The incidence of bacterial endosymbionts in terrestrial arthropods

Abstract

Intracellular endosymbiotic bacteria are found in many terrestrial arthropods and have a profound influence on host biology. A basic question about these symbionts is why they infect the hosts that they do, but estimating symbiont incidence (the proportion of potential host species that are actually infected) is complicated by dynamic or low prevalence infections. We develop a maximum-likelihood approach to estimating incidence, and testing hypotheses about its variation. We apply our method to a database of screens for bacterial symbionts, containing more than 3600 distinct arthropod species and more than 150 000 individual arthropods. After accounting for sampling bias, we estimate that 52% (CIs: 48-57) of arthropod species are infected with Wolbachia, 24% (CIs: 20-42) with Rickettsia and 13% (CIs: 13-55) with Cardinium. We then show that these differences stem from the significantly reduced incidence of Rickettsia and Cardinium in most hexapod orders, which might be explained by evolutionary differences in the arthropod immune response. Finally, we test the prediction that symbiont incidence should be higher in speciose host clades. But while some groups do show a trend for more infection in species-rich families, the correlations are generally weak and inconsistent. These results argue against a major role for parasitic symbionts in driving arthropod diversification.

Keywords: Cardinium; Rickettsia; Wolbachia; infection; maximum likelihood.

Figure 1.

Estimates of symbiont incidence, x_0.001 (i.e. the proportion of species infected at a prevalence of greater than 1/1000) in terrestrial arthropods. Estimates obtained from (a) fitting a beta distribution to the complete database; (b) fitting a doubly inflated beta distribution to the complete database, and so allowing for completely uninfected or completely infected species; (c) standardized sampling (i.e. a weighted sum of estimates from the largest arthropod taxa, using the single largest population sample from each sampled species).

Figure 2.

Estimates of symbiont incidence, x_0.001 (i.e. the proportion of species infected at a prevalence of greater than 1/1000) in the two major subphyla of Arthropoda. Each pair of bars shows the incidence of a different bacterial genus, and compares estimates for Hexapoda (left-hand bar) and Chelicerata (right-hand bar). Estimates used ‘standardized sampling’ (see main text). P-values above each set of bars are from a likelihood ratio test of heterogeneity in the estimates.

Figure 3.

Estimates of symbiont incidence, x_0.001 (i.e. the proportion of species infected at a prevalence of greater than 1/1000) for three genera of bacterial endosymbionts, across orders (and some superordinal groups) of terrestrial arthropods. Grey points show estimates from our complete database, and black points show estimates with standardized sampling, in which all sampled species were represented by the single largest population sample. Shading and vertical lines demarcate some major host groups, including Hexapoda (left-hand panel) and Chelicerata (right-hand panel).