No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Extreme Competence: Keystone Hosts of Infections
Abstract
Individual hosts differ extensively in their competence for parasites, but traditional research has discounted this variation, partly because modeling such heterogeneity is difficult. This discounting has diminished as tools have improved and recognition has grown that some hosts, the extremely competent, can have exceptional impacts on disease dynamics. Most prominent among these hosts are the superspreaders, but other forms of extreme competence (EC) exist and others await discovery; each with potentially strong but distinct implications for disease emergence and spread. Here, we propose a framework for the study and discovery of EC, suitable for different host–parasite systems, which we hope enhances our understanding of how parasites circulate and evolve in host communities.
... Indeed, fundamental to the challenge of understanding the dynamics of zoonotic diseases is that parasites are frequently highly aggregated among individual hosts (Poulin, 2007), often leading to extreme variation in parasite prevalence in time and space. Such variation is observed at the intraspecific and interspecific levels (i.e., superspreader individuals or diluter species) (Martin et al., 2019), and may be spatiotemporally variable (i.e., hotspots of pathogen prevalence) (Paull et al., 2012). To grapple with such extreme heterogeneity in systems often characterized by multiple hosts spread over large spatial scales, we must find a way to understand the causes of variation in key components of zoonoses, such as host-parasite encounters. ...
... Particular behaviors may provide insight into variation in host-vector interactions at multiple levels of organization (Sih et al., 2018). For instance, individuals that are more central in social networks or are highly mobile may more often contact vectors and other hosts, making them more likely to be superspreaders (Martin et al., 2019;Paull et al., 2012). Similarly, species that are highly social and, thus, readily acquire and transmit parasites, may be termed "amplification hosts" (Paull et al., 2012). ...
... Similarly, species that are highly social and, thus, readily acquire and transmit parasites, may be termed "amplification hosts" (Paull et al., 2012). By contrast, species that are highly effective at killing parasites may be "superdiluters" (Martin et al., 2019). Hotspots may arise spatially at feeding sites, breeding grounds, or watering holes, or temporally due to seasonal shifts in behavior (i.e., migration, breeding, wintering grounds) (Paull et al., 2012). ...
Identifying the factors that affect host–parasite interactions is essential for understanding the ecology and dynamics of vector‐borne diseases and may be an important component of predicting human disease risk. Characteristics of hosts themselves (e.g., body condition, host behavior, immune defenses) may affect the likelihood of parasitism. However, despite highly variable rates of parasitism and infection in wild populations, identifying widespread links between individual characteristics and heterogeneity in parasite acquisition has proven challenging because many zoonoses exist over wide geographic extents and exhibit both spatial and temporal heterogeneity in prevalence and individual and population‐level effects. Using seven years of data collected by the National Ecological Observatory Network (NEON), we examined relationships among individual host condition, behavior, and parasitism by Ixodid ticks in a keystone host species, the white‐footed mouse, Peromyscus leucopus. We found that individual condition, specifically sex, body mass, and reproductive condition, had both direct and indirect effects on parasitism by ticks, but the nature of these effects differed for parasitism by larval versus nymphal ticks. We also found that condition differences influenced rodent behavior, and behavior directly affected the rates of parasitism, with individual mice that moved farther being more likely to carry ticks. This study illustrates how individual‐level data can be examined using large‐scale datasets to draw inference and uncover broad patterns in host–parasite encounters at unprecedented spatial scales. Our results suggest that intraspecific variation in the movement ecology of hosts may affect host–parasite encounter rates and, ultimately, alter zoonotic disease risk through anthropogenic modifications and natural environmental conditions that alter host space use.
... Host competence, or the ability to transmit pathogens, is highly variable across individuals [1][2][3][4]. This variation can alter the persistence and magnitude of disease outbreaks [5][6][7], so understanding its underlying causes is crucial for predicting or mitigating epidemics. ...
... For example, tolerance describes a spectrum of disease phenotypes that reduce the per-pathogen costs of infection on host fitness [10]. Originally studied in animals as the population-level slope between pathogen load and pathology [11], with a shallower slope indicating higher tolerance, recent work has focused on tolerance in individuals, using pre-and during-infection data to calculate individual slopes [2][3][4]12]. Because tolerant individuals experience fewer deleterious impacts of disease, they may contact more susceptible hosts or fomites while infectious. ...
... Because tolerant individuals experience fewer deleterious impacts of disease, they may contact more susceptible hosts or fomites while infectious. As such, more tolerant hosts could be more competent [2,4]. However, because clinical signs often aid transmission (e.g. ...
Individuals can express a range of disease phenotypes during infection, with important implications for epidemics. Tolerance, in particular, is a host response that minimizes the per-pathogen fitness costs of infection. Because tolerant hosts show milder clinical signs and higher survival, despite similar pathogen burdens, their potential for prolonged pathogen shedding may facilitate the spread of pathogens. To test this, we simulated outbreaks of mycoplasmal conjunctivitis in house finches, asking how the speed of transmission varied with tissue-specific and behavioural components of tolerance, milder conjunctivitis and anorexia for a given pathogen load, respectively. Because tissue-specific tolerance hinders pathogen deposition onto bird feeders, important transmission hubs, we predicted it would slow transmission. Because behavioural tolerance should increase interactions with bird feeders, we predicted it would speed transmission. Our findings supported these predictions, suggesting that variation in tolerance could help identify individuals most likely to transmit pathogens.
... As a concept, it integrates the within-host processes involved in host health (e.g., those involved in limiting or eliminating infection) with the between-host processes involved in pathogen transmission (e.g., host-host or host-vector interactions; Gervasi et al. 2015, Martin et al. 2016). If we could predict, a priori, which hosts have high reservoir potential and where these hosts are likely to increase in abundance, we could control and prevent epidemics more effectively (Streicker et al. 2013, Martin et al. 2019. Doing so requires a better, physiological understanding of heterogeneity in reservoir potential, one that links the energetic or life-history trade-offs that shape host defense to the ecological interactions of host communities (Martin et al. 2016, VanderWaal and Ezenwa 2016. ...
... Because of its widespread use in plant ecology and the multiple mechanisms through which it could affect reservoir potential, we used the LES to explore the physiological basis of differences in reservoir potential across plant hosts. Several authors have stressed the importance of considering both among-and within-species variation in reservoir potential (in models of pathogen transmission; Gervasi et al. 2015, Martin et al. 2019) and host traits (in models of community assembly; Roscher et al. 2018, Crawford et al. 2019), but few empirical studies have considered among-and within-species variation in reservoir potential and host traits simultaneously. We factorially manipulated host species (23 plant hosts of a generalist, vector-borne virus) and resource (nitrogen) supply to generate both among-and within-species variation in host traits. ...
... intraspecific variation is included (Gervasi et al. 2015, Roscher et al. 2018, Crawford et al. 2019, Martin et al. 2019, and we found that the LES captured variation in host traits and reservoir potential across host species and resource supply rates simultaneously. ...
Two key knowledge gaps currently limit the development of more predictive and general models of pathogen transmission: (1) the physiological basis of heterogeneity in host contribution to pathogen transmission (reservoir potential) remains poorly understood and (2) a general means of integrating the ecological dynamics of host communities has yet to emerge. If the traits responsible for differences in reservoir potential also modulate host community dynamics, these traits could be used to predict pathogen transmission as host communities change. In two greenhouse experiments, across 23 host species and two levels of resource supply, the reservoir potential of plant hosts increased significantly along the Leaf Economics Spectrum, a global axis of plant physiological trait covariation that features prominently in models of plant community ecology. This indicates that the traits of the Leaf Economics Spectrum underlie broad differences in reservoir potential across host species and resource supplies. Therefore, host traits could be used to integrate epidemiological models of pathogen transmission with ecological models of host community change.
... Steroid hormones, such as corticosterone (CORT), profoundly affect vertebrate immunity and parasite-directed behaviours (Wingfield, 2003;Glaser and Kiecolt-Glaser, 2005;Dhabhar, 2009;Martin, 2009b), but how these and other hormones affect host competence is unclear (Martin and Boruta, 2014;Barron et al., 2015;Martin et al., 2016). Host competence represents the ability of a host to transmit a parasite to another host or vector (Keesing et al., 2010;Han et al., 2015b) and is an amalgamation of (i) risk of exposure to parasites, (ii) host susceptibility upon exposure, (iii) host suitability for parasite replication (including the duration of infectiousness) and (iv) the ability of an infected host to encounter and interact with another host or vector once infected (Luis et al., 2013;Barron et al., 2015;Gervasi et al., 2015;Downs et al., 2019;Martin et al., 2019). The relative lack of study of CORT on host competence is somewhat surprising given that many stressors (Beldomenico and Begon, 2016), anthropogenic and natural, alter CORT regulation and are implicated in the emergence of several diseases (Martin et al., 2010b;Martin and Boruta, 2014;Hassell et al., 2017). ...
... The relative lack of study of CORT on host competence is somewhat surprising given that many stressors (Beldomenico and Begon, 2016), anthropogenic and natural, alter CORT regulation and are implicated in the emergence of several diseases (Martin et al., 2010b;Martin and Boruta, 2014;Hassell et al., 2017). Moreover, epidemiological cycles of parasites are often driven by heterogeneity in, and covariance among, individual host traits (Lloyd-Smith et al., 2005;Bansal et al., 2007;Lloyd-Smith et al., 2009;Hawley and Altizer, 2011;Martin and Al, 2019), some of which arises because of stress (Gervasi et al., 2015;Vazquez-Prokopec et al., 2016). Superspreaders, for instance, are disproportionately responsible for transmitting parasites to other hosts because of their distinct behaviours affecting transmission (Lloyd-Smith et al., 2005;Beldomenico and Begon, 2010;Martin and Al, 2019), but it remains unclear whether stress plays a role in superspreading. ...
... Moreover, epidemiological cycles of parasites are often driven by heterogeneity in, and covariance among, individual host traits (Lloyd-Smith et al., 2005;Bansal et al., 2007;Lloyd-Smith et al., 2009;Hawley and Altizer, 2011;Martin and Al, 2019), some of which arises because of stress (Gervasi et al., 2015;Vazquez-Prokopec et al., 2016). Superspreaders, for instance, are disproportionately responsible for transmitting parasites to other hosts because of their distinct behaviours affecting transmission (Lloyd-Smith et al., 2005;Beldomenico and Begon, 2010;Martin and Al, 2019), but it remains unclear whether stress plays a role in superspreading. Perhaps the best-known human example is Typhoid Mary, an individual thought responsible for 53 cases of Salmonella typhi mortality in humans. ...
statement
Stress hormones affect immune responses, behaviour and other host traits that can influence how individual hosts contribute to disease cycles (i.e. competence). We found that differences in the duration of experimental elevations of one hormone, corticosterone, had very different effects on zebra finch responses to West Nile virus. Chronic elevations enabled birds to become infectious and more tolerant of WNV whereas birds experiencing acute elevations generally resembled untreated controls.
... The ability to effectively transmit pathogens, also known as host competence, varies dramatically among individual animals (Gervasi et al. 2015;Martin et al. 2016;Martin et al. 2019;Burgan et al. 2019). Because such heterogeneity can alter the course of epidemics and epizootics (Lloyd-Smith et al. 2005;Hall, 2019), revealing the host traits underlying this variation is critical to understanding and predicting infectious disease dynamics. ...
... Two key drivers of variation in competence are host resistance, or the ability to kill invading pathogens, and host tolerance, or the ability to maintain fitness during infection without reducing pathogen numbers (Simms 2000;Medzhitov et al. 2012;Råberg 2014;Gervasi et al. 2015;Martin et al. 2016;Burgan et al. 2019;Martin et al. 2019). Resistance will impact competence in at least two predictable ways: reducing the amount of pathogen available for transmission at any given instant and limiting the duration of infection. ...
... Resistance will impact competence in at least two predictable ways: reducing the amount of pathogen available for transmission at any given instant and limiting the duration of infection. In contrast, we know less about how tolerance will impact competence in animals (Martin et al. 2016;Burgan et al. 2019;Martin et al. 2019). Prior work has suggested that because tolerant animals can harbor high pathogen loads while avoiding death and maintaining fitness-enhancing behaviors, these hosts may be particularly likely to both contact and pass pathogens to susceptible individuals (Martin et al. 2016;Burgan et al. 2019;Martin et al. 2019). ...
Host competence, or how well an individual transmits pathogens, varies substantially within and among animal populations. As this variation can alter the course of epidemics and epizootics, revealing its underlying causes will help predict and control the spread of disease. One host trait that could drive heterogeneity in competence is host tolerance, which minimizes fitness losses during infection without decreasing pathogen load. In many cases, tolerance should increase competence by extending infectious periods and enabling behaviors that facilitate contact among hosts. However, we argue that the links between tolerance and competence are more varied. Specifically, the different physiological and behavioral mechanisms by which hosts achieve tolerance should have a range of effects on competence, enhancing the ability to transmit pathogens in some circumstances and impeding it in others. Because tissue-based pathology (damage) that reduces host fitness is often critical for pathogen transmission, we focus on two mechanisms that can underlie tolerance at the tissue level: damage-avoidance and damage-repair. As damage-avoidance reduces transmission-enhancing pathology, this mechanism is likely to decrease host competence and pathogen transmission. In contrast, damage-repair does not prevent transmission-relevant pathology from occurring. Rather, damage-repair provides new, healthy tissues that pathogens can exploit, likely extending the infectious period and increasing host competence. We explore these concepts through graphical models and present three disease systems in which damage-avoidance and damage-repair alter host competence in the predicted directions. Finally, we suggest that by incorporating these links, future theoretical studies could provide new insights into infectious disease dynamics and host-pathogen coevolution.
... Multi-host pathogens cause unprecedented biodiversity loss [6,7], therefore quantifying the distinct roles that species fill during the emergence of infectious disease can improve our understanding of the outcome of outbreaks [8][9][10]. Theoretical models investigating parasites in communities provide a starting point to link within and among host responses [11]. Unfortunately, because most disease emergence events are unpredictable, we have few long-term datasets on host ecology and pathogen surveillance that span epizootic outbreaks, precluding the empirical measurement of the contributions of naive species to community-level disease dynamics. ...
... The pre-epizootic host community included 74 species of amphibians [1,12,14] of which 30 (41% of total amphibian diversity) disappeared following the emergence of Bd in 2004 [14]. Naive and highly diverse communities, such as the El Copé amphibian assemblage, probably consisted of a continuum of host types, ranging from those that increase community vulnerability to pathogens, to those that contribute to community persistence [11,19]. Therefore, this dataset permits us to expand from studies of single species host-pathogen dynamics [20,21] to multispecies assemblages by quantifying speciesspecific contributions at various stages of the epizootic event. ...
Naive multi-host communities include species that may differentially maintain, transmit and amplify novel pathogens; therefore, we expect species to fill distinct roles during infectious disease emergence. Characterizing these roles in wildlife communities is challenging because most disease emergence events are unpredictable. Here, we used field-collected data to investigate how species-specific attributes influenced the degree of exposure, probability of infection, and pathogen intensity, during the emergence of the fungal pathogen Batrachochytrium dendrobatidis ( Bd ) in a highly diverse tropical amphibian community. Our findings confirmed that ecological traits commonly evaluated as correlates of decline were positively associated with infection prevalence and intensity at the species level during the outbreak. We identified key hosts that disproportionally contributed to transmission dynamics in this community and found a signature of phylogenetic history in disease responses associated with increased pathogen exposure via shared life-history traits. Our findings establish a framework that could be applied in conservation efforts to identify key species driving disease dynamics under enzootics before reintroducing amphibians back into their original communities. Reintroductions of supersensitive hosts that are unable to overcome infections will limit the success of conservation programmes by amplifying the disease at the community level.
This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.
... Super spreader is a host individual, population or species that increases the risk of infection for other hosts [11]. ...
... Epidemiologically, infected dispersing classes (e.g. juveniles/subadults and adult females) that migrate between breeding and non-breeding habitats are candidates for super spreading, capable of introducing the pathogens into previously naïve systems (figure 2a; [11]). By contrast, acute cases that are pre-morbid, with the highest tolerance and lowest resistance (i.e. the potential to reach the highest infection loads) likely function as super shedders. ...
Animal defences against infection involve two distinct but complementary mechanisms: tolerance and resistance. Tolerance measures the animal's ability to limit detrimental effects from a given infection, whereas resistance is the ability to limit the intensity of that infection. Tolerance is a valuable defence for highly prevalent, persistent or endemic infections where mitigation strategies based on traditional resistance mechanisms are less effective or evolutionarily stable. Selective breeding of amphibians for enhanced tolerance to Batrachochytrium spp . has been suggested as a strategy for mitigating the impacts of the fungal disease, chytridiomycosis. Here, we define infection tolerance and resistance in the context of chytridiomycosis, present evidence for variation in tolerance to chytridiomycosis, and explore epidemiological, ecological and evolutionary implications of tolerance to chytridiomycosis. We found that exposure risk and environmental moderation of infection burdens are major confounders of resistance and tolerance, chytridiomycosis is primarily characterized by variation in constitutive rather than adaptive resistance, tolerance is epidemiologically important in driving pathogen spread and maintenance, heterogeneity of tolerance leads to ecological trade-offs, and natural selection for resistance and tolerance is likely to be dilute. Improving our understanding of infection tolerance broadens our capacity for mitigating the ongoing impacts of emerging infectious diseases such as chytridiomycosis.
This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.
... Thus, our study, as well as others [20,30,48,49], emphasizes the range of advantages that can be gained by considering multiple aspects of host-pathogen interactions in diversity-disease research. ...
... [16,56,57]), and 'competency' models, which estimate the within-host R 0 in more detail (e.g. [20,30,48,49]. Such an extended view will bridge the theoretical-experimental gaps in diversitydisease research (see [14] for an example). ...
Disentangling the mechanisms that mediate the relationships between species diversity and disease risk has both theoretical and applied implications. We employed a model system of rodents and their Mycoplasma pathogens, in which an extreme negative diversity-disease relationship was demonstrated, to test the assumptions underlying three mechanisms that may explain this field pattern. Through quantifying the long-term dynamics and effects of the pathogen in its three host species, we estimated the between-host differences in pathogen spreading and transmission potentials , and host recovery potential and vulnerability to infection. The results suggest that one of the hosts is a pathogen amplifier and the other two hosts function as diluters. Considering the similarity in infection success and intensity among hosts, and the failure to detect any pathogen-induced damage, we could not validate the assumption underlying the hypotheses that diluters reduce the overall transmission or increase the mortality of infected hosts in the system. Instead, the results demonstrate that diluters clear the infection faster than amplifiers, supporting the possibility that the addition of diluters to the community may reduce the overall number of infected hosts through this mechanism. This study highlights the contribution of experimental studies that simultaneously explore different aspects of host-pathogen interactions in multiple hosts, in diversity-disease research.
... If this non-native parasite of the non-native CTF is indeed detrimental to native treefrogs, then any conservation intervention to reduce the effects of the CTF on native treefrogs would benefit from knowing the traits of the invasive host that produce supershedders of this parasite (Martin et al., 2010(Martin et al., , 2019. Hence, our second objective was to offer insights into the traits of CTFs that might predict their potential for parasite spillover and amplification by quantifying the relationship between the abundance of their parasitic infections (native and introduced) and the size of both male and female CTFs. ...
... In addition to exploring the potential effect that introduced parasites might have on native populations, it is also beneficial to understand how host traits influence the spread or acquisition of parasites, regardless of whether they are introduced or not (Ezenwa et al., 2016;Izhar & Ben-Ami, 2015;Lloyd-Smith et al., 2005;Martin et al., 2019Martin et al., , 2010Viljoen et al., 2011). Deciphering how traits influence parasite dynamics can be particularly useful for exploring how a species may be contributing to parasite spillover, spillback and dilution effects Rohr et al., 2015;Sears et al., 2015;Venesky et al., 2014). ...
Introduced hosts are capable of introducing parasite species and altering the abundance of parasites that are already present in native hosts, but few studies have compared the tolerances of native and invasive hosts to introduced parasites or identified the traits of introduced hosts that make them supershedders of non‐native parasites.
Here, we compare the effects of a nematode Aplectana hamatospicula that is native to Cuba but appears to be introduced to Florida on the native Floridian treefrog, Hyla femoralis, and on the Cuban treefrog (CTF), Osteopilus septentrionalis. We were particularly interested in CTFs because their introduction to Florida has led to reported declines of native treefrogs.
In the laboratory, infection with A. hamatospicula caused a greater loss in body mass of H. femoralis than CTFs despite H. femoralis shedding fewer total worms in their faeces than CTFs. Field collections of CTFs, H. femoralis, and another native Floridian treefrog, H. squirella (Squirrel treefrog) from Tampa, FL also showed that CTFs shed more larval worms in their faeces than both native frogs when controlling for body size. Hence, the non‐native CTF is a supershedder of this non‐native parasite that is spilling over to less tolerant native treefrogs.
Any conservation intervention to reduce the effects of CTFs on native treefrogs would benefit from knowing the traits that contribute to the invasive host being a supershedder of this parasite. Hence, we conducted necropsies on 330 CTFs to determine how host sex and body size affect the abundance of A. hamatospicula, and two other common parasites in this species (acuariid nematodes and trematode metacercariae).
There was a significant linear increase in A. hamatospicula and encysted acuariids with CTF body size, but there was no detectable relationship between host body size and the intensity of metacercariae. Female CTFs were bigger, lived longer and, on average, had more A. hamatospicula than male CTFs.
Synthesis and applications. These results of the study suggest that there is parasite spillover from the invasive Cuban treefrog (CTF) to native treefrogs in Florida. Additionally, at least some of the adverse effects of CTFs on native treefrogs could be caused by the introduction and amplification of this introduced parasite, and female and larger CTFs seem to be amplifying these infections more than males and smaller CTFs, respectively, suggesting that management could benefit from targeting these individuals.
... In multi-species assemblages, intra-and interspecific social contacts likely increase and complexify the interactions between different host and parasite species (Valera et al., 2003;Keesing et al., 2006). High host diversity could decrease infestation risk through dilution effects, as different host species may be differently susceptible and/or competent to different parasite species, but this effect may not always occur and likely depends on specific community compositions (Keesing et al., 2006;Randolph and Dobson, 2012;Civitello et al., 2015;Halsey, 2018;Martin et al., 2019). Mixed-species assemblages may also promote interspecific parasite exchange, especially within generalist parasite species. ...
... The importance of host species identity for ectoparasite ecology has already been described in small mammals (Krasnov et al., 2008;Lareschi and Krasnov, 2010). These results suggest that the four host species vary in their susceptibility (sensu Martin et al., 2019) to different ectoparasite groups (Keesing et al., 2006). Even the prevalence and intensity of Carnus, the most common and broadly considered generalist species (Veiga et al., 2019), varied considerably between hosts. ...
Coloniality in birds is often associated with an increase in parasite burden, but whether the co-occurrence of several host species influences the prevalence and abundance of ectoparasites and their relationship with colony size or density remains poorly known. Here, we studied mixed-species breeding colonies formed after the provision of artificial breeding structures for restoring the lesser kestrel (Falco naumanni) population in Portugal, to investigate the influence of colony traits on ectoparasite infestation. We sampled four groups of ectoparasites (carnid flies, haematophagous mites, louse flies and chewing lice) in four hosts: lesser kestrels, European rollers (Coracias garrulus), feral pigeons (Columba livia) and spotless starlings (Sturnus unicolor). Each host species had a distinct infracommunity of ectoparasites, regardless of colony traits such as size, density or host richness. The abundance of the most common ectoparasite, Carnus hemapterus, was influenced by colony composition – number of nests of each host species – rather than by colony size or density, with its abundance being diluted with increasing numbers of less suitable hosts such as starlings. The increased contact between multiple species of hosts in breeding colonies may complexify host–parasite interactions and challenge our current knowledge on the ecological relationships between host sociality and parasitism.
... Not all hosts are equally likely to be infected and to transmit pathogens, so pathogen prevalence and transmission rates can show high heterogeneity between host species [8,9]. This heterogeneity can be caused by fluctuations in host resistance and tolerance to pathogens [6,10], and by temporal and geographical factors influencing pathogen occurrence [11]. Prevalence and load can also be influenced by host sex, due to sex-specific immune responses [12]. ...
... However, direct evidence relating to the potential for differences in virulence between BFDV lineages remains lacking to date. In many host-pathogen systems, degrees of resistance and tolerance vary between host species [10,59], leading to heterogeneous prevalence and transmission rates of generalist pathogens [6]. A previous study from our group on Crimson Rosellas showed that prevalence and load can differ strongly even between subspecies, despite phylogenetic clustering of BFDV [24]. ...
Pathogens pose a major risk to wild host populations, especially in the face of ongoing biodiversity declines. Beak and feather disease virus (BFDV) can affect most if not all members of one of the largest and most threatened bird orders world-wide, the Psittaciformes. Signs of disease can be severe and mortality rates high. Its broad host range makes it a risk to threatened species in particular, because infection can occur via spill-over from abundant hosts. Despite these risks, surveillance of BFDV in locally abundant wild host species has been lacking. We used qPCR and haemagglutination assays to investigate BFDV prevalence, load and shedding in seven abundant host species in the wild in south-east Australia: Crimson Rosellas (Platycercus elegans), Eastern Rosellas (Platycercus eximius), Galahs (Eolophus roseicapillus), Sulphur-crested Cockatoos (Cacatua galerita), Blue-winged Parrots (Neophema chrysostoma), Rainbow Lorikeets (Trichoglossus moluccanus) and Red-rumped Parrots (Psephotus haematonotus). We found BFDV infection in clinically normal birds in six of the seven species sampled. We focused our analysis on the four most commonly caught species, namely Crimson Rosellas (BFDV prevalence in blood samples: 41.8%), Sulphur-crested Cockatoos (20.0%), Blue-winged Parrots (11.8%) and Galahs (8.8%). Species, but not sex, was a significant predictor for BFDV prevalence and load. 56.1% of BFDV positive individuals were excreting BFDV antigen into their feathers, indicative of active viral replication with shedding. Being BFDV positive in blood samples predicted shedding in Crimson Rosellas. Our study confirms that BFDV is endemic in our study region, and can inform targeted disease management by providing comparative data on interspecies variation in virus prevalence, load and shedding.
... Similarly, Henschen and Adelman (2019) discussed various ways of conceptualizing and measuring tolerance. Whereas ecoimmunology has traditionally focused on host resistance mechanisms that control parasite burden, tolerance has gained attention as an effective and common mechanism by which individuals mitigate the effects of an infection (Knutie et al. 2016;Budischak and Cressler 2018;Burgan et al. 2019;Martin et al. 2019). Henschen and Adelman (2019) highlighted how the effects of tolerance on parasite transmission should vary with the specific mechanisms involved. ...
... Recent work suggests focusing on host tolerance, competence, and resistance as defensive traits rather than on the outcomes of specific immunological assays. Arguably, these organismal traits have the capacity to bring us closest to the phenomena most relevant to disease dynamics at superindividual scales (Gervasi et al. 2015;Martin et al. 2016Martin et al. , 2019Burgan et al. 2019;Downs et al. 2019). Although understanding the cellular-or molecularlevel drivers of immunological variation is clearly important, we appeal that including organismallevel traits in studies of host defense and will become particularly important to interlinking various scales of analysis. ...
The immune system is the primary barrier to parasite infection, replication, and transmission following exposure, and variation in immunity can accordingly manifest in heterogeneity in traits that govern population-level infectious disease dynamics. While much work in ecoimmunology has focused on individual-level determinants of host immune defense (e.g., reproductive status, body condition), an ongoing challenge remains to understand the broader evolutionary and ecological contexts of this variation (e.g., phylogenetic relatedness, landscape heterogeneity) and to connect these differences into epidemiological frameworks. Ultimately, such efforts could illuminate general principles about the drivers of host defense and improve predictions and control of infectious disease. Here, we highlight recent work that synthesizes the complex drivers of immunological variation across biological scales of organization and scales these within-host differences to population-level infection outcomes. Such studies note the limitations involved in making species-level comparisons of immune phenotypes, stress the importance of spatial scale for immunology research, showcase several statistical tools for translating within-host data into epidemiological parameters, and provide theoretical frameworks for linking within-and between-host scales of infection processes. Building from these studies, we highlight several promising avenues for continued work, including the application of machine learning tools and phylogenetically controlled meta-analyses to immunology data and quantifying the joint spatial and temporal dependencies in immune defense using range expansions as model systems. We also emphasizing the use of organismal traits (e.g., host tolerance, competence, resistance) as a way to interlink various scales of analysis. Such continued collaboration and disciplinary cross-talk among ecoimmunology, disease ecology, and mathematical modeling will facilitate an improved understanding of the multi-scale drivers and consequences of variation in host defense.
... Likewise, scientists have long understood that organisms experiencing HIREC might provide valuable basic perspective into evolutionary change [142][143][144] and ecological impact (e.g. zoonosis spillover, extirpation of native populations by pests, etc.) [124,[145][146][147][148]. We agree in both senses, but we also argue strongly that we must reduce our reliance on simplistic approaches (i.e. using one or a few measures of GCs, especially in inert tissues or faeces), and direct attention instead to traits like HPA flexibility and FKBP5 [149]. ...
Hypothalamic–pituitary–adrenal axis (HPA) flexibility is an emerging concept recognizing that individuals that will cope best with stressors will probably be those using their hormones in the most adaptive way. The HPA flexibility concept considers glucocorticoids as molecules that convey information about the environment from the brain to the body so that the organismal phenotype comes to complement prevailing conditions. In this context, FKBP5 protein appears to set the extent to which circulating glucocorticoid concentrations can vary within and across stressors. Thus, FKBP5 expression, and the HPA flexibility it causes, seem to represent an individual's ability to regulate its hormones to orchestrate organismal responses to stressors. As FKBP5 expression can also be easily measured in blood, it could be a worthy target of conservation-oriented research attention. We first review the known and likely roles of HPA flexibility and FKBP5 in wildlife. We then describe putative genetic, environmental and epigenetic causes of variation in HPA flexibility and FKBP5 expression among and within individuals. Finally, we hypothesize how HPA flexibility and FKBP5 expression should affect organismal fitness and hence population viability in response to human-induced rapid environmental changes, particularly urbanization.
This article is part of the theme issue ‘Endocrine responses to environmental variation: conceptual approaches and recent developments’.
... Likewise, scientists have long understood that organisms experiencing HIREC might provide valuable basic perspective into evolutionary change [142][143][144] and ecological impact (e.g. zoonosis spillover, extirpation of native populations by pests, etc.) [124,[145][146][147][148]. We agree in both senses, but we also argue strongly that we must reduce our reliance on simplistic approaches (i.e. using one or a few measures of GCs, especially in inert tissues or faeces), and direct attention instead to traits like HPA flexibility and FKBP5 [149]. ...
Hypothalamic-pituitary-adrenal axis (HPA) flexibility is an emerging concept recognizing that individuals that will cope best with stressors will probably be those using their hormones in the most adaptive way. The HPA flexibility concept considers glucocorticoids as molecules that convey information about the environment from the brain to the body so that the organismal phenotype comes to complement prevailing conditions. In this context, FKBP5 protein appears to set the extent to which circulating glucocorticoid concentrations can vary within and across stressors. Thus, FKBP5 expression, and the HPA flexibility it causes, seem to represent an individual’s ability to regulate its hormones to orchestrate organismal responses to stressors. As FKBP5 expression can also be easily measured in blood, it could be a worthy target of conservation-oriented research attention. We first review the known and likely roles of HPA flexibility and FKBP5 in wildlife. We then describe putative genetic, environmental, and epigenetic causes of variation in HPA flexibility and FKBP5 expression among- and within-individuals. Finally, we hypothesize how HPA flexibility and FKBP5 expression should affect organismal fitness and hence population viability in response to human-induced rapid environmental changes, particularly urbanization.
... More recently, this practical shortcut has been revised due to the recurring observation of a Pareto-type distribution of infectiousness for most individuals. In other words, 20% of individuals tend to cause 80% of infections ( Hawley and Altizer 2011 ;Lively et al. 2014 ;Martin et al. 2019 ). Focusing just on small mammals sampled within NEON (e.g., Read et al. 2018 ;Guralnick et al. 2020 ;McLean and Guralnick 2021 ), one could integrate individual host phenotype, community diversity, and infection type, and burden data to probe how organismal variation affects risk of tick-borne infections (Levels 2-4 in Fig. 2 ; Klarenberg and Wisely 2019 ;Paull et al. 2022 ). ...
Synopsis
Human activities are rapidly changing ecosystems around the world. These changes have widespread implications for the preservation of biodiversity, agricultural productivity, prevalence of zoonotic diseases, and sociopolitical conflict. To understand and improve the predictive capacity for these and other biological phenomena, some scientists are now relying on observatory networks, which are often composed of systems of sensors, teams of field researchers, and databases of abiotic and biotic measurements across multiple temporal and spatial scales. One well-known example is NEON, the US-based National Ecological Observatory Network. Although NEON and similar networks have informed studies of population, community, and ecosystem ecology for years, they have been minimally used by organismal biologists. NEON provides organismal biologists, in particular those interested in NEON's focal taxa, with an unprecedented opportunity to study phenomena such as range expansions, disease epidemics, invasive species colonization, macrophysiology, and other biological processes that fundamentally involve organismal variation. Here, we use NEON as an exemplar of the promise of observatory networks for understanding the causes and consequences of morphological, behavioral, molecular, and physiological variation among individual organisms.
... In addition, the emergence of novel pathogens in naive multihost communities can have differential impacts on species, with some acting as reservoirs and others amplifying transmission [102,103]. However, characterizing the roles of different species in wildlife communities during infectious disease emergence is challenging as these events are often unpredictable. ...
Amphibian populations have been declining worldwide, with global climate changes and infectious diseases being among the primary causes of this scenario. Infectious diseases are among the primary drivers of amphibian declines, including ranavirosis and chytridiomycosis, which have gained more attention lately. While some amphibian populations are led to extinction, others are disease-resistant. Although the host's immune system plays a major role in disease resistance, little is known about the immune mechanisms underlying amphibian disease resistance and host–pathogen interactions. As ectotherms, amphibians are directly subjected to changes in temperature and rainfall, which modulate stress-related physiology, including immunity and pathogen physiology associated with diseases. In this sense, the contexts of stress, disease and ecoimmunology are essential for a better understanding of amphibian immunity. This issue brings details about the ontogeny of the amphibian immune system, including crucial aspects of innate and adaptive immunity and how ontogeny can influence amphibian disease resistance. In addition, the papers in the issue demonstrate an integrated view of the amphibian immune system associated with the influence of stress on immune–endocrine interactions. The collective body of research presented herein can provide valuable insights into the mechanisms underlying disease outcomes in natural populations, particularly in the context of changing environmental conditions. These findings may ultimately enhance our ability to forecast effective conservation strategies for amphibian populations.
This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.
... 'host quality') [1,[10][11][12]. Specifically, higher quality host species are often characterized by fast-growing, poorly defended tissues and short lifespans, [13][14][15][16][17][18][19][20][21][22]; and second, these functional trait values often underlie ecological and evolutionary trade-offs related to host growth and defence, resource acquisition and allocation and survival and reproduction (i.e. life history), resulting in higher levels of host competence (the contribution of a host species to disease transmission) [19,[23][24][25][26][27][28][29][30]. ...
Predicting how climate change will affect disease risk is complicated by the fact that changing environmental conditions can affect disease through direct and indirect effects. Species with fast-paced life-history strategies often amplify disease, and changing climate can modify life-history composition of communities thereby altering disease risk. However, individuals within a species can also respond to changing conditions with intraspecific trait variation. To test the effect of temperature, as well as inter- and intraspecifc trait variation on community disease risk, we measured foliar disease and specific leaf area (SLA; a proxy for life-history strategy) on more than 2500 host (plant) individuals in 199 communities across a 1101 m elevational gradient in southeastern Switzerland. There was no direct effect of increasing temperature on disease. Instead, increasing temperature favoured species with higher SLA, fast-paced life-history strategies. This effect was balanced by intraspecific variation in SLA: on average, host individuals expressed lower SLA with increasing temperature, and this effect was stronger among species adapted to warmer temperatures and lower latitudes. These results demonstrate how impacts of changing temperature on disease may depend on how temperature combines and interacts with host community structure while indicating that evolutionary constraints can determine how these effects are manifested under global change.
This article is part of the theme issue ‘Infectious disease ecology and evolution in a changing world’.
... Superspreading can happen if some hosts are more infectious than others, if some hosts are more exposed to vectors (due to differences in behaviour, e.g. staying outside late, house structure, access to interventions), or because a host is preferentially bitten by more vectors [6,49]. Several biological, demographic and economic factors will determine whether members of a household are considered super-spreaders. ...
Malaria hotspots have been the focus of public health managers for several years due to the potential elimination gains that can be obtained from targeting them. The identification of hotspots must be accompanied by the description of the overall network of stable and unstable hotspots of malaria, especially in medium and low transmission settings where malaria elimination is targeted. Targeting hotspots with malaria control interventions has, so far, not produced expected benefits. In this work we have employed a mechanistic-stochastic algorithm to identify clusters of super-spreader houses and their related stable hotspots by accounting for mosquito flight capabilities and the spatial configuration of malaria infections at the house level. Our results show that the number of super-spreading houses and hotspots is dependent on the spatial configuration of the villages. In addition, super-spreaders are also associated to house characteristics such as livestock and family composition. We found that most of the transmission is associated with winds between 6pm and 10pm although later hours are also important. Mixed mosquito flight (downwind and upwind both with random components) were the most likely movements causing the spread of malaria in two out of the three study areas. Finally, our algorithm (named MALSWOTS) provided an estimate of the speed of malaria infection progression from house to house which was around 200–400 meters per day, a figure coherent with mark-release-recapture studies of Anopheles dispersion. Cross validation using an out-of-sample procedure showed accurate identification of hotspots. Our findings provide a significant contribution towards the identification and development of optimal tools for efficient and effective spatio-temporal targeted malaria interventions over potential hotspot areas.
... For example, exploratory and bold hosts having larger home ranges and moving further from their natal site are more likely to encounter ticks, have high tick burdens and act as super-spreaders of ticks and tick-borne pathogens [39]. These individuals may have a central role in tick-borne pathogen transmission and spread processes [41], and should be considered in theoretical or applied epidemiological models of tick-borne diseases. To properly explore host dispersal, we need to develop spatially explicit and individual-based movement mechanistic models under the general conceptual framework of Nathan et al. [42]. ...
As the incidence of tick-borne diseases has sharply increased over the past decade, with serious consequences for human and animal health, there is a need to identify ecological drivers contributing to heterogeneity in tick-borne disease risk. In particular, the relative importance of animal host dispersal behaviour in its three context-dependent phases of emigration, transfer and settlement is relatively unexplored. We built a spatially explicit agent-based model to investigate how the host dispersal process, in concert with the tick and host demographic processes, habitat fragmentation and the pathogen transmission process, affects infected tick distributions among hosts. A sensitivity analysis explored the impacts of different input parameters on infected tick burdens on hosts and infected tick distributions among hosts. Our simulations indicate that ecological predictors of infected tick burdens differed among the post-egg life stages of ticks, with tick attachment and detachment, tick questing activity and pathogen transmission dynamics identified as key processes, in a coherent way. We also found that the type of host settlement strategy and the proportion of habitat suitable for hosts determined super-spreading of infected ticks. We developed a theoretical mechanistic framework that can serve as a first step towards applied studies of on-the-ground public health intervention strategies.
... While these examples are all in a single host species, Homo sapiens (although both SARS-CoV-2 and S. enterica can infect multiple host species [8,9]), super-spreading can also occur between host species as most viruses readily circulate between host species, which often hampers virus eradication [10]. Differences in defense mechanisms between host species may result in one species coping better with infections than others and/or transmitting a disproportional amount of pathogens [11]. For bee viruses, studies on viral defense strategies on individual level scarce are mostly investigated in conjunction with other factors, such as nutrition or pesticide exposure, which complicates the interpretation of 'pure' viral tolerance or resistance [12][13][14]. ...
Bees, both wild and domesticated ones, are hosts to a plethora of viruses, with most of them infecting a wide range of bee species and genera. Although viral discovery and research on bee viruses date back over 50 years, the last decade is marked by a surge of new studies, new virus discoveries, and reports on viral transmission in and between bee species. This steep increase in research on bee viruses was mainly initiated by the global reports on honeybee colony losses and the worldwide wild bee decline, where viruses are regarded as one of the main drivers. While the knowledge gained on bee viruses has significantly progressed in a short amount of time, we believe that integration of host defense strategies and their effect on viral dynamics in the multi-host viral landscape are important aspects that are currently still missing. With the large epidemiological dataset generated over the last two years on the SARS-CoV-2 pandemic, the role of these defense mechanisms in shaping viral dynamics has become eminent. Integration of these dynamics in a multi-host system would not only greatly aid the understanding of viral dynamics as a driver of wild bee decline, but we believe bee pollinators and their viruses provide an ideal system to study the multi-host viruses and their epidemiology.
... The activity of the exoribonuclease might differ in different hosts, modulating the level of sequence variation. Replication in different host species may therefore present heterogeneities in their sequence variation, which may influence the emergence of new variants 16,20,[74][75][76] . ...
In the past two decades, three coronaviruses with ancestral origins in bats have emerged and caused widespread outbreaks in humans, including severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Since the first SARS epidemic in 2002–2003, the appreciation of bats as key hosts of zoonotic coronaviruses has advanced rapidly. More than 4,000 coronavirus sequences from 14 bat families have been identified, yet the true diversity of bat coronaviruses is probably much greater. Given that bats are the likely evolutionary source for several human coronaviruses, including strains that cause mild upper respiratory tract disease, their role in historic and future pandemics requires ongoing investigation. We review and integrate information on bat–coronavirus interactions at the molecular, tissue, host and population levels. We identify critical gaps in knowledge of bat coronaviruses, which relate to spillover and pandemic risk, including the pathways to zoonotic spillover, the infection dynamics within bat reservoir hosts, the role of prior adaptation in intermediate hosts for zoonotic transmission and the viral genotypes or traits that predict zoonotic capacity and pandemic potential. Filling these knowledge gaps may help prevent the next pandemic. Bats harbour a multitude of coronaviruses and owing to their diversity and wide distribution are prime reservoir hosts of emerging viruses. Ruiz-Aravena, McKee and colleagues analyse the currently available information on bat coronaviruses and discuss their role in recent and potential future spillovers.
... At the beginning of this century, 75% of emerging pathogens in humans were estimated to be zoonotic and 77% of livestock pathogens could be transmitted between different host species (Cleaveland et al., 2001). Estimating the relative role different species play in sustaining or amplifying pathogen spread is fundamental for designing control strategies (Hollingsworth et al., 2015;Buhnerkempe et al., 2015;Lloyd-Smith et al., 2015;Webster et al., 2017), yet is hampered by an incomplete understanding of the host(-vector)-pathogen interactions that underlie the spread of these pathogens (Roche et al., 2013;Vazquez-Prokopec et al., 2016;Fenton et al., 2015;Martin et al., 2019). ...
Rift Valley fever (RVF) is a viral, vector-borne, zoonotic disease. The relative contributions of livestock species to RVFV transmission has not been previously quantified. To estimate their potential to transmit the virus over the course of their infection, we 1) fitted a within-host model to viral RNA and infectious virus measures, obtained daily from infected lambs, calves, and young goats, 2) estimated the relationship between vertebrate host infectious titers and probability to infect mosquitoes, and 3) estimated the net infectiousness of each host species over the duration of their infectious periods, taking into account different survival outcomes for lambs. Our results indicate that the efficiency of viral replication, along with the lifespan of infectious particles, could be sources of heterogeneity between hosts. For similar infectious titers, we found that infection rates in Aedes spp. vectors were significantly higher than in Culex spp. vectors. Consequently, for Aedes infections, we estimated the net infectiousness of lambs to be 2.93 (median) and 3.65 times higher than that of calves and goats, respectively. Among lambs, individuals which eventually died from the infection were 1.93 times more infectious than lambs recovering. Beyond infectiousness, the relative contributions of host species to transmission depend on local ecological factors, including relative abundances and vector host-feeding preferences. Quantifying these contributions will ultimately help design efficient, targeted, surveillance and vaccination strategies.
... Although the causal link is absent, large populations of reservoir animals harboring large pathogen populations have been predicted to serve as fertile sources of zoonotic diseases (Han et al., 2016). Also, the role of reduced inflammation and disease tolerance in maintaining such persistent zoonotic pathogen populations in reservoir species has already been implicated (Pavlovich et al., 2018;Martin et al., 2019), but how it can boost transmission and spillover is relatively unclear. ...
Researchers worldwide are repeatedly warning us against future zoonotic diseases resulting from humankind’s insurgence into natural ecosystems. The same zoonotic pathogens that cause severe infections in a human host frequently fail to produce any disease outcome in their natural hosts. What precise features of the immune system enable natural reservoirs to carry these pathogens so efficiently? To understand these effects, we highlight the importance of tracing the evolutionary basis of pathogen tolerance in reservoir hosts, while drawing implications from their diverse physiological and life-history traits, and ecological contexts of host-pathogen interactions. Long-term co-evolution might allow reservoir hosts to modulate immunity and evolve tolerance to zoonotic pathogens, increasing their circulation and infectious period. Such processes can also create a genetically diverse pathogen pool by allowing more mutations and genetic exchanges between circulating strains, thereby harboring rare alive-on-arrival variants with extended infectivity to new hosts (i.e., spillover). Finally, we end by underscoring the indispensability of a large multidisciplinary empirical framework to explore the proposed link between evolved tolerance, pathogen prevalence, and spillover in the wild.
... For example, when flowering does not occur or flowering trees are removed, nomadic nectivorous bats become resident frugivores in urban areas to reduce the energetic cost of foraging [45][46][47]. The risk of spillover from these populations is high because they have regular contact with humans and are energetically stressed and more likely to shed virus [48]. As an illustration, in response to the loss of winter habitat, Australian flying foxes rapidly relocated to urban and agricultural areas coincident with the emergence of Hendra virus [34]. ...
Pandemics are a consequence of a series of processes that span scales from viral biology at 10−9 m to global transmission at 106 m. The pathogen passes from one host species to another through a sequence of events that starts with an infected reservoir host and entails interspecific contact, innate immune responses, receptor protein structure within the potential host, and the global spread of the novel pathogen through the naive host population. Each event presents a potential barrier to the onward passage of the virus and should be characterized with an integrated transdisciplinary approach. Epidemic control is based on the prevention of exposure, infection, and disease. However, the ultimate pandemic prevention is prevention of the spillover event itself. Here, we focus on the potential for preventing the spillover of henipaviruses, a group of viruses derived from bats that frequently cross species barriers, incur high human mortality, and are transmitted among humans via stuttering chains. We outline the transdisciplinary approach needed to prevent the spillover process and, therefore, future pandemics.
... We then compared the likelihood that a worker bumble bee is infected with one of the three most common bumble bee parasites in these open and closed colonies, before and after placement in their environments for 30 days. For the second premise, we tested whether managed bumble bees act as parasite spreaders rather than dilutors, a concept known as a "parasite sink" (Martin et al., 2019). Managed bumble bees act as a parasite sink if they acquire parasites from their environment but reduce the risk of passing the infection back to wild bees. ...
The use of commercially reared bumble bees in agricultural environments has been recognized as a potential threat to wild pollinators due to competition, genetic contamination, and most notably, disease transmission. Higher parasite prevalence near greenhouses where managed bumble bees are used has been linked to parasite spillover from managed to wild bees. However, pathogen transmission is not unidirectional, and can also flow from wild to managed bees. These newly infected managed bees can subsequently re-infect (other) wild bees, in a process known as spillback, which is an alternative explanation for the increased parasite prevalence near greenhouses. Reducing parasite prevalence in managed bees is key to controlling host-parasite dynamics in cases of spillover; in spillback, producing managed bees that are resilient to infection is important. Here we establish that the managed bumble bee Bombus terrestris can acquire parasites from their foraging environment, which is the major infection route for Apicystis spp. and Crithidia spp., but not for Nosema spp.. Managed B. terrestris were found to have a higher prevalence of Crithdia and a higher load of Apicystis than local wild conspecifics, showing that for these parasites, spillback is a possible risk scenario.
... For example, eavesdropping has been shown to facilitate tritrophic interactions in aquatic communities. Plants released oxylipins and other VOCs as they were being consumed by herbivores, which attracted carnivores and parasitoids that subsequently reduced herbivore performance (Martin et al., 2019;Kergunteuil et al., 2020). ...
Chemical communication within an aquatic environment creates an intricate signaling web that provides species with information about their surroundings. Signaling molecules, like oxylipins, mediate a multitude of interactions between free-living members of a community including non-consumptive effects by predators. Parasites are another source of signaling molecules in aquatic communities and contribute directly by synthesizing them or indirectly by manipulating host chemical cues. If chemical cues of infected hosts are altered, then non-consumptive interactions between other members of the community may also be affected. Different cues from infected hosts may alter behaviors in other individuals related to foraging, competition, and defense priming. Here, we discuss how parasites could modify host chemical cues, which may have far reaching consequences for other community members and the ecosystem. We discuss how the modification of signaling molecules by parasites may also represent a mechanism for parasite-modified behavior within some systems and provide a mechanism for non-consumptive effects of parasites. Further, we propose a host-parasite system that could be used to investigate some key, unanswered questions regarding the relationship between chemical cues, parasite-modified behavior, and non-consumptive effects. We explain how trematode-gastropod systems can be used to test whether there are alterations in the diversity and amounts of signaling molecules available, and if habitat use, immune function, and behavior of other individuals and species are affected. Finally, we argue that changes to pathway crosstalk by parasites within communities may have broad ecological implications.
... Another property emerging from parasite overdispersion is the effect on parasite transmission. The small fraction of heavily infected individuals may act as super-spreaders, playing a large role in disease transmission [13][14][15]. In many host-parasite systems, 20% of hosts are responsible for 80% of new infections [16,17]. ...
A pervasive characteristic of parasite infections is their tendency to be overdispersed. Understanding the mechanisms underlying this overdispersed distribution is of key importance as it may impact the transmission dynamics of the pathogen. Although multiple factors ranging from environmental stochasticity to inter-individual heterogeneity may explain parasite overdispersion, parasite infection is also overdispersed in an inbred host population maintained under laboratory conditions, suggesting that other mechanisms are at play. Here, we show that the aggregated distribution of malaria parasites within mosquito vectors is partially explained by a temporal heterogeneity in parasite infectivity triggered by the bites of mosquitoes. Parasite transmission tripled between the mosquito's first and last blood feed in a period of only 3 h. Surprisingly, the increase in transmission is not associated with an increase in parasite investment in production of the transmissible stage. Overall, we highlight that Plasmodium is capable of responding to the bites of mosquitoes to increase its own transmission at a much faster pace than initially thought and that this is partly responsible for overdispersed distribution of infection. We discuss the underlying mechanisms as well as the broader implications of this plastic response for the epidemiology of malaria.
... Another property emerging from parasite overdispersion is the effect on parasite transmission. The small fraction of heavily infected individuals may act as super-spreaders, playing a large role in disease transmission [13][14][15]. In many host-parasite systems, 20% of hosts are responsible for 80% of new infections [16,17]. ...
A pervasive characteristic of parasite infections is their tendency to be overdispersed. Understanding the mechanisms underlying this overdispersed distribution is of key importance as it may impact the transmission dynamics of the pathogen. Although multiple factors ranging from environmental stochasticity to inter-individual heterogeneity may explain parasite overdispersion, parasite infection is also overdispersed in an inbred host population maintained under laboratory conditions, suggesting that other mechanisms are at play. Here, we show that the aggregated distribution of malaria parasites within mosquito vectors is partially explained by a temporal heterogeneity in parasite infectivity triggered by the bites of mosquitoes. Parasite transmission tripled between the mosquito's first and last blood feed in a period of only 3 h. Surprisingly, the increase in transmission is not associated with an increase in parasite investment in production of the transmissible stage. Overall, we highlight that Plasmodium is capable of responding to the bites of mosquitoes to increase its own transmission at a much faster pace than initially thought and that this is partly responsible for overdispersed distribution of infection. We discuss the underlying mechanisms as well as the broader implications of this plastic response for the epidemiology of malaria.
... While many studies focus on measuring the diversity of host species in the context of disease, the structure of host communities can also be measured in the context of disease using characteristics of host species or host functional traits (Johnson et al., 2013;Kirk et al., 2019), resulting in trait-based measures of host community competence (Stewart Merrill and Johnson, 2020). This approach, which has rapidly gained traction in disease ecology, suggests that host species that are the best able to spread diseases (i.e., the most competent hosts), often share particular suites of physiological traits (Huang et al., 2013;Martin et al., 2019;Becker and Han, 2020). Thus, host community competence can be linked to distributions of important host traits across host communities (Johnson et al., 2015b;Liu et al., 2017). ...
The dilution effect predicts increasing biodiversity to reduce the risk of infection, but the generality of this effect remains unresolved. Because biodiversity loss generates predictable changes in host community competence, we hypothesised that biodiversity loss might drive the dilution effect. We tested this hypothesis by reanalysing four previously published meta-analyses that came to contradictory conclusions regarding generality of the dilution effect. In the context of biodiversity loss, our analyses revealed a unifying pattern: dilution effects were inconsistently observed for natural biodiversity gradients, but were commonly observed for biodiversity gradients generated by disturbances causing losses of biodiversity. Incorporating biodiversity loss into tests of generality of the dilution effect further indicated that scale-dependency may strengthen the dilution effect only when biodiversity gradients are driven by biodiversity loss. Together, these results help to resolve one of the most contentious issues in disease ecology: the generality of the dilution effect.
... For example, intraspecific variation in foraging traits of single consumer species can change abundance dynamics of prey across multiple trophic levels in food webs, with the effect often being comparable to, and sometimes stronger than, adding new consumer species (Des Roches et al., 2018). Similarly, because vector-vector, host-vector and vector-pathogen interactions are non-linear, even small within-population and over-time variation in vector traits can have significant impacts on disease dynamics due to compounding effects (Lloyd-Smith et al., 2005;Martin et al., 2019). Furthermore, the traits of ectotherms vary directly and non-linearly with fluctuations in environmental conditions. ...
Many important endemic and emerging diseases are transmitted by vectors that are biting arthropods. The functional traits of vectors can affect pathogen transmission rates directly and also through their effect on vector population dynamics. Increasing empirical evidence shows that vector traits vary significantly across individuals, populations, and environmental conditions, and at time scales relevant to disease transmission dynamics. Here, we review empirical evidence for variation in vector traits and how this trait variation is currently incorporated into mathematical models of vector-borne disease transmission. We argue that mechanistically incorporating trait variation into these models, by explicitly capturing its effects on vector fitness and abundance, can improve the reliability of their predictions in a changing world. We provide a conceptual framework for incorporating trait variation into vector-borne disease transmission models, and highlight key empirical and theoretical challenges. This framework provides a means to conceptualize how traits can be incorporated in vector borne disease systems, and identifies key areas in which trait variation can be explored. Determining when and to what extent it is important to incorporate trait variation into vector borne disease models remains an important, outstanding question.
... This trend matches what previous studies have found with bolder tadpoles experiencing increased infection intensity with parasites [28,29]. Although a trend between host personality and Bd infection has not yet been identified at any amphibian life stage, if the same traits underlie the acquisition of both defensive bacteria and the pathogens against which they confer protection, these highly 'competent' individuals may play a crucial role in disease dynamics at the population level [39,40]. Further, we expect that the proportion of time that tadpoles spend in the open (i.e. ...
Individual differences in host phenotypes can generate heterogeneity in the acquisition and transmission of microbes. Although this has become a prominent factor of disease epidemiology, host phenotypic variation might similarly underlie the transmission of microbial symbionts that defend against pathogen infection. Here, we test whether host body size and behaviour influence the social acquisition of a skin bacterium, Janthinobacterium lividum, which in some hosts can confer protection against infection by Batrachochytrium dendrobatidis, the causative agent of the amphibian skin disease chytridiomycosis. We measured body size and boldness (time spent in an open field) of green frog tadpoles and haphazardly constructed groups of six individuals. In some groups, we exposed one individual in each group to J. lividum and, in other groups, we inoculated a patch of aquarium pebbles to J. lividum. After 24 h, we swabbed each individual to estimate the presence of J. lividum on their skin. On average, tadpoles acquired nearly four times more bacteria when housed with an exposed individual compared to those housed with a patch of inoculated substrate. When tadpoles were housed with an exposed group-mate, larger and 'bolder' individuals acquired more bacteria. These data suggest that phenotypically biased acquisition of defensive symbionts might generate biased patterns of mortality from the pathogens against which they protect.
... Our likelihood function may favour excessively short cycles of acute and latent infection because these can provide a wide range of probable serological transition times. Although experimental infection studies have failed to provide reliable data on the patterns and duration of henipavirus shedding [6], our results indicate that acute -latent infection cycles are able to reflect naturally observed variation in serological transition times ( perhaps reflecting individual heterogeneity [40] or dose-dependency [41] in immune responses). ...
Pathogen circulation among reservoir hosts is a precondition for zoonotic spillover. Unlike the acute, high morbidity infections typical in spillover hosts, infected reservoir hosts often exhibit low morbidity and mortality. Although it has been proposed that reservoir host infections may be persistent with recurrent episodes of shedding, direct evidence is often lacking. We construct a generalized SEIR (susceptible, exposed, infectious, recovered) framework encompassing 46 sub-models representing the full range of possible transitions among those four states of infection and immunity. We then use likelihood-based methods to fit these models to nine years of longitudinal data on henipavirus serology from a captive colony of Eidolon helvum bats in Ghana. We find that reinfection is necessary to explain observed dynamics; that acute infectious periods may be very short (hours to days); that immunity, if present, lasts about 1–2 years; and that recurring latent infection is likely. Although quantitative inference is sensitive to assumptions about serology, qualitative predictions are robust. Our novel approach helps clarify mechanisms of viral persistence and circulation in wild bats, including estimated ranges for key parameters such as the basic reproduction number and the duration of the infectious period. Our results inform how future field-based and experimental work could differentiate the processes of viral recurrence and reinfection in reservoir hosts.
This article is part of the theme issue ‘Dynamic and integrative approaches to understanding pathogen spillover’.
Geographic variation in host immunity could have major influences on disease dynamics, including zoonotic forms that affect humans. Such variation in immunity could be driven by variation in climate, either directly or, more likely, indirectly via resource availability. We compared the immune gene expression of wild Peromyscus leucopus mice, the primary reservoir for the bacterium that causes Lyme disease, Borrelia burgdorferi, among eight sites spanning 1,400 km of the northeastern United States. We discovered that climate conditions at sites strongly predicted immunity to the most common zoonotic pathogen in the U.S.: mice from warmer, wetter sites were more prepared to resist B. burgdorferi infections. Our results reveal a novel pathway by which climate change could affect pathogen spillover or zoonotic epidemics generally.
Amphibians face many challenges in their conservation, including threats from emerging infectious pathogens/parasites and habitat degradation. In diverse amphibian communities, where multiple emerging pathogens tend to co-occur, we know little about how the structural partitioning of host specificity impacts population maintenance despite disease. Here, we used field data from amphibian communities in north Florida to investigate host-specific traits influencing the prevalence, intensity, and transmission of three emerging pathogens of amphibians: Batrachochytrium dendrobatidis (Bd), Perkinsea (Pr), and Ranavirus (Rv). We found that Bd exhibited specificity for later developmental stages, and that overall infection patterns differed between ephemeral and semi-permanent sites and across seasons. For each pathogen, we identified key hosts overwhelmingly contributing to community transmission dynamics and found evidence of pathogen interactions that may facilitate Bd-Rv co-infections, and dilution effects of increased host diversity on Pr infection. Our findings confirmed that declining species within the region are routinely infected with emerging pathogens. However, the probability of infection depended on different habitat characteristics and associated host community composition. Thus, our study emphasizes the importance of identifying key and sensitive hosts that drive or succumb to infections in natural communities before reintroducing amphibians into the wild. This approach can help improve conservation efforts in diverse host communities as successful repatriation of sensitive species can benefit from detailed characterization of the established disease dynamics at the release site.
Seasonal variation in habitat use and animal behavior can alter host contact patterns with potential consequences for pathogen transmission dynamics. The endangered Florida panther (Puma concolor coryi) has experienced significant pathogen-induced mortality and continues to be at risk of future epidemics. Prior research has found increased panther movement in Florida’s dry versus wet seasons, which may affect panther population connectivity and seasonally increase potential pathogen transmission. Our objective was to determine if Florida panthers are more spatially connected in dry seasons relative to wet seasons, and test if identified connectivity differences resulted in divergent predicted epidemic dynamics. We leveraged extensive panther telemetry data to construct seasonal panther home range overlap networks over an 11 year period. We tested for differences in network connectivity, and used observed network characteristics to simulate transmission of a broad range of pathogens through dry and wet season networks. We found that panthers were more spatially connected in dry seasons than wet seasons. Further, these differences resulted in a trend toward larger and longer pathogen outbreaks when epidemics were initiated in the dry season. Our results demonstrate that seasonal variation in behavioral patterns—even among largely solitary species—can have substantial impacts on epidemic dynamics.
Seasonality in infectious disease prevalence is predominantly attributed to changes in exogenous risk factors. For vectored pathogens, high abundance, activity, and/or diversity of vectors can exacerbate disease risk for hosts. Conversely, many host defenses, particularly immune responses, are seasonally variable. Seasonality in host defenses has been attributed, in part, to the proximate (i.e., metabolic) and ultimate (i.e., reproductive fitness) costs of defense. In this study, our goal was to discern whether any seasonality is observable in how a common avian host, the house sparrow (Passer domesticus), copes with a common zoonotic arbovirus, the West Nile virus (WNV), when hosts are studied under controlled conditions. We hypothesized that if host biorhythms play a role in vector-borne disease seasonality, birds would be most vulnerable to WNV when breeding and/or molting (i.e., when other costly physiological activities are underway) and thus most transmissive of WNV at these times of year (unless birds died from infection). Overall, the results only partly supported our hypothesis. Birds were most transmissive of WNV in fall (after their molt is complete and when WNV is most prevalent in the environment), but WNV resistance, WNV tolerance, and WNV-dependent mortality did not vary among seasons. These results collectively imply that natural arboviral cycles could be partially underpinned by endogenous physiological changes in hosts. However, other disease systems warrant study, as this result could be specific to the nonnative and highly commensal nature of the house sparrow or a consequence of the relative recency of the arrival of WNV to the United States.
Individual animals vary greatly in their responses to infection, either killing off the invading pathogen (resistance) or minimizing the per-pathogen costs of infection on host fitness (tolerance). Though we understand little about the physiological drivers of tolerance in wild animals, phenotypically, it manifests as milder clinical signs of disease. Here, we use a well-described disease system, finch mycoplasmosis, to evaluate the role of inflammation in disease tolerance. House finches (Haemorhous mexicanus) infected with the bacterial pathogen Mycoplasma gallisepticum (MG) develop conjunctival pathology that satisfies the cardinal signs of inflammation. We report on a captive trial performed in 2016 and replicated in 2018 that tested whether chemotherapeutics, specifically nonsteroidal anti-inflammatory drugs (NSAIDs), can reduce lesion severity, thus pushing individuals toward more tolerant phenotypes. Though birds treated with NSAIDs in the first trial developed milder pathology per unit pathogen load, we found no effect of treatment in the second trial, perhaps due to natural variation in baseline tolerance within the source population across years. Second-trial control birds developed markedly milder pathology than first-year controls, suggesting that the effect of trial swamped the effect of treatment in this study. Moving forward, using birds from a population in which the disease is absent or only recently emerged-and so tolerance has not yet been selected for-may better elucidate the role of pro-inflammatory mediators in disease tolerance.
Quantifying the variation of pathogens’ life history traits in multiple host systems is crucial to understand their transmission dynamics. It is particularly important for arthropod-borne viruses (arboviruses), which are prone to infecting several species of vertebrate hosts. Here, we focus on how host-pathogen interactions determine the ability of host species to transmit a virus to susceptible vectors upon a potentially infectious contact. Rift Valley fever (RVF) is a viral, vector-borne, zoonotic disease, chosen as a case study. The relative contributions of livestock species to RVFV transmission has not been previously quantified. To estimate their potential to transmit the virus over the course of their infection, we 1) fitted a within-host model to viral RNA and infectious virus measures, obtained daily from infected lambs, calves, and young goats, 2) estimated the relationship between vertebrate host infectious titers and probability to infect mosquitoes, and 3) estimated the net infectiousness of each host species over the duration of their infectious periods, taking into account different survival outcomes for lambs. Our results indicate that the efficiency of viral replication, along with the lifespan of infectious particles, could be sources of heterogeneity between hosts. Given available data on RVFV competent vectors, we found that, for similar infectious titers, infection rates in the Aedes genus were on average higher than in the Culex genus. Consequently, for Aedes-mediated infections, we estimated the net infectiousness of lambs to be 2.93 (median) and 3.65 times higher than that of calves and goats, respectively. In lambs, we estimated the overall infectiousness to be 1.93 times higher in individuals which eventually died from the infection than in those recovering. Beyond infectiousness, the relative contributions of host species to transmission depend on local ecological factors, including relative abundances and vector host-feeding preferences. Quantifying these contributions will ultimately help design efficient, targeted, surveillance and vaccination strategies.
Exposure and susceptibility underlie every organism's infection status, and an untold diversity of factors can drive variation in both. Often, both exposure and susceptibility change in response to a given factor, and they can interact, such that their relative contributions to observed disease dynamics are obscured. These independent and interlinked changes often complicate empirical inference in disease ecology and ecoimmunology.
Although many disease ecology studies address this problem, it is often implicit rather than explicit and requires a specific set of tools to tackle. Moreover, as yet, there is no established conceptual framework for disentangling susceptibility and exposure processes.
Here, we consolidate previous theory and empirical understanding regarding the entwined effects of susceptibility and exposure, which we refer to as ‘the Twin Pillar Problem’. We provide a framework for conceptualising exposure–susceptibility interactions, where they obscure, confound, induce or counteract one another, providing some well‐known examples for each complicating mechanism.
We synthesise guidelines for anticipating and controlling for covariance between exposure and susceptibility, and we detail statistical and operational methodology that researchers have employed to deal with them. Finally, we discuss novel emerging frontiers in their study in ecology, and their potential for further integration in the fields of wildlife and human health.
Read the free Plain Language Summary for this article on the Journal blog.
Tuberculosis (TB) is an increasing threat to wildlife, yet tracking its spread is challenging because infections often appear to be asymptomatic, and diagnostic tools such as blood tests can be invasive and resource intensive. Our understanding of TB biology in wildlife is therefore limited to a small number of well-studied species. Testing of fecal samples using PCR is a noninvasive method that has been used to detect Mycobacterium bovis shedding amongst badgers, yet its utility more broadly for TB monitoring in wildlife is unclear. We combined observation data of clinical signs with PCR testing of 388 fecal samples to characterize longitudinal dynamics of TB progression in 66 wild meerkats (Suricata suricatta) socially exposed to Mycobacterium suricattae between 2000 and 2018. Our specific objectives were 1) to test whether meerkat fecal samples can be used to monitor TB; 2) to characterize TB progression between three infection states (PCR-negative exposed, PCR-positive asymptomatic, and PCR positive with clinical signs); and 3) estimate individual heterogeneity in TB susceptibility, defined here as the time between TB exposure and detection, and survival after TB detection. We found that the TB detection probability once meerkats developed clinical signs was 13% (95% confidence interval 3-46%). Nevertheless, with an adapted test protocol of 10 PCR replicates per sample we detected hidden TB infections in 59% of meerkats before the onset of clinical signs. Meerkats became PCR positive approximately 14 mo after initial exposure, developed clinical signs approximately 1 yr after becoming PCR positive, and died within 5 mo of developing clinical signs. Individual variation in disease progression was high, with meerkats developing clinical signs from immediately after exposure to 3.4 yr later. Overall, our study generates novel insights into wildlife TB progression, and may help guide adapted management strategies for TB-susceptible wildlife populations.
Natural herbivore populations have experienced uninterrupted pressures from direct and evident domestic-wildlife interactions and competition, to indirect or less obvious ones such as pathogen transmission. Thus, pathogen spillover between wild and domestic animals is a constant concern because the domestic-wildlife interface represents the ecological frontier in which pathogen transmission takes place in both directions. In Patagonian steppe communities, extensive sheep ranching, and guanaco (Lama guanicoe) populations coexist, and guanaco have shown to be infected by pathogens such as Mycobacterium avium subspecies paratuberculosis (MAP) likely transmitted from livestock. MAP causes chronic enteritis and affects mostly domestic ruminants. We evaluated MAP prevalence and pathogen shedding in both species’ faeces collected in non-shared and shared sites according to presence/absence of sheep and guanaco along a year, in four different seasons (autumn, winter, and spring 2018, and summer 2019). Our results indicate that MAP circulates in both sheep and guanaco populations with self-sustained transmission, however both species differ in their levels of competence. We detected higher pathogen shedding in sites occupied by sheep, suggesting that sheep populations may be the main source of infection for susceptible animals due to their large numbers which drive MAP dynamics.
This article is protected by copyright. All rights reserved
Host competence, defined as the likelihood that a host will transmit infection, may be affected by an individual's resistance to infection and its ability to withstand damage caused by infection (tolerance). Host competence may therefore be one of the most important factors to impact host–parasite dynamics, yet the relationships among resistance, tolerance and competence are poorly understood. The objective of the present study was to determine whether individual host resistance (ability to resist or minimize infection) and/or tolerance (ability to withstand or minimize reduction in fitness due to infection) contributed to the competence (ability to spread infection) of hosts using guppies infected with the ectoparasite, Gyrodactylus turnbulli. This individual-fish level analysis used data collected from a previous metapopulation experiment that had tracked host–parasite dynamics at the metapopulation scale using individually marked guppies that were moved among experimental tanks within replicate metapopulations. Fish tolerance was measured as the residual from a fish's expected survival post-infection for a given parasite burden. Fish resistance was measured as the peak parasite load (– log-transformed). Host competence was measured as the incidence (number of new infections over two days after the arrival of a fish to a tank) weighted by the density of available uninfected fish in the tank. In contrast to the assumption of a trade-off between resistance and tolerance, individual fish tolerance and resistance were both negatively associated with competence. Connectivity (the number of fish with which an individual came into contact) was not associated with competence. Our results indicate that resistance and tolerance are both important to disease spread. These findings highlight the importance of understanding how individual defence against parasites may contribute to its competence as a host, and therefore impact metapopulation-level dynamics.
Quantifying the relative impact of environmental conditions and host community structure on disease is one of the greatest challenges of the 21 st century, as both climate and biodiversity are changing at unprecedented rates. Both increasing temperature and shifting host communities towards more fast-paced life-history strategies are predicted to increase disease, yet their independent and interactive effects on disease in natural communities remains unknown. Here, we address this challenge by surveying foliar disease symptoms in 220, 0.5 meter-diameter herbaceous plant communities along a 1100-meter elevational gradient. We find that increasing temperature associated with lower elevation can increase disease by (1) relaxing constraints on parasite growth and reproduction, (2) determining which host species are present in a given location, and (3) strengthening the positive effect of host community pace-of-life on disease. These results provide the first field evidence, under natural conditions, that environmental gradients can alter how host community structure affects disease.
Predicting disease risk in an era of unprecedented biodiversity and climate change is more challenging than ever, largely because when and where hosts are at greatest risk of becoming infected depends on complex relationships between hosts, parasites, and the environment. Theory predicts that host species characterized by fast-paced life-history strategies are more susceptible to infection and contribute more to transmission than their slow-paced counterparts. Hence, disease risk should increase as host community structure becomes increasingly dominated by fast-paced hosts. Theory also suggests that environmental gradients can alter disease risk, both directly, due to abiotic constraints on parasite replication and growth, and indirectly, by changing host community structure. What is more poorly understood, however, is whether environmental gradients can also alter the effect of host community structure on disease risk. We addressed these questions using a detailed survey of host communities and infection severity along a 1100m elevational gradient in southeastern Switzerland. Consistent with prior studies, increasing elevation directly reduced infection severity, which we attribute to abiotic constraints, and indirectly reduced infection severity via changes in host richness, which we attribute to encounter reduction. Communities dominated by fast pace-of-life hosts also experienced more disease. Finally, although elevation did not directly influence host community pace-of-life, the relationship between pace-of-life and disease was sensitive to elevation: increasing elevation weakened the relationship between host community pace-of-life and infection severity. This result provides the first field evidence, to our knowledge, that an environmental gradient can alter the effect of host community structure on infection severity.
Parasite transmission is thought to depend on both parasite exposure and host susceptibility to infection; however, the relative contribution of these two factors to epidemics remains unclear. We used interactions between an aquatic host and its fungal parasite to evaluate how parasite exposure and host susceptibility interact to drive epidemics. In six lakes, we tracked the following factors from pre‐epidemic to epidemic emergence: (1) parasite exposure (measured observationally as fungal spores attacking wild‐caught hosts), (2) host susceptibility (measured experimentally as the number of fungal spores required to produce terminal infection), (3) host susceptibility traits (barrier resistance and internal clearance, both quantified with experimental assays), and (4) parasite prevalence (measured observationally from wild‐caught hosts). Tracking these factors over 6 months and in almost 7,000 wild‐caught hosts provided key information on the drivers of epidemics. We found that epidemics depended critically on the interaction of exposure and susceptibility; epidemics only emerged when a host population’s level of exposure exceeded its individuals’ capacity for recovery. Additionally, we found that host internal clearance traits (the hemocyte response) were critical in regulating epidemics. Our study provides an empirical demonstration of how parasite exposure and host susceptibility interact to inhibit or drive disease in natural systems and demonstrates that epidemics can be delayed by asynchronicity in the two processes. Finally, our results highlight how individual host traits can scale up to influence broad epidemiological patterns.
Biodiversity loss may increase the risk of infectious disease in a phenomenon known as the dilution effect. Circumstances that increase the likelihood of disease dilution are: (i) when hosts vary in their competence, and (ii) when communities disassemble predictably, such that the least competent hosts are the most likely to go extinct. Despite the central role of competence in diversity-disease theory, we lack a clear understanding of the factors underlying competence, as well as the drivers and extent of its variation. Our perspective piece encourages a mechanistic understanding of competence and a deeper consideration of its role in diversity-disease relationships. We outline current evidence, emerging questions and future directions regarding the basis of competence, its definition and measurement, the roots of its variation and its role in the community ecology of infectious disease.
A pervasive characteristic of malaria parasite infection in mosquito vector populations is their tendency to be overdispersed. Understanding the mechanisms underlying the overdispersed distribution of parasites is of key importance as it may drastically impact the transmission dynamics of the pathogen. The small fraction of heavily infected individuals might serve as superspreaders and cause a disproportionate number of subsequent infections. Although multiple factors ranging from environmental stochasticity to inter-individual heterogeneity may explain parasite overdispersion, Plasmodium infection has also been observed to be highly overdispersed in inbred mosquito population maintained under standardized laboratory conditions, suggesting that other mechanisms may be at play. Here, we show that the aggregated distribution of Plasmodium within mosquito vectors is partially explained by a temporal heterogeneity in parasite infectivity triggered by the bites of blood-feeding mosquitoes. Several experimental blocks carried out with three different Plasmodium isolates have consistently shown that the transmission of the parasite increases progressively with the order of mosquito bites. Surprisingly the increase in transmission is not associated with an increase in Plasmodium replication rate or higher investment in the production of the transmissible stage (gametocyte). Adjustment of the physiological state of the gametocytes could be, however, an adaptive strategy to respond promptly to mosquito bites. Overall our data show that malaria parasite appears to be able to respond to the bites of mosquitoes to increase its own transmission at a much faster pace than initially thought (hours rather than days). Further work needs to be carried out to elucidate whether these two strategies are complementary and, particularly, what are their respective underlaying mechanisms. Understanding the processes underlying the temporal fluctuations in Plasmodium infectivity throughout vertebrate host-to-mosquito transmission is essential and could lead to the development of new approaches to control malaria transmission.
Author summary
Plasmodium parasites are known for being the etiological agents of malaria and for the devastating effects they cause on human populations. A pervasive characteristic of Plasmodium infection is their tendency to be overdispersed in mosquito vector populations: the majority of mosquitoes tend to harbour few or no parasites while a few individuals harbor the vast majority of the parasite population. Understanding the mechanisms underlying Plasmodium overdispersed distribution is of key importance as it may drastically impact the transmission dynamics of the pathogen. Here, we show that the aggregated distribution of Plasmodium parasites within mosquito vectors is partially explained by a temporal heterogeneity in Plasmodium infectivity triggered by the bites of blood-feeding mosquitoes. In other words, mosquitoes that bite at the beginning of a 3h feeding session have significantly fewer parasites than those that bite towards the end. Malaria parasite is therefore capable of responding to the bites of mosquitoes to increase its own transmission at a much faster pace than thought (hours rather than days). Understanding the processes underlying the temporal fluctuations in Plasmodium infectivity throughout vertebrate host-to-mosquito transmission is essential and could lead to the development of new approaches to control malaria transmission.
Applying physiological tools, knowledge and concepts to understand conservation problems (i.e. conservation physiology) has become commonplace and confers an ability to understand mechanistic processes, develop predictive models and identify cause-and-effect relationships. Conservation physiology is making contributions to conservation solutions; the number of ‘success stories’ is growing, but there remain unexplored opportunities for which conservation physiology shows immense promise and has the potential to contribute to major advances in protecting and restoring biodiversity. Here, we consider how conservation physiology has evolved with a focus on reframing the discipline to be more inclusive and integrative. Using a ‘horizon scan’, we further explore ways in which conservation physiology can be more relevant to pressing conservation issues of today (e.g. addressing the Sustainable Development Goals; delivering science to support the UN Decade on Ecosystem Restoration), as well as more forward-looking to inform emerging issues and policies for tomorrow. Our horizon scan provides evidence that, as the discipline of conservation physiology continues to mature, it provides a wealth of opportunities to promote integration, inclusivity and forward-thinking goals that contribute to achieving conservation gains. To advance environmental management and ecosystem restoration, we need to ensure that the underlying science (such as that generated by conservation physiology) is relevant with accompanying messaging that is straightforward and accessible to end users.
Influenza A viruses (IAVs) possess a great zoonotic potential as they are able to infect different avian and mammalian animal hosts, from which they can be transmitted to humans. This is based on the ability of IAV to gradually change their genome by mutation or even reassemble their genome segments during co-infection of the host cell with different IAV strains, resulting in a high genetic diversity. Variants of circulating or newly emerging IAVs continue to trigger global health threats annually for both humans and animals. Here, we provide an introduction on IAVs, highlighting the mechanisms of viral evolution, the host spectrum, and the animal/human interface. Pathogenicity determinants of IAVs in mammals, with special emphasis on newly emerging IAVs with pandemic potential, are discussed. Finally, an overview is provided on various approaches for the prevention of human IAV infections.
Despite estimates that, each year, as many as 300 million dengue virus (DENV) infections result in either no perceptible symptoms (asymptomatic) or symptoms that are sufficiently mild to go undetected by surveillance systems (inapparent), it has been assumed that these infections contribute little to onward transmission. However, recent blood-feeding experiments with Aedes aegypti mosquitoes showed that people with asymptomatic and pre-symptomatic DENV infections are capable of infecting mosquitoes. To place those findings into context, we used models of within-host viral dynamics and human demographic projections to (1) quantify the net infectiousness of individuals across the spectrum of DENV infection severity and (2) estimate the fraction of transmission attributable to people with different severities of disease. Our results indicate that net infectiousness of people with asymptomatic infections is 80% (median) that of people with apparent or inapparent symptomatic infections (95% credible interval (CI): 0–146%). Due to their numerical prominence in the infectious reservoir, clinically inapparent infections in total could account for 84% (CI: 82–86%) of DENV transmission. Of infections that ultimately result in any level of symptoms, we estimate that 24% (95% CI: 0–79%) of onward transmission results from mosquitoes biting individuals during the pre-symptomatic phase of their infection. Only 1% (95% CI: 0.8–1.1%) of DENV transmission is attributable to people with clinically detected infections after they have developed symptoms. These findings emphasize the need to (1) reorient current practices for outbreak response to adoption of pre-emptive strategies that account for contributions of undetected infections and (2) apply methodologies that account for undetected infections in surveillance programs, when assessing intervention impact, and when modeling mosquito-borne virus transmission.
Significance
In vector-borne disease systems, there is mounting evidence that vertebrate hosts become more attractive to disease vectors during infection, yet in human malaria, the underlying mechanism has not been studied. We identified compounds, including aldehydes, that are produced in relatively greater amounts in the skin odor of individuals with malaria, thus demonstrating a basis for this phenomenon in the cues used during mosquito host location. By establishing the attractiveness of these compounds to malaria mosquito vectors in laboratory bioassays, we characterize a process by which Plasmodium infection of humans could lead to increased mosquito biting. These compounds may serve as biomarkers of malaria or be used to enhance the efficacy of chemical lures used to trap mosquitoes.
Parasites can enhance their fitness by modifying the behavior of their hosts in ways that increase rates of production and transmission of parasite larvae. We used an antihelminthic drug to experimentally alter infections of lungworms (Rhabdias pseudosphaerocephala) in cane toads (Rhinella marina). We then compared subsequent behaviors of dewormed toads versus toads that retained infections. Both in the laboratory and in the field, the presence of parasites induced hosts to select higher body temperatures (thereby increasing rates of lungworm egg production), to defecate in moister sites, and to produce feces with higher moisture content (thereby enhancing survival of larvae shed in feces). Because those behavioral modifications enhance rather than decrease parasite fitness, they are likely to have arisen as adaptive manipulations of host behavior rather than as host adaptations to combat infection or as nonadaptive consequences of infection on host physiology. However, the mechanisms by which lungworms alter cane toad thermal preference and defecation are not known. Although many examples of host manipulation by parasites involve intermediate hosts facilitating their own demise, our findings indicate that manipulation of definitive hosts can be as subtle as when and where to defecate.
Viral variants that arise in the global influenza population begin asde novomutations in single infected hosts, but the evolutionary dynamics that transform within-host variation to global genetic diversity are poorly understood. Here, we demonstrate that influenza evolution within infected humans recapitulates many evolutionary dynamics observed at the global scale. We deep-sequence longitudinal samples from four immunocompromised patients with long-term H3N2 influenza infections. We find parallel evolution across three scales: within individual patients, in different patients in our study, and in the global influenza population. In hemagglutinin, a small set of mutations arises independently in multiple patients. These same mutations emerge repeatedly within single patients and compete with one another, providing a vivid clinical example of clonal interference. Many of these recurrent within-host mutations also reach a high global frequency in the decade following the patient infections. Our results demonstrate surprising concordance in evolutionary dynamics across multiple spatiotemporal scales.
Variation in biting frequency by Anopheles mosquitoes can explain some of the heterogeneity in malaria transmission in endemic areas. In this study in Burkina Faso, we assessed natural exposure to mosquitoes by matching the genotype of blood meals from 1066 mosquitoes with blood from residents of local households. We observed that the distribution of mosquito bites exceeded the Pareto rule (20/80) in two of the three surveys performed (20/85, 76, and 96) and, at its most pronounced, is estimated to have profound epidemiological consequences, inflating the basic reproduction number of malaria by 8-fold. The distribution of bites from sporozoite-positive mosquitoes followed a similar pattern, with a small number of individuals within households receiving multiple potentially infectious bites over the period of a few days. Together, our findings indicate that heterogeneity in mosquito exposure contributes considerably to heterogeneity in infection risk and suggest significant variation in malaria transmission potential.
Genetic diversity at community, population and individual levels is thought to influence the spread of infectious disease. At the individual level, inbreeding and heterozygosity are associated with increased risk of infection and disease severity. Host genotype rarity may also reduce infection risk if pathogens are co-adapted to common or local hosts, but to date, no studies have investigated the relative importance of genotype rarity and heterozygosity for infection in a wild, sexually reproducing vertebrate. With beak and feather disease virus (BFDV) infection in a wild parrot (Platycercus elegans), we show that both heterozygosity and genotype rarity of individual hosts predicted infection, but in contrasting ways. Heterozygosity was negatively associated with probability of infection, but not with infection load. In contrast, increased host genotype rarity was associated with lower viral load in infected individuals, but did not predict infection probability. These effects were largely consistent across subspecies, but were not evident at the population level. Subspecies and age were also strongly associated with infection. Our study provides novel insights into infection dynamics by quantifying rarity and diversity simultaneously. We elucidate roles that host genetic diversity can play in infection dynamics, with implications for understanding population divergence, intraspecific diversity and conservation.
Urban expansion has widespread impacts on wildlife species globally, including the transmission and emergence of infectious diseases. However, there is almost no information about how urban landscapes shape transmission dynamics in wildlife. Using an innovative phylodynamic approach combining host and pathogen molecular data with landscape characteristics and host traits, we untangle the complex factors that drive transmission networks of Feline Immunodeficiency Virus (FIV) in bobcats (Lynx rufus). We found that the urban landscape played a significant role in shaping FIV transmission. Even though bobcats were often trapped within the urban matrix, FIV transmission events were more likely to occur in areas with more natural habitat elements. Urban fragmentation also resulted in lower rates of pathogen evolution, possibly owing to a narrower range of host genotypes in the fragmented area. Combined, our findings show that urban landscapes can have impacts on a pathogen and its evolution in a carnivore living in one of the most fragmented and urban systems in North America. The analytical approach used here can be broadly applied to other host-pathogen systems, including humans. This article is protected by copyright. All rights reserved.
The host mechanisms involved in Escherichia coli O157 super-shedding in cattle is largely unknown. In this study, the comparison of transcriptomes of intestinal tissues between super-shedders (SS) and cattle negative for E. coli O157 (NS) was performed, aiming to identify genes that are potentially associated with super-shedding. In total, 16,846 ± 639 (cecum) to 18,137 ± 696 (distal jejunum) were expressed throughout the intestine, with the expressed genes associated with immune functions more pronounced in the small intestine. In total, 351 differentially expressed (DE) genes were identified throughout the intestine between SS and NS, with 101 being up-regulated and 250 down-regulated in SS. Functional analysis revealed DE genes were involved in increased T-cell responses and cholesterol absorption in the distal jejunum and descending colon, and decreased B-cell maturation in the distal jejunum of SS. RNA-Seq based SNP discovery revealed that the mutations in seven DE genes involved in leukocyte activation and cholesterol transportation were associated with E. coli O157 shedding. Our findings suggest that T-cell responses and cholesterol metabolism in the intestinal tract may be associated with super-shedding phenomenon, and the SNPs in the DE genes are possibly associated with the observed gene expression difference between SS and NS.
Glucocorticoid stress hormones, such as corticosterone (CORT), have profound effects on the behaviour and physiology of organisms, and thus have the potential to alter host competence and the contributions of individuals to population- and community-level pathogen dynamics. For example, CORT could alter the rate of contacts among hosts, pathogens and vectors through its widespread effects on host metabolism and activity levels. CORT could also affect the intensity and duration of pathogen shedding and risk of host mortality during infection. We experimentally manipulated songbird CORT, asking how CORT affected behavioural and physiological responses to a standardizedWest Nile virus (WNV) challenge. Although all birds became infected after exposure to the virus, only birdswith elevated CORT had viral loads at or above the infectious threshold. Moreover, though the rate of mortality was faster in birds with elevated CORT compared with controls, most hosts with elevated CORT survived past the day of peak infectiousness. CORT concentrations just prior to inoculation with WNV and anti-inflammatory cytokine concentrations following viral exposure were predictive of individual duration of infectiousness and the ability tomaintain physical performance during infection (i.e. tolerance), revealing putative biomarkers of competence. Collectively, our results suggest that glucocorticoid stress hormones could directly and indirectly mediate the spread of pathogens. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
Host responses to pathogens include defenses that reduce infection burden (i.e., resistance) and traits that reduce the fitness consequences of an infection (i.e., tolerance). Resistance and tolerance are affected by an organism's physiological status. Corticosterone ("CORT") is a hormone that is associated with the regulation of many physiological processes, including metabolism and reproduction. Because of its role in the stress response, CORT is also considered the primary vertebrate stress hormone. When secreted at high levels, CORT is generally thought to be immunosuppressive. Despite the known association between stress and disease resistance in domesticated organisms, it is unclear whether these associations are ecologically and evolutionary relevant in wildlife species. We conducted a 3x3 fully crossed experiment in which we exposed American toads (Anaxyrus [Bufo] americanus) to one of three levels of exogenous CORT (no CORT, low CORT, or high CORT) and then to either low or high doses of the pathogenic chytrid fungus Batrachochytrium dendrobatidis ("Bd") or a sham exposure treatment. We assessed Bd infection levels and tested how CORT and Bd affected toad resistance, tolerance, and mortality. Exposure to the high CORT treatment significantly elevated CORT release in toads; however, there was no difference between toads given no CORT or low CORT. Exposure to CORT and Bd each increased toad mortality, but they did not interact to affect mortality. Toads that were exposed to CORT had higher Bd resistance than toads exposed to ethanol controls/low CORT, a pattern opposite that of most studies on domesticated animals. Exposure to CORT did not affect toad tolerance to Bd. Collectively, these results show that physiological stressors can alter a host's response to a pathogen, but that the outcome might not be straightforward. Future studies that inhibit CORT secretion are needed to better our understanding of the relationship between stress physiology and disease resistance and tolerance in wild vertebrates.
Stress hormones might represent a key link between individual-level infection outcome, population-level parasite transmission, and zoonotic disease risk. Although the effects of stress on immunity are well known, stress hormones could also affect host–vector interactions via modification of host behaviours or vector-feeding patterns and subsequent reproductive success. Here, we experimentally manipulated songbird stress hormones and examined subsequent feeding preferences, feeding success, and productivity of mosquito vectors in addition to defensive behaviours of hosts. Despite being more defensive, birds with elevated stress hormone concentrations were approximately twice as likely to be fed on by mosquitoes compared to control birds. Moreover, stress hormones altered the relationship between the timing of laying and clutch size in blood-fed mosquitoes. Our results suggest that host stress could affect the transmission dynamics of vector-borne parasites via multiple pathways. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
Host variation in parasite load abounds, both within and across natural populations. The forces that shape and maintain this variation, however, are much less obvious. Over the past two decades, the emerging field of ecoimmunology has begun to address the underlying sources of this variation and its evolutionary consequences. Clearly, spatial and temporal heterogeneity in the environment contribute to variation in host parasite load by varying parasite distribution and abundance. However, host variation in the ability to acquire resources, and differences in how these resources are allocated, also play an integral role in parasite susceptibility. That is to say, not all individuals within a population are capable of managing the cost of immune defense, or may employ different cost-managing strategies. This realization has spurred a surge in studies focused on how immune pathways compete with other costly physiological pathways, such as those associated with reproduction. Interest in this relationship has no doubt been driven by the reproductive system's high energetic cost and its direct association with host fitness. In this chapter, I examine the interactions between reproduction and immunity to highlight the simultaneous role both play in the evolution of immunological and reproductive adaptations. I begin by placing this interaction in the context of life history theory and discuss how competition for limited resources may constrain the evolution and expression of both systems. I then discuss the role that parasites play in directly shaping reproductive adaptations through sexual selection. In this discussion, I attempt to shed light on the lingering controversy that has overshadowed genetic benefit models and provide concrete predictions for future directions. © 2014 Springer Science+Business Media Dordrecht. All rights reserved.
Individual heterogeneity can influence the dynamics of infectious diseases in wildlife and humans alike. Thus, recent work has sought to identify behavioural characteristics that contribute disproportionately to individual variation in pathogen acquisition (super-receiving) or transmission (super-spreading). However, it remains unknown whether the same behaviours enhance both acquisition and transmission, a scenario likely to result in explosive epidemics. Here, we examined this possibility in an ecologically relevant host–pathogen system: house finches and their bacterial pathogen, Mycoplasma gallisepticum, which causes severe conjunctivitis. We examined behaviours likely to influence disease acquisition (feeder use, aggression, social network affiliations) in an observational field study, finding that the time an individual spends on bird feeders best predicted the risk of conjunctivitis. To test whether this behaviour also influences the likelihood of transmitting M. gallisepticum, we experimentally inoculated individuals based on feeding behaviour and tracked epidemics within captive flocks. As predicted, transmission was fastest when birds that spent the most time on feeders initiated the epidemic. Our results suggest that the same behaviour underlies both pathogen acquisition and transmission in this system and potentially others. Identifying individuals that exhibit such behaviours is critical for disease management.
Infectious diseases often emerge from interactions among multiple species and across nested levels of biological organization. Threats as diverse as Ebola virus, human malaria, and bat white-nose syndrome illustrate the need for a mechanistic understanding of the ecological interactions underlying emerging infections. We describe how recent advances in community ecology can be adopted to address contemporary challenges in disease research. These analytical tools can identify the factors governing complex assemblages of multiple hosts, parasites, and vectors, and reveal how processes link across scales from individual hosts to regions. They can also determine the drivers of heterogeneities among individuals, species, and regions to aid targeting of control strategies. We provide examples where these principles have enhanced disease management and illustrate how they can be further extended.
Copyright © 2015, American Association for the Advancement of Science.
The progression of an infection within a host determines the ability of a pathogen to transmit to new hosts and to maintain itself in the population. While the general connection between the infection dynamics within a host and the population-level transmission dynamics of pathogens is widely acknowledged, a comprehensive and quantitative understanding that would allow full integration of the two scales is still lacking. Here, we provide a brief discussion of both models and data that have attempted to provide quantitative mappings from within-host infection dynamics to transmission fitness. We present a conceptual framework and provide examples of studies that have taken first steps towards development of a quantitative framework that scales from within-host infections to population-level fitness of different pathogens. We hope to illustrate some general themes, summarize some of the recent advances and-maybe most importantly-discuss gaps in our ability to bridge these scales, and to stimulate future research on this important topic.
© 2015 The Author(s) Published by the Royal Society. All rights reserved.
Mitochondria are well appreciated for their role as biosynthetic and bioenergetic organelles. In the past two decades, mitochondria have emerged as signaling organelles that contribute critical decisions about cell proliferation, death, and differentiation. Mitochondria not only sustain immune cell phenotypes but also are necessary for establishing immune cell phenotype and their function. Mitochondria can rapidly switch from primarily being catabolic organelles generating ATP to anabolic organelles that generate both ATP and building blocks for macromolecule synthesis. This enables them to fulfill appropriate metabolic demands of different immune cells. Mitochondria have multiple mechanisms that allow them to activate signaling pathways in the cytosol including altering in AMP/ATP ratio, the release of ROS and TCA cycle metabolites, as well as the localization of immune regulatory proteins on the outer mitochondrial membrane. In this Review, we discuss the evidence and mechanisms that mitochondrial dependent signaling controls innate and adaptive immune responses.
Copyright © 2015 Elsevier Inc. All rights reserved.
Despite some notable successes in the control of infectious diseases, transmissible pathogens still pose an enormous threat to human and animal health. The ecological and evolutionary dynamics of infections play out on a wide range of interconnected temporal, organizational, and spatial scales, which span hours to months, cells to ecosystems, and local to global spread. Moreover, some pathogens are directly transmitted between individuals of a single species, whereas others circulate among multiple hosts, need arthropod vectors, or can survive in environmental reservoirs. Many factors, including increasing antimicrobial resistance, increased human connectivity and changeable human behavior, elevate prevention and control from matters of national policy to international challenge. In the face of this complexity, mathematical models offer valuable tools for synthesizing information to understand epidemiological patterns, and for developing quantitative evidence for decision-making in global health.
Copyright © 2015, American Association for the Advancement of Science.
Wildlife epidemiological outcomes can depend strongly on the composition of an ecological community, particularly when multiple host species are affected by the same pathogen. However, the relationship between host species richness and disease risk can vary with community context and with the degree of spillover transmission that occurs among co-occurring host species. We examined the degree to which host species composition influences infection by Batrachochytrium dendrobatidis (Bd), a widespread fungal pathogen associated with amphibian population declines around the world, and whether transmission occurs from one highly susceptible host species to other co-occurring host species. By manipulating larval assemblages of three sympatric amphibian species in the laboratory, we characterized the relationship between host species richness and infection severity, whether infection mediates growth and survivorship differently across various combinations of host species, and whether Bd is transmitted from experimentally inoculated tadpoles to uninfected tadpoles. We found evidence of a dilution effect where Bd infection severity was dramatically reduced in the most susceptible of the three host species (Anaxyrus boreas). Infection also mediated survival and growth of all three host species such that the presence of multiple host species had both positive (e.g., infection reduction) and negative (e.g., mortality) effects on focal species. However, we found no evidence that Bd infection is transmitted by this species. While these results demonstrate that host species richness as well as species identity underpin infection dynamics in this system, dilution is not the product of reduced transmission via fewer infectious individuals of a susceptible host species. We discuss various mechanisms, including encounter reduction and antagonistic interactions such as competition and opportunistic cannibalism that may act in concert to mediate patterns of infection severity, growth, and mortality observed in multihost communities.
There is no doubt that viruses require cells to successfully reproduce and effectively infect the next host. The question is what is the fate of the infected cells? All eukaryotic cells can"sense" viral infections and exhibit defence strategies to oppose viral replication and spread. This often leads to the elimination of the infected cells by programmed cell death or apoptosis. This"sacrifice" of infected cells represents the most primordial response of multicellular organisms to viruses. Subverting host cell apoptosis, at least for some time, is therefore a crucial strategy of viruses to ensure their replication, the production of essential viral proteins, virus assembly and the spreading to new hosts. For that reason many viruses harbor apoptosis inhibitory genes, which once inside infected cells are expressed to circumvent apoptosis induction during the virus reproduction phase. On the other hand, viruses can take advantage of stimulating apoptosis to (i) facilitate shedding and hence dissemination, (ii) to prevent infected cells from presenting viral antigens to the immune system or (iii) to kill non-infected bystander and immune cells which would limit viral propagation. Hence the decision whether an infected host cell undergoes apoptosis or not depends on virus type and pathogenicity, its capacity to oppose antiviral responses of the infected cells and/or to evade any attack from immune cells. Viral genomes have therefore been adapted throughout evolution to satisfy the need of a particular virus to induce or inhibit apoptosis during its life cycle. Here we review the different strategies used by viruses to interfere with the two major apoptosis as well as with the innate immune signaling pathways in mammalian cells. We will focus on the intrinsic mitochondrial pathway and discuss new ideas about how particular viruses could activately engage mitochondria to induce apoptosis of their host.
Copyright © 2015. Published by Elsevier B.V.
Significance
A minority of infected hosts is thought to be responsible for the majority of pathogen transmission events. Surprisingly little is known about what distinguishes superspreader hosts from the rest of the infected population. Using a mouse model of Salmonella infection, we show that levels of Salmonella are equivalent between antibiotic-treated superspreader and nonsuperspreader hosts; however, superspreader hosts are uniquely able to tolerate antibiotic treatment, unlike nonsuperspreader hosts. We find that nonsuperspreaders have a hyperinflammatory response to antibiotic treatment, resulting in increased inflammatory myeloid cells that contribute to the morbidity observed. Superspreaders display neither an increased frequency of inflammatory myeloid cells nor morbidity upon antibiotic treatment. Our data describe tolerance mechanisms unique to superspreader hosts that enable sustained pathogen transmission.
The mammalian intestine is colonized by beneficial commensal bacteria and is a site of infection by pathogens, including helminth
parasites. Helminths induce potent immunomodulatory effects, but whether these effects are mediated by direct regulation of
host immunity or indirectly through eliciting changes in the microbiota is unknown. We tested this in the context of virus-helminth
coinfection. Helminth coinfection resulted in impaired antiviral immunity and was associated with changes in the microbiota
and STAT6-dependent helminth-induced alternative activation of macrophages. Notably, helminth-induced impairment of antiviral
immunity was evident in germ-free mice, but neutralization of Ym1, a chitinase-like molecule that is associated with alternatively
activated macrophages, could partially restore antiviral immunity. These data indicate that helminth-induced immunomodulation
occurs independently of changes in the microbiota but is dependent on Ym1.
Although network analysis has drawn considerable attention as a promising tool for disease ecology, empirical research has been hindered by limitations in detecting the occurrence of pathogen transmission (who transmitted to whom) within social networks.
Using a novel approach, we utilize the genetics of a diverse microbe, E scherichia coli , to infer where direct or indirect transmission has occurred and use these data to construct transmission networks for a wild giraffe population ( G iraffe camelopardalis ). Individuals were considered to be a part of the same transmission chain and were interlinked in the transmission network if they shared genetic subtypes of E . coli .
By using microbial genetics to quantify who transmits to whom independently from the behavioural data on who is in contact with whom, we were able to directly investigate how the structure of contact networks influences the structure of the transmission network. To distinguish between the effects of social and environmental contact on transmission dynamics, the transmission network was compared with two separate contact networks defined from the behavioural data: a social network based on association patterns, and a spatial network based on patterns of home‐range overlap among individuals.
We found that links in the transmission network were more likely to occur between individuals that were strongly linked in the social network. Furthermore, individuals that had more numerous connections or that occupied ‘bottleneck’ positions in the social network tended to occupy similar positions in the transmission network. No similar correlations were observed between the spatial and transmission networks. This indicates that an individual's social network position is predictive of transmission network position, which has implications for identifying individuals that function as super‐spreaders or transmission bottlenecks in the population.
These results emphasize the importance of association patterns in understanding transmission dynamics, even for environmentally transmitted microbes like E. coli . This study is the first to use microbial genetics to construct and analyse transmission networks in a wildlife population and highlights the potential utility of an approach integrating microbial genetics with network analysis.
Sickle cell trait (HbAS) is the best-characterized genetic polymorphism known to protect against falciparum malaria. Although the protective effect of HbAS against malaria is well known, the mechanism(s) of protection remain unclear. A number of biochemical and immune-mediated mechanisms have been proposed, and it is likely that multiple complex mechanisms are responsible for the observed protection. Increased evidence for an immune component of protection as well as novel mechanisms, such as enhanced tolerance to disease mediated by HO-1 and reduced parasitic growth due to translocation of host micro-RNA into the parasite, have recently been described. A better understanding of relevant mechanisms will provide valuable insight into the host-parasite relationship, including the role of the host immune system in protection against malaria.
Since the identification and imprisonment of "Typhoid Mary," a woman who infected at least 47 people with typhoid in the early 1900s, epidemiologists have recognized that 'superspreading' hosts play a key role in disease epidemics. Such variability in transmission also exists among species within a community (amplification hosts) and among habitat patches across a landscape (disease 'hotspots'), underscoring the need for an integrative framework for studying transmission heterogeneity. Here, we synthesize literature on human, plant, and animal diseases to evaluate the relative contributions of host, pathogen, and environmental factors in driving transmission heterogeneity across hosts and space. We show that host and spatial heterogeneity are closely linked and that quantitatively assessing the contribution of infectious individuals, species, or environmental patches to overall transmission can aid management strategies. We conclude by posing hypotheses regarding how pathogen natural history influences transmission heterogeneity and highlight emerging frontiers in the study of transmission heterogeneity.