Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis

Many insects rely on symbiotic microbes for survival, growth, or reproduction. Over evolutionary timescales, the association with intracellular symbionts is stabilized by partner fidelity through strictly vertical symbiont transmission, resulting in congruent host and symbiont phylogenies. However,...

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Published in:Proceedings of the National Academy of Sciences - PNAS 2014-04, Vol.111 (17), p.6359-6364
Main Authors: Kaltenpoth, Martin, Roeser-Mueller, Kerstin, Koehler, Sabrina, Peterson, Ashley, Nechitaylo, Taras Y., Stubblefield, J. William, Herzner, Gudrun, Seger, Jon, Strohm, Erhard
Format: Article
Language:English
Subjects:
Animals
Bacteria
Biological Evolution
Biological Sciences
Biological taxonomies
Brood cells
Cocoons
Female
Female animals
Fungi
Hymenoptera
Insects
Maxillary glands
Microorganisms
Philanthus
Phylogenetics
Phylogeny
Predation
Streptomyces
Streptomyces - physiology
Symbionts
Symbiosis
Symbiosis - physiology
Time Factors
Wasps - microbiology
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Summary:Many insects rely on symbiotic microbes for survival, growth, or reproduction. Over evolutionary timescales, the association with intracellular symbionts is stabilized by partner fidelity through strictly vertical symbiont transmission, resulting in congruent host and symbiont phylogenies. However, little is known about how symbioses with extracellular symbionts, representing the majority of insect-associated microorganisms, evolve and remain stable despite opportunities for horizontal exchange and de novo acquisition of symbionts from the environment. Here we demonstrate that host control over symbiont transmission (partner choice) reinforces partner fidelity between solitary wasps and antibiotic-producing bacteria and thereby stabilizes this Cretaceous-age defensive mutualism. Phylogenetic analyses show that three genera of beewolf wasps (Philanthus , Trachypus , and Philanthinus) cultivate a distinct clade of Streptomyces bacteria for protection against pathogenic fungi. The symbionts were acquired from a soil-dwelling ancestor at least 68 million years ago, and vertical transmission via the brood cell and the cocoon surface resulted in host–symbiont codiversification. However, the external mode of transmission also provides opportunities for horizontal transfer, and beewolf species have indeed exchanged symbiont strains, possibly through predation or nest reuse. Experimental infection with nonnative bacteria reveals that—despite successful colonization of the antennal gland reservoirs—transmission to the cocoon is selectively blocked. Thus, partner choice can play an important role even in predominantly vertically transmitted symbioses by stabilizing the cooperative association over evolutionary timescales.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1400457111