Convergent evolution of a nutritional symbiosis in ants

Abstract

Ants are among the most successful organisms on earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have repeatedly evolved symbioses to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Cardiocondyla, Formica and Plagiolepis ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine, which is essential for insect cuticles. We also reveal that in certain multi-queen lineages, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived nutrients. Our results suggest symbioses can arise to solve common problems, but hosts may differ in their dependence on symbionts, highlighting the evolutionary forces influencing the persistence of long-term endosymbiotic mutualisms.

Evidence of phylosymbiosis inFormicaants

“…As previously reported by Jackson et al (2022), we found that Liliensternia is restricted to a single clade of Serviformica ants, while Wolbachia is present in every species screened and the majority of queens screened overall (112/131). Wolbachia is not only widely distributed among Formica species but also highly abundant, accounting for 54% of all sequences across all queens analysed.…”

“…It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted January 21, 2023. ; https://doi.org/10.1101/2023.01.20.524858 doi: bioRxiv preprint mirrored in all phylobiome trees. We expected this pattern in the full phylobiome tree, because one clade of Serviformica carries Liliensternia, a strictly vertically transmitted symbiont whose phylogeny mirrors that of its host (Jackson et al, 2022). However, even when we considered trees of the single bacterial genera Spiroplasma, Wolbachia, and Lactobacillus, the paraphyletic pattern was still apparent (Fig.…”

“…While there are a few detailed investigations of unique, vertically transmitted symbionts (e.g. Jackson et al, 2022, Klein et al, 2016, and broad comparative analyses across phylogenetically diverse host species (e.g. Sanders et al, 2017, Russell et al, 2009, ants, in general, have been understudied for microbes.…”

“…1101/2023 Studying microbiome structure across related hosts helps us disentangle the factors driving patterns observed in individual species and answer key questions, such as: whether phylogenetically related hosts evolved similar microbiomes, a signature of phylosymbiosis (Lim and Bordenstein, 2020); whether the presence of host-bound microbes is influenced by antagonistic or synergistic interactions with other microbes; or whether shared host ecologies shape the communities of microbes insects carry (Brooks et al, 2017). Formica ants are an ideal model to address these questions, as they have formed persistent associations with at least two heritable symbionts, the bacteriocyte-associated mutualist Liliensternia, and the reproductive parasite Wolbachia, as well as with gut-associated microbes such as Lactobacillus (Russell, 2012;Jackson et al, 2022;Zheng et al, 2022).…”

Evolution and ontogeny of bacteriocytes in insects

“…In lineages that contain endosymbionts, these cells become bacteriocytes whereas in other lineages they contribute to the midgut. Consistently, it has been shown that in the ant lineage within the genera Formica and Cardiocondyla, and in some lineages of beetles of subfamily Cassidinae, endosymbiosis has been repeatedly lost but the relics of the existence of bacteriocytes or bacteriocyte-like cells have been retained (Lilienstern, 1932;Jackson et al, 2021;Fukumori et al, 2022). Moreover, when endosymbionts are experimentally removed from A. pisum aphids and C. floridanus ants the bacteriocytes are still specified and migrate to the midgut epithelium (Braendle et al, 2003;Stoll et al, 2010;Rafiqi et al, 2020).…”