Infected Conspecifics Research Articles

Juvenile agile frogs spatially avoid ranavirus-infected conspecifics

Exposure to contagious pathogens can result in behavioural changes, which can alter the spread of infectious diseases. Healthy individuals can express generalized social distancing or avoid the sources of infection, while infected individuals can show passive or active self-isolation. Amphibians are globally threatened by contagious diseases, yet their behavioural responses to infections are scarcely known. We studied behavioural changes in agile frog (Rana dalmatina) juveniles upon exposure to a Ranavirus (Rv) using classic choice tests. We found that both non-infected and Rv-infected focal individuals spatially avoided infected conspecifics, while there were no signs of generalized social distancing, nor self-isolation. Avoidance of infected conspecifics may effectively hinder disease transmission, protecting non-infected individuals as well as preventing secondary infections in already infected individuals. On the other hand, the absence of self-isolation by infected individuals may facilitate it. Since infection status did not affect the time spent near conspecifics, it is unlikely that the pathogen manipulated host behaviour. More research is urgently needed to understand under what circumstances behavioural responses can help amphibians cope with infections, and how that affects disease dynamics in natural populations.

Chemical sensing and avoidance of PaV1-infected conspecifics by pueruli post-larvae of the reef-dwelling Caribbean spiny lobster Panulirus argus Latreille, 1804 (Decapoda: Achelata: Palinuridae)

Abstract Little is known about chemical sensing during settlement by pueruli of the Caribbean spiny lobster Panulirus argus Latreille, 1804 and the effect that Panulirus argus virus 1 (PaV1), the first pathogenic virus to infect any spiny lobster, has on settling pueruli. Considering that the avoidance of PaV1-infected lobsters by early-benthic juveniles is well documented and the previously reported costs of close proximity to PaV1-infected early-benthic juveniles (increased mortality risk), pueruli of P. argus should avoid infected conspecifics during settlement. We experimentally tested if pueruli show aversion to PaV1-infected conspecifics. We also re-tested the previously reported effect of red algae (Laurencia spp.) and healthy conspecifics on pueruli settlement decisions. Considering the known benefits of inhabiting red algae and costs of close proximity to conspecific juveniles, pueruli were predicted to be attracted to metabolites produced by red algae and repulsed by metabolites produced by conspecifics. We also predicted that attraction to red algae would decrease or cease if this cue was presented together with cues produced by PaV1-infected conspecifics. Our experiments indicate that pueruli do not avoid metabolites produced by benthic juveniles and are not attracted to metabolites produced by red algae. Importantly, pueruli are attracted to a combination of metabolites produced by red algae and conspecific juveniles but this attraction ceases if conspecifics are PaV1-infected. Our results indicate that PaV1 disrupts habitat selection by settling pueruli and suggest that assumptions about cost and benefits experienced by settling pueruli need to be revisited. Research to improve the understanding of the relationship between recruitment, disease avoidance, and fishery stock in this heavily exploited spiny lobster is needed.

Human scent as a first-line defense against disease

Individuals may have a different body odor, when they are sick compared to healthy. In the non-human animal literature, olfactory cues have been shown to predict avoidance of sick individuals. We tested whether the mere experimental activation of the innate immune system in healthy human individuals can make an individuals’ body odor be perceived as more aversive (intense, unpleasant, and disgusting). Following an endotoxin injection (lipopolysaccharide; 0.6 ng/kg) that creates a transient systemic inflammation, individuals smelled more unpleasant compared to a placebo group (saline injection). Behavioral and chemical analyses of the body odor samples suggest that the volatile components of samples from “sick” individuals changed qualitatively rather than quantitatively. Our findings support the hypothesis that odor cues of inflammation in axillary sweat are detectable just a few hours after experimental activation of the innate immune system. As such, they may trigger behavioral avoidance, hence constituting a first line of defense against pathogens of infected conspecifics.

Disgusted snails, oxytocin, and the avoidance of infection threat

Disgust is considered to be a fundamental affective state associated with triggering the behavioral avoidance of infection and parasite/pathogen threat. In humans, and other vertebrates, disgust affects how individuals interact with, and respond to, parasites, pathogens and potentially infected conspecifics and their sensory cues. Here we show that the land snail, Cepaea nemoralis, displays a similar “disgust-like” state eliciting behavioral avoidance responses to the mucus associated cues of infected and potentially infected snails. Brief exposure to the mucus of snails treated with the Gram-negative bacterial endotoxin, lipopolysaccharide (LPS), elicited dose-related behavioral avoidance, including acute antinociceptive responses, similar to those expressed by mammals. In addition, exposure to the mucus cues of LPS treated snails led to a subsequent avoidance of unfamiliar individuals, paralleling the recognition of and avoidance responses exhibited by vertebrates exposed to potential pathogen risk. Further, the avoidance of, and antinociceptive responses to, the mucus of LPS treated snails were attenuated in a dose-related manner by the oxytocin (OT) receptor antagonist, L-368,899. This supports the involvement of OT and OT receptor homologs in the expression of infection avoidance, and consistent with the roles of OT in the modulation of responses to salient social and infection threats by rodents and other vertebrates. These findings with land snails are indicative of evolutionarily conserved disgust-like states associated with OT/OT receptor homolog modulated behavioral avoidance responses to infection and pathogen threat.

Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms.

German cockroaches (Blattella germanica) can be both mechanical and biological (amplifying) vectors of enteric pathogens, including Salmonella enterica serovar Typhimurium (S. Typhimurium), which they acquire by feeding upon contaminated substances. Blattella germanica is also a gregarious species that shelters in groups and partakes in unique feeding behaviors such as conspecific coprophagy, necrophagy, and emetophagy. These properties create an interphase for potential horizontal transmission of pathogens among cockroach populations through the fecal-oral route, which could in turn enhance transmission to humans and other animals. Here, we performed a series of experiments to determine: (1) whether horizontal transmission of S. Typhimurium infection takes place in B. germanica, (2) the prevalence of the phenomenon, and (3) the route(s) through which it may occur. We reveal that true horizontal transmission of S. Typhimurium occurs among B. germanica. That is, uninfected cockroaches acquire infection of the gut when co-housed with orally infected conspecifics, albeit at low frequency. Furthermore, we provide definitive evidence that coprophagy and necrophagy are routes of transmission but could not exclude sharing of food or water as contributing routes. On the contrary, transmission by emetophagy appears less likely as oral regurgitates from infected cockroaches contained S. Typhimurium for less than one day after ingesting the bacteria. Together, our data enhance current understanding of the ecology of vector-borne S. Typhimurium transmission by cockroaches, implicating conspecific horizontal transmission as a phenomenon that contributes to maintaining infected cockroach populations independently of contact with primary sources of the pathogen. Although the relative importance of horizontal transmission of pathogens in cockroaches in the field remains to be determined, these results also highlight the important role that food and water sources in the local environment may play in cockroach-borne pathogen transmission and emphasize the importance of sanitation for not only abating infestations but also mitigating pathogen transmission.

Ranavirus infection-induced avoidance behaviour in wood frog juveniles: do amphibians socially distance?

Hosts may limit exposure to pathogens through changes in behaviour, such as avoiding infected individuals or contaminated areas. Here, we tested for a behavioural response to ranavirus infection in juvenile wood frogs (<i>Rana sylvatica</i>) because the majority of dispersal between populations occurs during this life stage. We hypothesized that if infections are transmissible and detectable at this life stage, then susceptibles would display avoidance behaviours when introduced to an infected conspecific. Despite no apparent signs of infection, we observed a greater distance between susceptible-infected pairs, compared to pairs of either two infected or two susceptible animals. Further, distances between susceptible-infected pairs were positively related to the infection intensity of the focal exposed frog, suggesting the cue to avoid infected conspecifics may become more detectable with more intense infections. Although we did not quantify whether the transmission was affected by their distancing, our findings suggest that juvenile frogs have the potential to reduce terrestrial transmission of ranaviruses through avoidance behaviours.

Social factors and the neurobiology of pathogen avoidance.

Although the evolutionary causes and consequences of pathogen avoidance have been gaining increasing interest, there has been less attention paid to the proximate neurobiological mechanisms. Animals gauge the infection status of conspecifics and the threat they represent on the basis of various sensory and social cues. Here, we consider the neurobiology of pathogen detection and avoidance from a cognitive, motivational and affective state (disgust) perspective, focusing on the mechanisms associated with activating and directing parasite/pathogen avoidance. Drawing upon studies with laboratory rodents, we briefly discuss aspects of (i) olfactory-mediated recognition and avoidance of infected conspecifics; (ii) relationships between pathogen avoidance and various social factors (e.g. social vigilance, social distancing (approach/avoidance), social salience and social reward); (iii) the roles of various brain regions (in particular the amygdala and insular cortex) and neuromodulators (neurotransmitters, neuropeptides, steroidal hormones and immune components) in the regulation of pathogen avoidance. We propose that understanding the proximate neurobiological mechanisms can provide insights into the ecological and evolutionary consequences of the non-consumptive effects of pathogens and how, when and why females and males engage in pathogen avoidance.

No evidence that songbirds use odour cues to avoid malaria-infected conspecifics

Abstract Many animals have evolved mechanisms to detect and avoid parasitized conspecifics, primarily through odour cues, but whether birds are capable of odour-mediated parasite avoidance is unknown. Recently, we showed that exposing song sparrows (Melospiza melodia) to avian malaria parasites (Plasmodium sp.) alters the chemical composition of their preen oil, which is the major source of body odour in birds. Here, we presented song sparrows with preen oil from uninfected (sham-inoculated) and malaria-infected conspecifics, predicting that birds would spend more time with odour cues from uninfected than infected birds. Birds without detectable malarial infections spent about 50% more time with preen oil from uninfected than infected conspecifics, and females spent nearly twice as much time with preen oil from uninfected than infected conspecifics. However, neither difference was statistically significant. Song sparrows may be able to detect odour cues of infection, but further experiments are needed to confirm or refute this.

Parasitism Risk and Infection Alter Host Dispersal

Dispersal determines the spatial dynamics of host-parasite assemblages, particularly during invasions and disease epidemics. The risk of parasitism may create an incentive for dispersal, but infection is expected to reduce dispersal ability, which may alter the host's dispersal response to biotic stressors, including population density. We measured the dispersal of a semiaquatic insect (Notonecta undulata) in aquatic mesocosms in which we manipulated the presence of ectoparasitic Hydrachnidia mites and infected conspecifics. We found that parasitism risk increases host dispersal propensity. Using a flight assay, we determined that parasite infection reduces host dispersal ability. Finally, we used a mark-release-recapture study to investigate the joint effects of both parasitism risk and parasite infection on host dispersal in a natural, spatially structured population. We found that parasitism risk reduced dispersal probability, eliminated positive density-dependent dispersal, and increased dispersal distance. Infection had no effect on dispersal in the natural population. Our results show that parasites can both increase and decrease the movement rates of their hosts, depending on the ecological context, and can alter the host's dispersal response to other biotic stressors. Future studies should consider the consequences of this double-headed impact of parasites for landscape connectivity, population persistence, and host-parasite coevolution.

Recovery from infection is more likely to favour the evolution of migration than social escape from infection.

Pathogen and parasite infections are increasingly recognized as powerful drivers of animal movement, including migration. Yet, infection-related migration benefits can result from a combination of environmental and/or social conditions, which can be difficult to disentangle. Here, we focus on two infection-related mechanisms that can favour migration: moving to escape versus recover from infection. By directly comparing the evolution of migration in response to each mechanism, we can evaluate the likely importance of changing abiotic conditions (linked to migratory recovery) with changing social conditions (linked to migratory escape) in terms of infection-driven migration. We built a mathematical model and analysed it using numerically simulated adaptive dynamics to determine when migration should evolve for each migratory recovery and social migratory escape. We found that a higher fraction of the population migrated under migratory recovery than under social migratory escape. We also found that two distinct migratory strategies (e.g. some individuals always migrate and others only occasionally migrate) sometimes coexisted within populations with social migratory escape, but never with migratory recovery. Our results suggest that migratory recovery is more likely to promote the evolution of migratory behaviour, rather than escape from infected conspecifics (social migratory escape).

Parasites influence cannibalistic and predatory interactions within and between native and invasive amphipods.

In Northern Ireland, the amphipods Gammarus duebeni celticus (native) and G. pulex (invasive) coexist in some places, whilst in others the native species has been replaced by the invader. We explored the role of parasites in mediating interactions between these amphipods, which demonstrate mutual intraguild predation (IGP: predation between animals that also compete for prey). IGP and cannibalism can be important factors in structuring populations and communities. We investigated the effects of parasitism on rates of IGP between G. d. celticus and G. pulex and on cannibalism within each species by comparing functional responses (FRs: relationships between the use of a prey resource and its availability). Infection with the microsporidian Pleistophora mulleri caused an increase in IGP and cannibalism by G. d. celticus, which showed increased attack rates and reduced prey handling times. In contrast, infection with the acanthocephalan parasite Echinorhynchus truttae did not alter IGP or cannibalism by G. pulex. A prey preference experiment revealed that both amphipods were more likely to feed on heterospecific rather than conspecific prey, and this was also corroborated by the fact that overall IGP FRs were higher than cannibalism FRs. This may be selectively advantageous, as feeding on heterospecific prey removes possible competitors without the risk of consuming juvenile kin or acquiring parasites from infected conspecifics. Infection of the native G. d. celticus with P. mulleri enhanced IGP on the invasive G. pulex, which is likely to facilitate the coexistence of the 2 species.

Conspecific infection threat rapidly biases the social responses of female mice: Involvement of oxytocin

Pathogen threat affects social preferences and responses across species. Here we examined the effects of social context and the infection status of conspecific females and males on the social and mate responses of female mice. The responses of female mice to males were rapidly affected by the presence of infected female conspecifics and infected males. In mice odor cues drive appetitive and aversive social and mate responses. Brief (1 min) exposure to the fresh urinary odors of females infected with the murine nematode parasite, Heligmosomoides polygyrus, attenuated the responses of other uninfected females to the odors of naturally preferred unfamiliar males and enhanced their preferences for familiar males. Likewise exposure to the odors of a male either infected with H. polygyrus or treated with the bacterial endotoxin, lipopolysaccharide, reduced the responses of females to the odors of unfamiliar males. In addition, females displayed an avoidance of, and discrimination against, male mice whose odors had been associated with that of an infected female (“guilt by association”) and a preference for the odors associated with an uninfected female (“mate copying”). These shifts in preferences for female associated male odors were attenuated in a dose-related manner by pre-treatment with the oxytocin receptor antagonist, L-368,899. These findings show that social information associated with the infection status of conspecifics can rapidly bias the mate preferences of female mice in an oxytocin receptor dependent manner.

Male chemical cues as reliable indicators of infection in the wolf spider Schizocosa ocreata

AbstractSexual signals can convey important information about mate quality, such as critical information about a signaler's health status, helping an individual to avoid infected or immunocompromised conspecifics. Chemical signals are especially important in this context, because they represent an honest and dynamic signaling modality that receivers can use to make updated mate choice decisions to avoid compromising their own health. In this study, we investigated the viability of male chemical cues in the wolf spider Schizocosa ocreata as a reliable indicator of health status. Using video playback with images of an average male that is simultaneously paired with male cuticular compounds on filter paper, we show that females are more receptive to videos paired with cues from control males rather than infected males. We also show that these cuticular compounds can be isolated and retain similar female behavioral responses when extracted with a nonpolar solvent, suggesting that these cuticular compounds may not be just complex hydrocarbons, but a combination of cuticular compounds. This is the first evidence for female discrimination and recognition of male chemical cues in this species, which opens up important new avenues of research in a well‐studied species with complex multimodal signaling.

White spot syndrome virus and the Caribbean spiny lobster, Panulirus argus: Susceptibility and behavioral immunity.

The Caribbean spiny lobster Panulirus argus is susceptible to infection by Panulirus argus Virus 1 (PaV1), the only virus known to naturally infect any lobster species. However, P. argus is able to mitigate PaV1 transmission risk by avoiding infected individuals. P. argus may also be susceptible to another lethal virus, White Spot Syndrome Virus (WSSV). WSSV has not been documented in wild populations of spiny lobsters, but has been experimentally transmitted to six other lobster species from the genus Panulirus. Although WSSV has been detected intermittently in wild populations of shrimp in the Caribbean region, the risk to P. argus has not been evaluated. Potential emergence of the disease could result in fisheries losses and ecological disruption. To assess the risk to P. argus, we tested its susceptibility to WSSV via injection and waterborne transmission. We also tested whether healthy lobsters can detect and avoid conspecifics with qPCR-quantifiable WSSV infections. We found P. argus to be highly susceptible to WSSV via intramuscular injection, with mortality reaching 88% four weeks post inoculation. Panulirus argus was also susceptible to WSSV via waterborne transmission, but WSSV burden was low after four weeks via qPCR. Behavioral assays indicated that P. argus can detect and avoid conspecifics infected with WSSV and the avoidance response was strongest for the most heavily infected individuals - a response comparable to PaV1-infected conspecifics. Panulirus argus is the first spiny lobster found to be susceptible to WSSV in the Americas, but it is possible that a generalized avoidance response by healthy lobsters against infected conspecifics provides a behavioral defense and may reduce WSSV infection potential and prevalence. Preliminary evidence suggests that the infiltration of hemolymph constituents into the urine may be the source of the avoidance behavior and could therefore extend to other directly transmitted pathogens in spiny lobster populations preventing them from becoming common in their population.

Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies.

Associating with conspecifics afflicted with infectious diseases increases the risk of becoming infected, but engaging in avoidance behaviour incurs the cost of lost social benefits. Across systems, infected individuals vary in the transmission risk they pose, so natural selection should favour risk-sensitive avoidance behaviour that optimally balances the costs and benefits of sociality. Here, we use the guppy Poecilia reticulata-Gyrodactylus turnbulli host-parasite system to test the prediction that individuals avoid infected conspecifics in proportion to the transmission risk they pose. In dichotomous choice tests, uninfected fish avoided both the chemical and visual cues, presented separately, of infected conspecifics only in the later stages of infection. A transmission experiment indicated that this avoidance behaviour accurately tracked transmission risk (quantified as both the speed at which transmission occurs and the number of parasites transmitting) through the course of infection. Together, these findings reveal that uninfected hosts can use redundant cues across sensory systems to inform dynamic risk-sensitive avoidance behaviour. This correlation between the transmission risk posed by infected individuals and the avoidance response they elicit has implications for the evolutionary ecology of infectious disease, and its explicit inclusion may improve the ability of epidemic models to predict disease spread.

Shoaling with infected conspecifics does not improve resistance to trematode infection

AbstractGroup‐living animals can gain protection against parasitic infections through social contacts with previously infected conspecifics (social immunization). Recent research suggests that such protective effects can be induced through visual or chemical cues released by infected individuals, resulting in anticipatory immune upregulation among group members. Here, we study cue‐induced social resistance in rainbow trout Oncorhynchus mykiss exposed to a trematode parasite, the eye‐fluke Diplostomum pseudospathaceum. We established groups of naïve individuals (receivers) that were paired with previously infected individuals (donors) at different ratios of donors to receivers and at different time points since donor exposure to capture varying concentrations of the anticipated cues. While the pre‐infection elevated resistance among the donors, there was no evidence of social transfer of resistance, regardless of the ratio of donors and receivers in a group or the time since the pre‐infection. The results suggest that resistance through social signalling may be system‐specific and requires further study into the generality of the phenomenon as well as the nature of the cues involved.

Parasitic infection of the eye lens affects shoaling preferences in three-spined stickleback

The ability to compete with conspecifics and to adequately respond to visual stimuli of group mates are important prerequisites for profiting from group benefits such as confusion of predators and greater efficiency in acquiring food. By impairing their host’s physical abilities or making the host conspicuous, even non-contagious parasites that do not pose a direct risk of infection can interfere with group dynamics. Diplostomum pseudospathaceum, a widespread parasite of freshwater fishes, infects the eye lens and can impair the vision of its fish host. To test whether this eyefluke affects competitiveness and/or shoaling behaviour in three-spined stickleback (Gasterosteus aculeatus), experimentally infected fish were kept in mixed groups comprising infected and uninfected sticklebacks under limited food availability in semi-natural outdoor tanks. Change in body mass over time was measured and sticklebacks were given the choice to shoal with uninfected conspecifics or a mixed group in binary shoal choice experiments. Surprisingly, uninfected sticklebacks spent significantly more time with mixed shoals than with uninfected shoals while this preference was not found in infected sticklebacks. Infection did not significantly affect body condition or immune parameters indicative of stress level (relative spleen mass, granulocyte-to-lymphocyte ratio). The results suggest that sticklebacks can distinguish mixed from uninfected groups, but that they are also able to tolerate potential detrimental effects of infection. Whether uninfected fish can benefit from shoaling with infected but non-contagious conspecifics remains to be tested. Although the present data do not indicate a significant effect of infection on competitiveness, this should be examined further.

No evidence for homosubtypic immunity of influenza H3 in Mallards following vaccination in a natural experimental system.

The Mallard (Anas platyrhynchos) is an important reservoir species for influenza A viruses (IAV), and in this host, prevalence and virus diversity are high. Studies have demonstrated the presence of homosubtypic immunity, where individuals are unlikely to be reinfected with the same subtype within an autumn season. Further, evidence for heterosubtypic immunity exists, whereby immune responses specific for one subtype offer partial or complete protection against related HA subtypes. We utilized a natural experimental system to determine whether homo‐ or heterospecific immunity could be induced following experimental vaccination. Thirty Mallards were vaccinated with an inactivated H3, H6 or a sham vaccine and after seroconversion were exposed to naturally infected wild conspecifics. All ducks were infected within 2 days and had both primary and secondary infections. Overall, there was no observable difference between groups; all individuals were infected with H3 and H10 IAV. At the cessation of the experiment, most individuals had anti‐NP antibodies and neutralizing antibodies against H10. Not all individuals had H3 neutralizing antibodies. The isolated H3 IAVs revealed genetic dissimilarity to the H3 vaccine strain, specifically substitutions in the vicinity of the receptor‐binding site. There was no evidence of vaccine‐induced homosubtypic immunity to H3, a likely result of both a poor H3 immune response in the ducks and H3 immune escape. Likewise, there was no observed heterosubtypic protection related to H6 vaccination. This study highlights the need for experimental approaches to assess how exposure to pathogens and resulting immune processes translates to individual and population disease dynamics.

Cannibalism amplifies the spread of vertically transmitted pathogens.

Cannibalism is a widespread behavior. Abundant empirical evidence demonstrates that cannibals incur a risk of contracting pathogenic infections when they consume infected conspecifics. However, current theory suggests that cannibalism generally impedes disease spread, because each victim is usually consumed by a single cannibal, such that cannibalism does not function as a spreading process. Consequently, cannibalism cannot be the only mode of transmission of most parasites. We develop simple, but general epidemiological models to analyze the interaction of cannibalism and vertical transmission. We show that cannibalism increases the prevalence of vertically transmitted pathogens whenever the host population density is not solely regulated by cannibalism. This mechanism, combined with additional, recently published, theoretical mechanisms, presents a strong case for the role of cannibalism in the spread of infectious diseases across a wide range of parasite-host systems.

Symbiont transmission entails the risk of parasite infection.

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.