Refining the Roots of the Beewolf-Streptomyces Symbiosis: Antennal Symbionts in the Rare Genus Philanthinus (Hymenoptera, Crabronidae)

Abstract

Insects engage in symbiotic associations with a large diversity of beneficial microorganisms. While the majority of well-studied symbioses have a nutritional basis, several cases are known in which bacteria protect their host from pathogen infestation. Solitary wasps of the genera Philanthus and Trachypus (beewolves; Hymenoptera, Crabronidae) cultivate the actinomycete "Candidatus Streptomyces philanthi" in specialized antennal gland reservoirs. The symbionts are transferred to the larval cocoon, where they provide protection against pathogenic fungi by producing at least nine different antibiotics. Here we investigated the closest relatives of Philanthus and Trachypus, the rare genus Philanthinus, for the presence of antennal gland reservoirs and symbiotic streptomycetes. Molecular analyses identified "Ca. Streptomyces philanthi" in reservoirs of Philanthinus quattuordecimpunctatus. Phylogenies based on the 16S rRNA gene suggest that P. quattuordecimpunctatus may have acquired "Ca. Streptomyces philanthi" by horizontal transfer from other beewolf species. In histological sections and three-dimensional reconstructions, the antennal gland reservoirs were found to occupy six antennal segments (as opposed to only five in Philanthus and Trachypus) and to be structurally less complex than those of the evolutionarily more derived genera of beewolves. The presence of "Ca. Streptomyces philanthi" in antennal glands of Philanthinus indicates that the symbiosis between beewolves and Streptomyces bacteria is much older than previously thought. It probably evolved along the branch leading to the monophyletic tribe Philanthini, as it seems to be confined to the genera Philanthus, Trachypus, and Philanthinus, which together comprise 172 described species of solitary wasps.

Multiorganismal Insects: Diversity and Function of Resident Microorganisms

“…For example, solitary digger wasps of the tribe Philanthini retain Streptomyces spp. in cuticle-lined glandular reservoirs, in each of 5–6 antennal segments (61) (Figure 1a); and attine ants house actinobacteria of the genus Pseudonocardia in similar glandular invaginations, known as crypts or foveae, on the thorax, legs, or other locations of the body, varying with ant species (26). …”

Biogeography of a defensive symbiosis

“…Female beewolves cultivate symbiotic bacteria in specialized gland reservoirs in the antennae and secrete them into the brood cells prior to oviposition. [11][12][13][14] The larvae later transfer the symbionts to the cocoon silk, 15 where they provide protection during subsequent development-which is often not completed until the following year 16-18 -by producing a mixture of at least 9 different antimicrobial substances. 19 Recent phylogenetic analyses indicated that the symbionts are descendants of soil-dwelling streptomycetes that were acquired by the insects at least 68 million years ago (Fig.…”

A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior

“…To localize Westeberhardia, we performed fluorescence in situ hybridization (FISH) as described previously (Kaltenpoth et al, 2012(Kaltenpoth et al, , 2014 and Supplementary Information) on abdominal sections of queen, worker and wingless male pupae from BR (Ilhéus, 2009) and adult queens from BR (Ilhéus, 2009) and JP (OypB) with the general eubacterial probe EUB338 (5′-GCTGCCTCCCGTAGGAGT-3′) (Amann et al, 1990) and one of the Westeberhardiaspecific probes Wcard1 (5′-ATCAGTTTCGAACG CCATTC-3′) and Wcard2 (5′-CGGAAGCCACAATT Based on a diagnostic PCR screen using the nrdB gene.…”