Convergent evolution of a labile 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 evolved symbioses repeatedly to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Plagiolepis, Formica and Cardiocondyla ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine. We also show that in certain multi-queen lineages that have co-diversified with their symbiont for millions of years, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived resources. Our results imply that 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.

Blochmanniaendosymbionts reduce brood rearing success in a carpenter ant (Camponotussp.)

“…The cross-fostering experiments confirmed that Blochmannia is relevant for brood development, since brood with reduced Blochmannia titers had a higher egg mortality and slower development rate than brood containing endosymbionts (e.g. (1,16,30)) In particular, these endosymbionts selectively regulate germline genes in early development stages of their hosts to successfully integrate Blochmannia into the Camponotini ants and facilitate the horizontal transfer and biosynthesis pathways (19,24,32). By contrast, the frequency of Blochmannia decreases in older workers and the endosymbionts seem to play a minor role for adult ants (30).…”

“…(i) Blochmannia provides access to nutrients necessary for host development (22)(23)(24), while the ants bacteriocytes provide their endosymbionts with a protected environment (16,(26)(27)(28).…”

“…The Blochmannia genome contains genes for biosynthesis pathways for essential amino acids (except arginine) necessary for the host's development, especially for sclerotization, recycling of ammonia, and sulfate reduction (22)(23)(24). In contrast, biosynthesis pathways for non-essential amino acids have been lost (20,(23)(24)(25).…”

Maternal control over caste allocation in the ant Cardiocondyla obscurior

“…Westeberhardia cardiocondylae, an endosymbiont with a highly reduced genome that resides in gut-associated bacteriomes, as well as in ovaries in queens [34]. Cardiocondyla minutior carries the symbiont [35] but does not display caste-specific patterns, while a C. obscurior lineage that is naturally free of Cand . Westeberhardia [34,36] and has been maintained in the lab since 2011 shows the patterns (Schultner, pers.…”

Evolution and ontogeny of bacteriocytes in insects

“…In addition, methylation mediated by endosymbiont has been shown as a regulator of the expression of key host genes in bacteriocytes, which affect aphid hosts' selection of plants for feeding (Kim et al, 2018). Some specific examples of amino acid complementation include i) The aphid host which may play a role in biosynthesizing and thus regulating ornithine for Buchnera, whereas many Buchnera taxa have lost the genes responsible for ornithine biosynthesis (Hansen and Moran, 2014), ii) The case of B. tabaci populations from Asia, where several endosymbiont genomes sampled have lost major components of the vitamin B biosynthesis pathways, and presumably, the host supplements these to the endosymbiont (Zhu et al, 2022), iii) A recent study proving that the only metabolic function consistently retained in symbiont genomes of ants that have cellular endosymbionts, namely Camponotus, Plagiolepis, Formica, and Cardiocondyla, is the capacity to synthesise tyrosine implying that they supplement the host amino acid deficiency (Jackson et al, 2022).…”