The distribution of Wolbachia in Cubitermes (Termitidae, Termitinae) castes and colonies: a modelling approach

Abstract

Wolbachia are endosymbiotic bacteria of arthropods and nematodes that are able to manipulate host reproduction. Although vertically transmitted via the cytoplasm in eggs, horizontal transmission of Wolbachia among and within arthropod species has been shown to be common. Eusocial insects represent interesting models for studying Wolbachia transmission due to colonial organization and close interaction between nestmates. Here we conducted a detailed screening of Wolbachia infection for 15 colonies of the very common soil-feeding termites Cubitermes spp. affinis subarquatus (Termitidae, Termitinae) that consist of four distinct phylogenetic species in the Lopé forest Reserve, Gabon. Infection tests showed that 50% of the individuals were Wolbachia positive (N = 555) with 90% of reproductives and 48% of offspring infected. White soldiers, which are transitional stages preceding mature soldiers, had a significantly higher mean infection rate (74%) than the other castes and stages (63%, 33% and 39% for larvae, workers and mature soldiers, respectively). We used a maximum likelihood method and Akaike's Information Criterion in order to explain the non-expected high rate of Wolbachia infection in white soldiers. The best model included a species effect for the stochastic loss of Wolbachia and a caste effect for the rate of gain. After fitting, the best model selected was for a species-specific rate of loss with a null rate of new gain for larvae, workers and soldiers and a probability of 0.72 whatever the species, that a white soldier becomes newly contaminated during that stage. The mean expected infection rate in white soldiers without a new gain was estimated to 17% instead of the 74% observed. Here we discuss the possible explanations to the high infection rate observed in white soldiers.

Fig 1. a) Development of non-sexual lines in the genus Cubitermes synthetized from various reports about Cubitermes species life cycle [,–81]. Larval stages comprise males and females, which both differentiate into a single stage of male and female workers (Worker stage I). A subset of the female workers further differentiates into pre-soldiers (i.e. white soldiers, transitional stage preceding mature soldiers), b) Left: fitted parameters for the selected model: probability of stochastic loss of Wolbachia between two stages according to the species and right: probability of gain of Wolbachia during stages. c) Observed (bold lines) and expected under the model (dotted lines) infection rates for the four species Cubitermes sp. A, B, C and D and stages/castes.