotenicus and Silvestritermes minutus use automixis with central fusion, resulting in heterozygous parthenogens (Fougeyrollas et al 2015(Fougeyrollas et al , 2017.…”

“…Note that recent studies identified three AQS species in higher termites(Termitidae), which arephylogeneticallydistant from the lower termite genus Reticulitermes (Fougeyrollas et al 2015(Fougeyrollas et al , 2017Fournier et al 2016). The termitid species with AQS exhibit different mechanisms of parthenogenesis: Cavitermes tuberosus uses automixis with terminal fusion (Fournier et al 2016), resulting in homozygous female parthenogens as in Reticulitermes, whereas Embiratermes neotenicus and Silvestritermes minutus use automixis with central fusion, resulting in heterozygous parthenogens (Fougeyrollas et al 2015(Fougeyrollas et al , 2017. Although there is no genetic difference between the founder queen, which is derived from an alate, and her parthenogenetic daughters in the latter species, the parthenogenetic daughters (carrying only maternal chromosomes) also have a higher propensity to develop into neotenic queens than sexually produced daughters (carrying paternal and maternal chromosomes).…”

Bacteriome-associatedWolbachiaof the parthenogenetic termiteCavitermes tuberosus

“…We also screened for the presence of the three endosymbionts in all other reported cases of facultative parthenogenesis in the Neotropics: Embiratermes neotenicus and Silvestritermes minutus (Termitidae: Syntermitinae), both restoring ploidy through central fusion (Fougeyrollas et al 2015;Fougeyrollas et al 2017) (heads and gonads of 25 neotenic queens distributed in five nests).…”

Secondary queens in the parthenogenetic termite Cavitermes tuberosus develop through a transitional helper stage

“…Developmental origin of neotenic parthenogens in C. tuberosus differs from that observed in the two AQS species recently identified in the higher termite subfamily Syntermitinae, that is, Embiratermes neotenicus (Fougeyrollas et al ) and Silvestritermes minutus (Fougeyrollas et al ). In both species, the neotenics differentiate from parthenogenetically produced nymphs of the fourth stage.…”

“…This replacement supposedly enhances the reproductive capacity of the colony (Matsuura, ). First reported from Reticulitermes species (Luchetti, Velonà, Mueller, & Mantovani, ; Matsuura et al, ; Vargo, Labadie, & Matsuura, ), AQS was recently demonstrated in several Termitidae (Fougeyrollas et al, , ; Fournier, Hellemans, Hanus, & Roisin, ; Hellemans, Bourguignon, Kyjaková, Hanus, & Roisin, ). Observations on all these species suggest that the caste fate of asexually produced females is determined by their parthenogenetic origin since most parthenogens develop into neotenic queens and only a small portion into other castes (Matsuura, ).…”