A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review

Abstract

Maternally transmitted bacteria have been important players in the evolution of insects and other arthropods, affecting their nutrition, defense, development, and reproduction. Wolbachia are the best studied among these and typically the most prevalent. While several other bacteria have independently evolved a heritable lifestyle, less is known about their host ranges. Moreover, most groups of insects have not had their heritable microflora systematically surveyed across a broad range of their taxonomic diversity. To help remedy these shortcomings we used diagnostic PCR to screen for five groups of heritable symbionts—Arsenophonus spp., Cardinium hertigii, Hamiltonella defensa, Spiroplasma spp., and Wolbachia spp.—across the ants and lepidopterans (focusing, in the latter case, on two butterfly families—the Lycaenidae and Nymphalidae). We did not detect Cardinium or Hamiltonella in any host. Wolbachia were the most widespread, while Spiroplasma (ants and lepidopterans) and Arsenophonus (ants only) were present at low levels. Co-infections with different Wolbachia strains appeared especially common in ants and less so in lepidopterans. While no additional facultative heritable symbionts were found among ants using universal bacterial primers, microbes related to heritable enteric bacteria were detected in several hosts. In summary, our findings show that Wolbachia are the dominant heritable symbionts of ants and at least some lepidopterans. However, a systematic review of symbiont frequencies across host taxa revealed that this is not always the case across other arthropods. Furthermore, comparisons of symbiont frequencies revealed that the prevalence of Wolbachia and other heritable symbionts varies substantially across lower-level arthropod taxa. We discuss the correlates, potential causes, and implications of these patterns, providing hypotheses on host attributes that may shape the distributions of these influential bacteria.

Insect Gut Bacterial Diversity Determined by Environmental Habitat, Diet, Developmental Stage, and Phylogeny of Host

“…3b), in accordance with a statistical analysis reported by Hilgenboecker et al (54). Despite several reports about the distribution of intracellular symbionts that regulate host reproduction, such as Wolbachia, Spiroplasma, and "Candidatus Cardinium" (53)(54)(55)(56)(58)(59)(60), there are few studies addressing the broad distribution of hostspecific bacteria from a wide range of insect hosts.…”

Novel Rickettsiella Bacterium in the Leafhopper Orosius albicinctus (Hemiptera: Cicadellidae)

“…Both the DGGE and pyrosequencing screens also identified Arsenophonus as an abundant symbiont in O. albicinctus. Arsenophonus, a very common facultative inherited symbiont of terrestrial arthropods, was found to infect ϳ4% of arthropod species in a recent large screening study of 136 species in 15 orders (3); Hemiptera, including leafhoppers, are commonly infected (3,40).…”

The incidence of bacterial endosymbionts in terrestrial arthropods

“…Several authors have suggested that symbiont infection frequency might vary predictably with host biology [1,3,6,7,[9][10][11][12][13][14][15][16]. For example, two distinct arguments predict that symbionts should be more common in host taxa that are species rich.…”