One nutritional symbiosis begat another: Phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects

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.

The Phylogeny and Evolution of Ants

“…The subfamily Dolichoderinae, for example, has 706 described species (AntCat 2014) and many others as yet undescribed, compared with its sister group, the subfamily Aneuretinae, with one extant species; the tribe Camponotini contains 1,840 described species, against its putative sister group, Myrmoteras, with 39 species. Such examples abound and although it is often possible to identify potential causes, such as enhanced chemical defenses in Dolichoderinae (Blum & Hermann 1978) and obligate intracellular symbionts in Camponotini (Wernegreen et al 2009), these ad hoc explanations are difficult to test if the putative cause is evolutionarily unique (Nunn 2011). The success of ants as a whole is often attributed to the development in many ant taxa of close associations with trophobionts: plant-feeding, honeydew-producing insects, primarily Hemiptera (Delabie 2001, Wilson & Hölldobler 2005.…”

A revised phylogenetic classification of the ant subfamily Formicinae (Hymenoptera: Formicidae), with resurrection of the genera Colobopsis and Dinomyrmex

“…Overbeckia, not sequenced in this study, is likely a junior synonym of Camponotus (Bolton 2003). All members of this tribe have a unique, vertically inherited bacterial symbiont, Blochmannia, whose evolutionary history mirrors that of the ants (Wernegreen et al 2009). Morphologically the workers of Camponotini can be recognized by the combination of distinctive mandibular dentition (5-8 teeth, with the third tooth from apex not reduced in size), antennal insertions well separated from the posterior clypeal margin, and twelve antennal segments (Bolton 1994(Bolton , 2003.…”

Effects of B Vitamin Deletion in Chemically Defined Diets on Brood Development in Camponotus vicinus (Hymenoptera: Formicidae)

“…Most of the recent work on carpenter ant nutrition has focused on the nutritional enhancement provided by the bacterial intracellular gut endosymbiont Blochmannia , de Souza et al 2009, Wernegreen et al 2009, Stoll et al 2010. The presence of Blochmannia enhanced larval development and colony immune response to parasitoids in carpenter ants fed artiÞcial diets with or without antibiotics Feldhaar 2007, de Souza et al 2009).…”

“…Most recent work relating to microorganisms and their role in the nutrition of carpenter ants has focused on midgut intracellular bacterial endosymbionts of the genus Blochmannia found in members of the ant tribe Camponotini (Sauer et al 2002, Zientz et al 2005, Cook and Davidson 2006, de Souza et al 2009, Wernegreen et al 2009, Stoll et al 2010. Blochmannia have been shown to contribute to nutritional upgrading, enhance brood development, and may increase ant immune response against parasitoids.…”