Tricking Parents: A Review of Mechanisms and Signals of Host Manipulation by Brood-Parasitic Young

Obligate avian brood parasites depend entirely on heterospecific hosts for rearing their offspring. From hatching until independence, the young parasites must deal with the challenge of obtaining sufficient parental care from foster parents that are attuned to provisioning their own offspring. Parent-offspring communication is mediated by complex begging displays in which nestlings and fledglings exhibit visual (e.g., gaping and postures) and vocal (e.g., begging calls) traits that serve as signals to parents to adjust and allocate parental effort. Parasites can manipulate host parental behavior by exploiting these stable parent-offspring communication systems in their favor. During the past 30 years, the study of host exploitation by parasitic chicks has yielded important insights into the function and evolution of manipulative signals in brood parasites. However, despite these major advances, there are still important gaps in our knowledge about how parasitic nestling and fledglings tune into the host’s communication channels and the adaptive value of the visual and acoustic signals they exhibit. Here we review the literature pertaining to host manipulation by parasitic young, focusing on four non-mutually exclusive mechanisms (i.e., host chick mimicry, begging exaggeration, host-attuned begging calls, and sensory exploitation) and the function and evolution of the signals involved, with the aim to summarize and discuss putative adaptations for stimulating parental feeding and escaping host discrimination. Finally, we bring some concluding remarks and suggest directions for future research on the ways in which brood parasites adapt to the communication systems of other birds to exploit the necessary parental care.

The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

Background Manipulative parasites are thought to liberate molecules in their external environment, acting as manipulation factors with biological functions implicated in their host’s physiological and behavioural alterations. These manipulation factors are part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite. It is necessary to study the molecular interaction between a manipulative parasite and its host to better understand how such alterations evolve. Methods Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission. We studied Schistocephalus solidus during the life stage in which behavioural changes take place in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We produced a novel genome sequence and assembly of S. solidus to improve protein coding gene prediction and annotation for this parasite. We then described the whole worm’s proteome and its secretome during fish host infection using LC–MS/MS. Results A total of 2290 proteins were detected in the proteome of S. solidus, and 30 additional proteins were detected specifically in the secretome. We found that the secretome contains proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We detected receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be manipulation factors. We also detected 12 S. solidus-specific proteins in the secretome that may play important roles in host–parasite interactions. Conclusions Our results suggest that S. solidus liberates molecules with putative host manipulation functions in the host and that many of them are species-specific. Graphical abstract

Transmission, infection, and pathogenesis

Transmission is a key process for parasites. Different routes (e.g. faecal–oral) and modes (e.g. by aerosols or vectors) exist. A major context is vertical (to offspring) or horizontal (all other) transmission. All components of the transmission process evolve. Successful transmission includes the infection of a new host. Macroparasites typically infect as individuals, but microparasites need an infective dose. Doses vary enormously among parasites. Various models describe variation in infective dose. Process-based models assume random colonization, co-operative parasite manipulation, or are focused on early dynamics. With the processes of pathogenesis (e.g. tissue destruction, reducing host capacities), damage to the host emerges. Virulence factors are important mediators of parasite success and often involved in host manipulation and pathogenesis, including immunopathology.

Viral-eukaryotic gene exchange drives infection mode and cellular evolution

Gene exchange between viruses and their hosts acts as a key facilitator of horizontal gene transfer and is thought to be a major driver of evolutionary change 1–3. Our understanding of this process comes primarily from bacteria and phage co-evolution4, but the mode and functional significance of gene transfers between eukaryotes and their viruses remains more anecdotal. Here we show that viral-eukaryotic gene exchange can define infection strategies and has recurrently influenced eukaryotic evolution. Using a systematic, phylogenetically-informed approach, we characterized viral-eukaryotic gene exchange across diverse taxa, identifying thousands of transfers, and revealing their frequency, taxonomic distribution, and projected functions, across the eukaryotic tree of life. Eukaryote-derived viral genes revealed common viral host-manipulation strategies, including the key cellular pathways and compartments targeted during infection, identifying potential targets for broad-spectrum host-targeted antiviral therapeutics. Furthermore, viral-derived eukaryotic genes exposed a recurring role for viral glycosyltransferases in the diversification of eukaryotic morphology, as viral-derived genes have impacted the evolution of structures as diverse as algal cell walls, trypanosome mitochondria, and animal tissues. These findings illuminate the nature of viral-eukaryotic gene exchange and its impact on the biology of viruses and their eukaryotic hosts, providing novel perspectives for understanding viral infection mechanisms and revealing the influence of viruses on eukaryotic evolution.

Behavioral manipulation of the spider Macrophyes pacoti (Araneae: Anyphaenidae) by the araneopathogenic fungus Gibellula sp. (Hypocreales: Cordycipitaceae)

Host manipulation has already been documented in several distinct host-parasite associations, covering all major phyla of living organisms. While in animals we know that several species have the ability to manipulate their hosts for the benefit of the parasite, in arthropopathogenic fungi there is very little knowledge about possible behavioral manipulation. We report for the first time the interaction between the araneopathogenic fungus Gibellula sp. Cavara and the spider Macrophyes pacoti Brescovit, Oliveira, Sobczak & Sobczak, 2019 (Anyphaenidae) in addition to investigating the potential change in behavior of spiders infected by the parasitic fungus. We also investigated whether the rainfall regime influences the abundance of infected spiders and the parasitism rate by the araneopathogenic fungus. Our results corroborated our hypothesis that the fungus induces vertical segregation in the spider population, inducing infected spiders to be at higher heights than uninfected ones. Dead infected spiders were found in a stretched position that probably helps in fixing the carcass on the leaves by increasing the contact surface between the host and the substrate. Our results also confirm the positive relationship between the rainy season and the greater number of parasitic spiders and the parasitism rate.