Parasite-mediated predation determines infection in a complex predator-prey-parasite system.

The interplay of host-parasite and predator-prey interactions is critical in ecological dynamics because both predators and parasites can regulate communities. But what is the prevalence of infected prey and predators when a parasite is transmitted through trophic interactions considering stochastic demographic changes? Here, we modelled and analysed a complex predator-prey-parasite system, where parasites are transmitted from prey to predators. We varied parasite virulence and infection probabilities to investigate how those evolutionary factors determine species' coexistence and populations' composition. Our results show that parasite species go extinct when the infection probabilities of either host are small and that success in infecting the final host is more critical for the survival of the parasite. While our stochastic simulations are consistent with deterministic predictions, stochasticity plays an important role in the border regions between coexistence and extinction. As expected, the proportion of infected individuals increases with the infection probabilities. Interestingly, the relative abundances of infected and uninfected individuals can have opposite orders in the intermediate and final host populations. This counterintuitive observation shows that the interplay of direct and indirect parasite effects is a common driver of the prevalence of infection in a complex system.

Season and host-community composition inside roosts may affect host-specificity of bat flies.

Bat flies are one of the most abundant ectoparasites of bats, showing remarkable morphological adaptations to the parasitic habit, while the relationship with their hosts is characterized by a high level of specificity. By collecting bat flies from live hosts, our intention was to elucidate the seasonal differences in bat fly occurrence and to describe factors regulating the level of incipient host specificity. Our results indicate that the prevalence and the intensity of infestation is increasing from spring to autumn for most host species, with significant differences among different fly species. Males showed higher infestation levels than females in autumn, suggesting a non-random host choice by flies, targeting the most active host sex. Bat-bat fly host specificity shows seasonal changes and host choice of bat flies are affected by the seasonal differences in hosts' behavior and ecology, the intensity of infestation and the species composition of the local host community. Nycteribiid bat flies showed lower host specificity in the swarming (boreal autumn) period, with higher prevalence recorded on non-primary hosts. Choosing a non-primary bat host may be an adaptive choice for bat flies in the host's mating period, thus increasing their dispersive ability in a high activity phase of their hosts.

Progeny counter mechanism in malaria parasites is linked to extracellular resources.

Malaria is caused by the rapid proliferation of Plasmodium parasites in patients and disease severity correlates with the number of infected red blood cells in circulation. Parasite multiplication within red blood cells is called schizogony and occurs through an atypical multinucleated cell division mode. The mechanisms regulating the number of daughter cells produced by a single progenitor are poorly understood. We investigated underlying regulatory principles by quantifying nuclear multiplication dynamics in Plasmodium falciparum and knowlesi using super-resolution time-lapse microscopy. This confirmed that the number of daughter cells was consistent with a model in which a counter mechanism regulates multiplication yet incompatible with a timer mechanism. P. falciparum cell volume at the start of nuclear division correlated with the final number of daughter cells. As schizogony progressed, the nucleocytoplasmic volume ratio, which has been found to be constant in all eukaryotes characterized so far, increased significantly, possibly to accommodate the exponentially multiplying nuclei. Depleting nutrients by dilution of culture medium caused parasites to produce fewer merozoites and reduced proliferation but did not affect cell volume or total nuclear volume at the end of schizogony. Our findings suggest that the counter mechanism implicated in malaria parasite proliferation integrates extracellular resource status to modify progeny number during blood stage infection.

Virus replication in the honey bee parasite, Varroa destructor.

IMPORTANCE: The parasitic mite Varroa destructor is a significant driver of worldwide colony losses of our most important commercial pollinator, the Western honey bee Apis mellifera. Declines in honey bee health are frequently attributed to the viruses that mites vector to honey bees, yet whether mites passively transmit viruses as a mechanical vector or actively participate in viral amplification and facilitate replication of honey bee viruses is debated. Our work investigating the antiviral RNA interference response in V. destructor demonstrates that key viruses associated with honey bee declines actively replicate in mites, indicating that they are biological vectors, and the host range of bee-associated viruses extends to their parasites, which could impact virus evolution, pathogenicity, and spread.

How colonization bottlenecks, tissue niches, and transmission strategies shape protozoan infections.

Protozoan pathogens such as Plasmodium spp., Leishmania spp., Toxoplasma gondii, and Trypanosoma spp. are often associated with high-mortality, acute and chronic diseases of global health concern. For transmission and immune evasion, protozoans have evolved diverse strategies to interact with a range of host tissue environments. These interactions are linked to disease pathology, yet our understanding of the association between parasite colonization and host homeostatic disruption is limited. Recently developed techniques for cellular barcoding have the potential to uncover the biology regulating parasite transmission, dissemination, and the stability of infection. Understanding bottlenecks to infection and the in vivo tissue niches that facilitate chronic infection and spread has the potential to reveal new aspects of parasite biology.

Light pollution may alter host-parasite interactions in aquatic ecosystems.

With growing human populations living along freshwater shores and marine coastlines, aquatic ecosystems are experiencing rising levels of light pollution. Through its effects on hosts and parasites, anthropogenic light at night can disrupt host-parasite interactions evolved under a normal photoperiod. Yet its impact on aquatic parasites has been ignored to date. Here, I discuss the direct effects of light on the physiology and behaviour of parasite infective stages and their hosts. I argue that night-time lights can change the spatiotemporal dynamics of infection risk and drive the rapid evolution of parasites. I then highlight knowledge gaps and how impacts on parasitic diseases should be incorporated into the design of measures aimed at mitigating the impact of anthropogenic light on wildlife.

Environmental parasitology: stressor effects on aquatic parasites.

Anthropogenic stressors are causing fundamental changes in aquatic habitats and to the organisms inhabiting these ecosystems. Yet, we are still far from understanding the diverse responses of parasites and their hosts to these environmental stressors and predicting how these stressors will affect host-parasite communities. Here, we provide an overview of the impacts of major stressors affecting aquatic ecosystems in the Anthropocene (habitat alteration, global warming, and pollution) and highlight their consequences for aquatic parasites at multiple levels of organisation, from the individual to the community level. We provide directions and ideas for future research to better understand responses to stressors in aquatic host-parasite systems.

Infection burdens and virulence under heat stress: ecological and evolutionary considerations.

As a result of global change, hosts and parasites (including pathogens) are experiencing shifts in their thermal environment. Despite the importance of heat stress tolerance for host population persistence, infection by parasites can impair a host's ability to cope with heat. Host-parasite eco-evolutionary dynamics will be affected if infection reduces host performance during heating. Theory predicts that within-host parasite burden (replication rate or number of infecting parasites per host), a key component of parasite fitness, should correlate positively with virulence-the harm caused to hosts during infection. Surprisingly, however, the relationship between within-host parasite burden and virulence during heating is often weak. Here, we describe the current evidence for the link between within-host parasite burden and host heat stress tolerance. We consider the biology of host-parasite systems that may explain the weak or absent link between these two important host and parasite traits during hot conditions. The processes that mediate the relationship between parasite burden and host fitness will be fundamental in ecological and evolutionary responses of host and parasites in a warming world. This article is part of the theme issue 'Infectious disease ecology and evolution in a changing world'.

Exploration of aminoacyl-tRNA synthetases from eukaryotic parasites for drug development.

Parasitic diseases result in considerable human morbidity and mortality. The continuous emergence and spread of new drug-resistant parasite strains is an obstacle to controlling and eliminating many parasitic diseases. Aminoacyl-tRNA synthetases (aaRSs) are ubiquitous enzymes essential for protein synthesis. The design and development of diverse small molecule, drug-like inhibitors against parasite-encoded and expressed aaRSs have validated this enzyme family as druggable. In this work, we have compiled the progress to date towards establishing the druggability of aaRSs in terms of their biochemical characterization, validation as targets, inhibitor development, and structural interpretation from parasites responsible for malaria (Plasmodium), lymphatic filariasis (Brugia,Wuchereria bancrofti), giardiasis (Giardia), toxoplasmosis (Toxoplasma gondii), leishmaniasis (Leishmania), cryptosporidiosis (Cryptosporidium), and trypanosomiasis (Trypanosoma). This work thus provides a robust framework for the systematic dissection of aaRSs from these pathogens and will facilitate the cross-usage of potential inhibitors to jump-start anti-parasite drug development.

Few studies of wild animal performance account for parasite infections: A systematic review.

Wild animals have parasites. This inconvenient truth has far-reaching implications for biologists measuring animal performance traits: infection with parasites can alter host behaviour and physiology in profound and sometimes counterintuitive ways. Yet, to what extent do studies on wild animals take individual infection status into account? We performed a systematic review across eight scientific journals primarily publishing studies in animal behaviour and physiology over a 5-year period to assess the proportion of studies which acknowledge, treat or control for parasite infection in their study design and/or analyses. We explored whether parasite inclusion differed between studies that are experimental versus observational, conducted in the field vs the laboratory and measured behavioural vs physiological traits. We also investigated the importance of other factors such as the journal, the trait category (e.g. locomotion, reproduction) measured, the vertebrate taxonomic group investigated and the host climatic zone of origin. Our results show that parasite inclusion was generally lacking across recent studies on wild vertebrates. In over 680 filtered papers, we found that only 21.9% acknowledged the potential effects of infections on animal performance in the text, and only 5.1% of studies treated animals for infection (i.e. parasite control) or considered infection status in the statistical analyses (i.e. parasite analysis). Parasite inclusion, control and analysis were higher in laboratory compared to field studies and higher for physiological studies compared to behavioural studies but did not differ among journals, performance trait categories and taxonomic groups. Among climatic zones, parasite inclusion, control and analysis were higher in tropical, subtropical and temperate zones than in boreal and polar zones. Overall, our literature review suggests that parasites are sorely under-acknowledged by researchers in recent years despite growing evidence that infections can modify animal performance. Given the ubiquity of parasites in the environment, we encourage scientists to consider individual infection status when assessing performance of wild animals. We also suggest ways for researchers to implement such practices in both experimental and observational studies.

The Defensive Interactions of Prominent Infectious Protozoan Parasites: The Host's Complement System.

The complement system exerts crucial functions both in innate immune responses and adaptive humoral immunity. This pivotal system plays a major role dealing with pathogen invasions including protozoan parasites. Different pathogens including parasites have developed sophisticated strategies to defend themselves against complement killing. Some of these strategies include the employment, mimicking or inhibition of host's complement regulatory proteins, leading to complement evasion. Therefore, parasites are proven to use the manipulation of the complement system to assist them during infection and persistence. Herein, we attempt to study the interaction´s mechanisms of some prominent infectious protozoan parasites including Plasmodium, Toxoplasma, Trypanosoma, and Leishmania dealing with the complement system. Moreover, several crucial proteins that are expressed, recruited or hijacked by parasites and are involved in the modulation of the host´s complement system are selected and their role for efficient complement killing or lysis evasion is discussed. In addition, parasite's complement regulatory proteins appear as plausible therapeutic and vaccine targets in protozoan parasitic infections. Accordingly, we also suggest some perspectives and insights useful in guiding future investigations.

Managing host-parasite interactions in humans and wildlife in times of global change.

Global change in the Anthropocene has modified the environment of almost any species on earth, be it through climate change, habitat modifications, pollution, human intervention in the form of mass drug administration (MDA), or vaccination. This can have far-reaching consequences on all organisational levels of life, including eco-physiological stress at the cell and organism level, individual fitness and behaviour, population viability, species interactions and biodiversity. Host-parasite interactions often require highly adapted strategies by the parasite to survive and reproduce within the host environment and ensure efficient transmission among hosts. Yet, our understanding of the system-level outcomes of the intricate interplay of within host survival and among host parasite spread is in its infancy. We shed light on how global change affects host-parasite interactions at different organisational levels and address challenges and opportunities to work towards better-informed management of parasite control. We argue that global change affects host-parasite interactions in wildlife inhabiting natural environments rather differently than in humans and invasive species that benefit from anthropogenic environments as habitat and more deliberate rather than erratic exposure to therapeutic drugs and other control efforts.

Predation shifts coevolution toward higher host contact rate and parasite virulence.

Hosts can avoid parasites (and pathogens) by reducing social contact, but such isolation may carry costs, e.g. increased vulnerability to predators. Thus, many predator-host-parasite systems confront hosts with a trade-off between predation and parasitism. Parasites, meanwhile, evolve higher virulence in response to increased host sociality and consequently, increased multiple infections. How does predation shift coevolution of host behaviour and parasite virulence? What if predators are selective, i.e. predators disproportionately capture the sickest hosts? We answer these questions with an eco-coevolutionary model parametrized for a Trinidadian guppy-Gyrodactylus spp. system. Here, increased predation drives host coevolution of higher grouping, which selects for higher virulence. Additionally, higher predator selectivity drives the contact rate higher and virulence lower. Finally, we show how predation and selectivity can have very different impacts on host density and prevalence depending on whether hosts or parasites evolve, or both. For example, higher predator selectivity led to lower prevalence with no evolution or only parasite evolution but higher prevalence with host evolution or coevolution. These findings inform our understanding of diverse systems in which host behavioural responses to predation may lead to increased prevalence and virulence of parasites.

RECRUITMENT AND SEASONAL OCCURRENCE OF PARASITES IN JUVENILE INVASIVE ROUND GOBIES (NEOGOBIUS MELANOSTOMUS) IN THE ST. LAWRENCE RIVER, QUEBEC, CANADA.

The round goby (Neogobius melanostomus) is an invasive species that has become one of the most abundant fish in the St. Lawrence River, Quebec, Canada over the past 15 yr. Since its introduction, the round goby has acquired a number of native parasites, yet little is known about the dynamics of parasite recruitment. To examine this question, young-of-the-year and juvenile round gobies were collected monthly from 2 localities in the river (Îles de la Paix, Île Dorval) from June through November 2012. At Îles de la Paix, round gobies (n = 180) were infected with 3 species of parasites, all larval stages (Diplostomum spp., Tylodelphys scheuringi, Neoechinorhynchus tenellus). Prevalence of the digenean Diplostomum spp. varied from 3.3 to 13.3%, and mean abundance from 0.03 to 0.53 from June through September, with a maximum in August. The digenean T. scheuringi was seen only in August, at a prevalence of 10.0% and a mean abundance of 0.53. The acanthocephalan N. tenellus was observed in June, August, and September, prevalence ranging from 3.3 to 10.0% and mean abundance from 0.03 to 0.27. Maximum infection for all 3 species occurred in August. All infected fish were ≥44 mm in total length (TL). Fish infected with more than 1 parasite species were >60 mm TL. No round goby (n = 178) was infected at Île Dorval. This study demonstrated that the invasive round goby starts to acquire parasite infections in the St. Lawrence River in the first year of life and may contribute to the transmission of some parasites within this ecosystem.

Evolutionary Transitions of Parasites between Freshwater and Marine Environments.

Evolutionary transitions of organisms between environments have long fascinated biologists, but attention has been focused almost exclusively on free-living organisms and challenges to achieve such transitions. This bias requires addressing because parasites are a major component of biodiversity. We address this imbalance by focusing on transitions of parasitic animals between marine and freshwater environments. We highlight parasite traits and processes that may influence transition likelihood (e.g., transmission mode, life cycle, host use), and consider mechanisms and directions of transitions. Evidence for transitions in deep time and at present are described, and transitions in our changing world are considered. We propose that environmental transitions may be facilitated for endoparasites because hosts reduce exposure to physiologically challenging environments and argue that adoption of an endoparasitic lifestyle entails an equivalent transitioning process as organisms switch from living in one environment (e.g., freshwater, seawater, or air) to living symbiotically within hosts. Environmental transitions of parasites have repeatedly resulted in novel forms and diversification, contributing to the tree of life. Recognizing the potential processes underlying present-day and future environmental transitions is crucial in view of our changing world and the current biodiversity crisis.

Host-parasite coevolution: Backseat drivers take the wheel at the Red Queen's race.

Defensive microbial symbionts are common in plants and animals, protecting their hosts against parasitic enemies. Rafaluk-Mohr et al. show that defensive microbes alter the trajectory of host-parasite coevolution, favouring the evolution of fundamentally different life-history responses to infection.

Malaria parasites do respond to heat.

The capacity of malaria parasites to respond to changes in their environment at the transcriptional level has been the subject of debate, but recent evidence has unambiguously demonstrated that Plasmodium spp. can produce adaptive transcriptional responses when exposed to some specific types of stress. These include metabolic conditions and febrile temperature. The Plasmodium falciparum protective response to thermal stress is similar to the response in other organisms, but it is regulated by a transcription factor evolutionarily unrelated to the conserved transcription factor that drives the heat shock (HS) response in most eukaryotes. Of the many genes that change expression during HS, only a subset constitutes an authentic response that contributes to parasite survival.

Neuroimmunology of Common Parasitic Infections in Africa.

Parasitic infections of the central nervous system are an important cause of morbidity and mortality in Africa. The neurological, cognitive, and psychiatric sequelae of these infections result from a complex interplay between the parasites and the host inflammatory response. Here we review some of the diseases caused by selected parasitic organisms known to infect the nervous system including Plasmodium falciparum, Toxoplasma gondii, Trypanosoma brucei spp., and Taenia solium species. For each parasite, we describe the geographical distribution, prevalence, life cycle, and typical clinical symptoms of infection and pathogenesis. We pay particular attention to how the parasites infect the brain and the interaction between each organism and the host immune system. We describe how an understanding of these processes may guide optimal diagnostic and therapeutic strategies to treat these disorders. Finally, we highlight current gaps in our understanding of disease pathophysiology and call for increased interrogation of these often-neglected disorders of the nervous system.

The weaker sex: Male lingcod (Ophiodon elongatus) with blue color polymorphism are more burdened by parasites than are other sex-color combinations.

The unusual blue color polymorphism of lingcod (Ophiodon elongatus) is the subject of much speculation but little empirical research; ~20% of lingcod individuals exhibit this striking blue color morph, which is discrete from and found within the same populations as the more common brown morph. In other species, color polymorphisms are intimately linked with host-parasite interactions, which led us to ask whether blue coloration in lingcod might be associated with parasitism, either as cause or effect. To test how color and parasitism are related in this host species, we performed parasitological dissection of 89 lingcod individuals collected across more than 26 degrees of latitude from Alaska, Washington, and California, USA. We found that male lingcod carried 1.89 times more parasites if they were blue than if they were brown, whereas there was no difference in parasite burden between blue and brown female lingcod. Blue individuals of both sexes had lower hepatosomatic index (i.e., relative liver weight) values than did brown individuals, indicating that blueness is associated with poor body condition. The immune systems of male vertebrates are typically less effective than those of females, due to the immunocompromising properties of male sex hormones; this might explain why blueness is associated with elevated parasite burdens in males but not in females. What remains to be determined is whether parasites induce physiological damage that produces blueness or if both blue coloration and parasite burden are driven by some unmeasured variable, such as starvation. Although our study cannot discriminate between these possibilities, our data suggest that the immune system could be involved in the blue color polymorphism-an exciting jumping-off point for future research to definitively identify the cause of lingcod blueness and a hint that immunocompetence and parasitism may play a role in lingcod population dynamics.

The hump-shaped effect of plant functional diversity on the biological control of a multi-species pest community.

Plant taxonomic and functional diversity promotes interactions at higher trophic levels, but the contribution of functional diversity effects to multitrophic interactions and ecosystem functioning remains unclear. We investigated this relationship in a factorial field experiment comparing the effect of contrasting plant communities on parasitism rates in five herbivore species. We used a mechanistic trait-matching approach between plant and parasitoids to determine the amount of nectar available and accessible to parasitoids. This trait-matching approach best explained the rates of parasitism of each herbivorous species, confirming the predominant role of mass-ratio effects. We found evidence for an effect of functional diversity only in analyses considering the ability of plant communities to support the parasitism of all herbivores simultaneously. Multi-species parasitism was maximal at intermediate levels of functional diversity. Plant specific richness had a negligible influence relative to functional metrics. Plant communities providing large amounts of accessible nectar and with intermediate levels of functional diversity were found to be the most likely to enhance the conservation biological control of diverse crop herbivores.