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

Abstract

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.protective symbiosis | cospeciation | mutualism stability | Hymenoptera | Crabronidae

A novel intracellular mutualistic bacterium in the invasive antCardiocondyla 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.…”

Evolution of host specialization in gut microbes: the bee gut as a model

“…Reported mechanisms of specificity References 51,52 Streptomyces philanthi beewolf wasps host response or behavior 53 Vibrio fischeri squid, fish, environmental biofilm production, bioluminescence 35,43 Xenorhabdus nematophila nematodes nilABC locus 40 …”

Possible odour-mediated attraction of flies to Bacillus subtilis NRS-762 stationary phase culture

“…Quorum-sensing is known to mediate communications between bacteria and higher organisms such as insects [21]. Extensive research over decades have characterized the directionality, mechanistic underpinnings, and molecular effectors of such parasitic and mutualistic relationships [22], where an insect either serve as a passive transporter of the microbe or, plays a more active role in helping complete part of the parasites' life cycle (e.g., malaria). In fact, many insects rely on symbiotic microbes for growth, survival and reproduction.…”

“…In fact, many insects rely on symbiotic microbes for growth, survival and reproduction. Beeoove wasps, for example, cultivate antibiotic-producing Streptomyces for protecting their larvae against microbial pathogens [22]. On the other hand, bacteria are reported to affect various stages of host development [23].…”

“…On the other hand, bacteria are reported to affect various stages of host development [23]. Similar to humans and other mammals, insects' gastrointestinal (GI) tracts are also colonized by a community of diverse microbes, many of which are commensals and non-pathogenic [22,24,25]. Looking beyond the well-understood roles of insects as disease vectors, less focus is placed on understanding alternate mechanisms underpinning the colonization of the insects' gastrointestinal (GI) tracts by specific bacteria, besides the oft-noted roles of microbes facilitating host digestion of recalcitrant nutrients, or providing the host with essential vitamins.…”