title: Symbiont transmission entails the risk of parasite infection.
abstract: Like many animals, firebugs (Hemiptera, Pyrrhocoridae) rely on behavioural adaptations to successfully endow their offspring with microbial mutualists. To transmit the nutritionally beneficial Coriobacteriaceae symbionts, female firebugs smear egg surfaces with symbiont-containing faecal droplets that are subsequently ingested by newly hatched nymphs through active probing to initiate infection. Alternatively, the symbionts can be acquired horizontally through contact with faeces of infected conspecifics. Here, we report that these adaptations ensuring successful transmission of bacterial symbionts among firebugs are exploited by the specialized trypanosomatid parasite Leptomonas pyrrhocoris. Using comparative transcriptomics, fluorescence in situ hybridization (FISH) and controlled bioassays, we demonstrate that the transmission cycle of L. pyrrhocoris mirrors that of the bacterial mutualists, with high efficiency for both vertical and horizontal transmission. This indicates that the parasite capitalizes on pre-existing behavioural adaptations (egg smearing and probing) to facilitate its own transfer within host populations, adaptations that likely evolved to initiate and maintain an association with beneficial gut symbionts. Thus, the transmission of mutualistic microbes across host generations can entail a significant risk of co-transmitting pathogens or parasites, thereby exerting selective pressures on the host to evolve more specific mechanisms of transfer.
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany hsalem@ice.mpg.de.
authors.forename: Hassan
authors.initials: H
authors.lastname: Salem
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Thomas O
authors.initials: TO
authors.lastname: Onchuru
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany Luxembourg Centre for Systems Biomedicine, University of Luxembourg, L-4362 Esch-sur-Alzette, Luxembourg.
authors.forename: Eugen
authors.initials: E
authors.lastname: Bauer
authors.affiliation: Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany Department of Evolutionary Ecology, Johannes Gutenberg University, 55128 Mainz, Germany mkaltenpoth@uni-mainz.de.
authors.forename: Martin
authors.initials: M
authors.lastname: Kaltenpoth
mesh_terms: D039903:Actinobacteria / Q000502:physiology*; D000818:Animals; D001522:Behavior, Animal; D005243:Feces / Q000382:microbiology / Q000469:parasitology; D005260:Female; D020062:Heteroptera / Q000235:genetics / Q000382:microbiology* / Q000469:parasitology*; D013559:Symbiosis; D059467:Transcriptome; D014351:Trypanosomatina / Q000502:physiology*
keywords: host–parasite interaction; mutualism; symbiont; vertical and horizontal transmission