Abstract
BackgroundBacterial endosymbiosis has a recurring significance in the evolution of insects. An estimated 10-20% of insect species depend on bacterial associates for their nutrition and reproductive viability. Members of the ant tribe Camponotini, the focus of this study, possess a stable, intracellular bacterial mutualist. The bacterium, Blochmannia, was first discovered in Camponotus and has since been documented in a distinct subgenus of Camponotus, Colobopsis, and in the related genus Polyrhachis. However, the distribution of Blochmannia throughout the Camponotini remains in question. Documenting the true host range of this bacterial mutualist is an important first step toward understanding the various ecological contexts in which it has evolved, and toward identifying its closest bacterial relatives. In this study, we performed a molecular screen, based on PCR amplification of 16S rDNA, to identify bacterial associates of diverse Camponotini species.ResultsPhylogenetic analyses of 16S rDNA gave four important insights: (i) Blochmannia occurs in a broad range of Camponotini genera including Calomyrmex, Echinopla, and Opisthopsis, and did not occur in outgroups related to this tribe (e.g., Notostigma). This suggests that the mutualism originated in the ancestor of the tribe Camponotini. (ii) The known bacteriocyte-associated symbionts of ants, in Formica, Plagiolepis, and the Camponotini, arose independently. (iii) Blochmannia is nestled within a diverse clade of endosymbionts of sap-feeding hemipteran insects, such as mealybugs, aphids, and psyllids. In our analyses, a group of secondary symbionts of mealybugs are the closest relatives of Blochmannia. (iv) Blochmannia has cospeciated with its known hosts, although deep divergences at the genus level remain uncertain.ConclusionsThe Blochmannia mutualism occurs in Calomyrmex, Echinopla, and Opisthopsis, in addition to Camponotus, and probably originated in the ancestral lineage leading to the Camponotini. This significant expansion of its known host range implies that the mutualism is more ancient and ecologically diverse than previously documented. Blochmannia is most closely related to endosymbionts of sap-feeding hemipterans, which ants tend for their carbohydrate-rich honeydew. Based on phylogenetic results, we propose Camponotini might have originally acquired this bacterial mutualist through a nutritional symbiosis with other insects.
Highlights
Bacterial endosymbiosis has a recurring significance in the evolution of insects
Our results indicate that Blochmannia is more widespread within the tribe than previously documented and strongly suggest a single, ancient origin for this endosymbiosis
All 16S rDNA sequences from the Camponotini isolates proved to be a close match to known Blochmannia strains, as detailed in the database comparisons and phylogenetic analyses below
Summary
Bacterial endosymbiosis has a recurring significance in the evolution of insects. An estimated 1020% of insect species depend on bacterial associates for their nutrition and reproductive viability. An estimated 10-20% of insect species, in several taxonomic orders, depend on intracellular bacterial mutualists for their viability and reproduction [1]. These obligate associates, called 'primary' (P-) endosymbionts because they are required for host survival and fecundity, often synthesize key nutrients that are lacking in the hosts' unbalanced diet (e.g., plant sap or vertebrate blood) [2,3,4]. The bacteria live within specialized host cells called bacteriocytes and undergo maternal transmission to developing eggs or embryos Consistent with this stable transmission through host lineages, the phylogenies of Pendosymbionts match those of their insect hosts (e.g., [59]). This phylogenetic congruence points to host-symbiont cospeciation, which can be traced back to a single, often ancient, infection event in each host group
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