Inherited bacteria have come to be recognised as important components of arthropod biology. In addition to mutualistic symbioses, a range of other inherited bacteria are known to act either as reproductive parasites or as secondary symbionts. Whilst the incidence of the α-proteobacterium Wolbachia is relatively well established, the current knowledge of other inherited bacteria is much weaker. Here, we tested 136 arthropod species for a range of inherited bacteria known to demonstrate reproductive parasitism, sampling each species more intensively than in past surveys.

Rickettsia-like maternally inherited bacteria have been shown to be involved in a variety of alterations of arthropod sexuality, such as female-biased sex ratios, parthenogenesis, and sterility of crosses either between infected males and uninfected females or between infected individuals (cytoplasmic incompatibility). We have characterized several of these microorganisms through partial sequences of the small (16S) and large (23S) subunit ribosomal DNA. All the symbionts identified, which include several cytoplasmic incompatibility microorganisms, several endosymbionts of terrestrial isopods, and symbionts of two thelytokous Trichogramma wasp species, belong to a monophyletic group of related symbionts, some of which have previously been detected in several insects exhibiting cytoplasmic incompatibility. Three molecular lineages can be identified on the basis of 16S as well as 23S sequences. Although they are only known as endocellular symbionts, Wolbachia spread by horizontal transfer across host lineages as evidenced by their diversification which occurred long after that of their hosts, and by the non-congruence of the phylogenetic relationships of symbionts and their hosts. Indeed, symbionts of two different lineages have been found in the same host species, whereas closely related endosymbionts are found in distinct insect orders. Isopod endosymbionts form a separate lineage, and they can determine feminization as well as cytoplasmic incompatibility. The ability to determine cytoplasmic incompatibility, found in all lineages, is probably ancestral to this group.

Wolbachia are maternally inherited, intracellular, alpha proteobacteria that infect a wide range of arthropods. They cause three kinds of reproductive alterations in their hosts: cytoplasmic incompatibility, parthenogenesis and feminization. There have been many studies of the distribution of Wolbachia in arthropods, but very few crustacean species are known to be infected. We investigated the prevalence of Wolbachia in 85 species from five crustacean orders. Twenty–two isopod species were found to carry these bacteria. The bacteria were found mainly in terrestrial species suggesting that Wolbachia came from a continental environment. The evolutionary relationships between these Wolbachia strains were determined by sequencing bacterial genes and by interspecific transfers. All the bacteria associated with isopods belonged to the wolbachiae B group, based on 16S rDNA sequence data. All the terrestrial isopod symbionts in this group except one formed an independent clade. The results of interspecific transfers show evidence of specialization of Wolbachia symbionts to their isopod hosts. They also suggest that host species plays a more important role than bacterial phylogeny in determining the phenotype induced by Wolbachia infection.

Vertical transmission (VT) and associated manipulation of host reproduction are widely reported among prokaryotic endosymbionts. Here, we present evidence for widespread use of VT and associated sex–ratio distortion in a eukaryotic phylum. The Microspora are an unusual and diverse group of eukaryotic parasites that infect all animal phyla. Following our initial description of a microsporidian that feminizes its crustacean host, we survey the diversity and distribution of VT within the Microspora. We find that vertically transmitted microsporidia are ubiquitous in the amphipod hosts sampled and that they are also diverse, with 11 species of microsporidia detected within 16 host species. We found that infections were more common in females than males, suggesting that host sex–ratio distortion occurs in five out of eight parasite species tested. Phylogenetic reconstruction demonstrates that VT occurs in all major lineages of the phylum Microspora and that sex–ratio distorters are found on multiple branches of the phylogenetic tree. We propose that VT is either an ancestral trait or evolves with peculiar frequency in this phylum. If the association observed here between VT and host sex–ratio distortion holds true across other host taxa, these eukaryotic parasites may join the bacterial endosymbionts in their importance as sex–ratio distorters.

Thirty-five percent of isopods are estimated to be infected by Wolbachia, an intracellular maternally inherited α-Proteobacterium. Previous studies have indicated that horizontal transfer of Wolbachia strains may occur, although the mechanisms are unclear. The wsp gene was sequenced from 17 Wolbachia strains harboured by crustacean host species and three from their associated predators and parasites. Two major clades of Wolbachia were found in crustacean, with relatives also found in insects, the other restricted to crustaceans. Highly divergent Wolbachia strains were found in a woodlouse-eating spider and its prey, suggesting no intertaxon bacterial exchange via the predator–prey route. The phylogenetic proximity of Wolbachia from parasitoid flies or phoretic mites to those from isopods suggests that horizontal symbiont transmission may have occurred between those taxa. Two distant Wolbachia strains were detected in two intertidal amphipods; these strains were closely related to different coastal isopod symbionts, suggesting Wolbachia transmission may occur between distantly related crustacean hosts living under the same ecological conditions.