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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.

SUBMITTER: Kaltenpoth M

PROVIDER: S-EPMC3264120 | biostudies-literature | 2012 Feb

REPOSITORIES: biostudies-literature

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Refining the roots of the beewolf-Streptomyces symbiosis: antennal symbionts in the rare genus Philanthinus (Hymenoptera, Crabronidae).

Kaltenpoth Martin M Yildirim Erol E Gürbüz M Faruk MF Herzner Gudrun G Strohm Erhard E

Applied and environmental microbiology 20111123 3

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 ...[more]

PMID: 22113914

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Project description:BACKGROUND: 'Candidatus Streptomyces philanthi' is a monophyletic clade of formerly uncultured bacterial symbionts in solitary digger wasps of the genera Philanthus, Philanthinus and Trachypus (Hymenoptera, Crabronidae). These bacteria grow in female-specific antennal reservoirs and - after transmission to the cocoon - produce antibiotics protecting the host larvae from fungal infection. However, the symbionts' refractoriness to cultivation has thus far hampered detailed in vitro studies on their physiology and on the evolutionary changes in metabolic versatility in response to the host environment. RESULTS: Here we isolated in axenic culture 22 'Streptomyces philanthi' biovars from different host species. Sequencing of gyrB revealed no heterogeneity among isolates within host individuals, suggesting low levels of (micro)diversity or even clonality of the symbionts in individual beewolf antennae. Surprisingly, however, isolates from different host species differed strongly in their physiology. All biovars from the Eurasian/African Philanthus and the South American Trachypus host species had high nutritional demands and were susceptible to most antibiotics tested, suggesting a tight association with the hosts. By contrast, biovars isolated from the genus Philanthinus and the monophyletic North American Philanthus clade were metabolically versatile and showed broad antibiotic resistance. Concordantly, recent horizontal symbiont transfer events - reflected in different symbiont strains infecting the same host species - have been described only among North American Philanthus species, altogether indicative of facultative symbionts potentially capable of a free-living lifestyle. Phylogenetic analyses reveal a strong correlation between symbiont metabolic versatility and host phylogeny, suggesting that the host environment differentially affects the symbionts' evolutionary fate. Although opportunistic bacteria were occasionally isolated from the antennae of different host species, only filamentous Actinobacteria (genera Streptomyces, Amycolatopsis and Nocardia) could replace 'S. philanthi' in the antennal gland reservoirs. CONCLUSION: Our results indicate that closely related bacteria from a monophyletic clade of symbionts can experience very different evolutionary trajectories in response to the symbiotic lifestyle, which is reflected in different degrees of metabolic versatility and host-dependency. We propose that the host-provided environment could be an important factor in shaping the degenerative metabolic evolution in the symbionts and deciding whether they evolve into obligate symbionts or remain facultative and capable of a host-independent lifestyle.

Project description:BackgroundSexual selection is thought to promote evolutionary changes and diversification. However, the impact of sexual selection in relation to other selective forces is difficult to evaluate. Male digger wasps of the tribe Philanthini (Hymenoptera, Philanthinae) scent mark territories to attract receptive females. Consequently, the organs for production and storage of the marking secretion, the mandibular gland (MG) and the postpharyngeal gland (PPG), are subject to sexual selection. In female Philanthini, these glands are most likely solely subject to natural selection and show very little morphological diversity. According to the hypothesis that sexual selection drives interspecific diversity, we predicted that the MG and PPG show higher interspecific variation in males than in females. Using histological methods, 3D-reconstructions, and multivariate statistical analysis of morphological characters, we conducted a comparative analysis of the MG and the PPG in males of 30 species of Philanthini and three species of the Cercerini and Aphilanthopsini, two related tribes within the Philanthinae.ResultsWe found substantial interspecific diversity in gland morphology with regard to gland incidence, size, shape and the type of associated secretory cells. Overall there was a phylogenetic trend: Ensuing from the large MGs and small PPGs of male Cercerini and Aphilanthopsini, the size and complexity of the MG was reduced in male Philanthini, while their PPG became considerably enlarged, substantially more complex, and associated with an apparently novel type of secretory cells. In some clades of the Philanthini the MG was even lost and entirely replaced by the PPG. However, several species showed reversals of and exceptions from this trend. Head gland morphology was significantly more diverse among male than among female Philanthinae.ConclusionOur results show considerable variation in male head glands including the loss of an entire gland system and the evolution of a novel kind of secretory cells, confirming the prediction that interspecific diversity in head gland morphology is higher in male than in female Philanthini. We discuss possible causes for the remarkable evolutionary changes in males and we conclude that this high diversity has been caused by sexual selection.

Dataset Information

Refining the roots of the beewolf-Streptomyces symbiosis: antennal symbionts in the rare genus Philanthinus (Hymenoptera, Crabronidae).

Publications

Refining the roots of the beewolf-Streptomyces symbiosis: antennal symbionts in the rare genus Philanthinus (Hymenoptera, Crabronidae).

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