Host Social Structure Research Articles

The influence of social and spatial processes on the epidemiology of environmentally transmitted pathogens in wildlife: implications for management.

Social and spatial structures of host populations play important roles in pathogen transmission. For environmentally transmitted pathogens, the host space use interacts with both the host social structure and the pathogen's environmental persistence (which determines the time-lag across which two hosts can transmit). Together, these factors shape the epidemiological dynamics of environmentally transmitted pathogens. While the importance of both social and spatial structures and environmental pathogen persistence has long been recognized in epidemiology, they are often considered separately. A better understanding of how these factors interact to determine disease dynamics is required for developing robust surveillance and management strategies. Here, we use a simple agent-based model where we vary host mobility (spatial), host gregariousness (social) and pathogen decay (environmental persistence), each from low to high levels to uncover how they affect epidemiological dynamics. By comparing epidemic peak, time to epidemic peak and final epidemic size, we show that longer infectious periods, higher group mobility, larger group size and longer pathogen persistence lead to larger, faster growing outbreaks, and explore how these processes interact to determine epidemiological outcomes such as the epidemic peak and the final epidemic size. We identify general principles that can be used for planning surveillance and control for wildlife host-pathogen systems with environmental transmission across a range of spatial behaviour, social structure and pathogen decay rates. This article is part of the theme issue 'The spatial-social interface: a theoretical and empirical integration'.

Host age structure reshapes parasite symbiosis: collaboration begets pathogens, competition begets virulent mutualists

BackgroundSymbiotic relationships are ubiquitous in the biosphere. Inter-species symbiosis is impacted by intra-specific distinctions, in particular, those defined by the age structure of a population. Older individuals compete with younger individuals for resources despite being less likely to reproduce, diminishing the fitness of the population. Conversely, however, older individuals can support the reproduction of younger individuals, increasing the population fitness. Parasitic relationships are commonly age structured, typically, more adversely affecting older hosts.ResultsWe employ mathematical modeling to explore the differential effects of collaborative or competitive host age structures on host-parasite relationships. A classical epidemiological compartment model is constructed with three disease states: susceptible, infected, and recovered. Each of these three states is partitioned into two compartments representing young, potentially reproductive, and old, post-reproductive, hosts, yielding 6 compartments in total. In order to describe competition and collaboration between old and young compartments, we model the reproductive success to depend on the fraction of young individuals in the population. Collaborative populations with relatively greater numbers of post-reproductive hosts enjoy greater reproductive success whereas in purely competitive populations, increasing the post-reproductive subpopulation reduces reproductive success.ConclusionsWe demonstrate that, in collaborative host populations, pathogens strictly impacting older, post-reproductive individuals can reduce population fitness even more than pathogens that directly impact younger, potentially reproductive individuals. In purely competitive populations, the reverse is observed, and we demonstrate that endemic, virulent pathogens can oxymoronically form a mutualistic relationship with the host, increasing the fitness of the host population. Applications to endangered species conservation and invasive species containment are discussed.

Age structure of amphibian populations with endemic chytridiomycosis, across climatic regions with markedly different infection risk.

Threatening processes, such as disease, can drive major changes in population demographics of the host. Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), has led to the decline of at least 500 amphibian species across the globe and has been shown to truncate host age structure by lowering adult survival rates. This results in heavy reliance on annual recruitment and the inability to recover in the event of periodic recruitment failure. We used skeletochronology to determine the age structure, growth, and survival rates of populations of an endangered amphibian, Litoria raniformis, with endemic chytridiomycosis, across two climatically disparate regions in south‐eastern Australia: semi‐arid and temperate. Contrary to predictions, populations in the semi‐arid region (in which chytrid prevalence is substantially lower due to high temperatures) displayed a more truncated age structure than populations in the temperate study regions. Maximum recorded age was only two years in the semi‐arid region compared with up to four years in the temperate region. Wetland hydroperiod and average seasonal air temperature were correlated with age, and males had a slightly higher survival rate than females (0.31 for males and 0.27 for females). Despite the previously documented differences in chytrid prevalence between the two climatic regions, water availability and wetland hydroperiods appear the over‐riding determinants of the age structure and survival rates of L. raniformis. Targeted management which ensures water availability and improves survival of 1‐year‐old frogs into their second and third breeding season would reduce the impact of stochastic events on L. raniformis, and this may be true for numerous frog species susceptible to chytridiomycosis.

Intra- and interspecific similarity in species composition of helminth communities in two closely-related rodents from South Africa

To reveal factors responsible for spatial variation in parasite community composition we studied patterns of similarity in helminth species composition in two closely-related rodents (Rhabdomys pumilio and Rhabdomys dilectus) that differ in their social and spatial behaviour and live under different environmental conditions across 20 localities in South Africa. We asked whether the two hosts harbour similar assemblages, whether these are more dissimilar between than within hosts and if host social structure, behaviour or environment affects similarity patterns in helminth infracommunities within and among localities. We also investigated whether similarity in species composition of helminth component communities decreases with an increase of geographic distance between host populations. We found that the pattern of space use by the hosts rather than their social behaviour promotes differences in helminth species composition between host species as well as among host populations from different localities. The rate of distance decay of similarity in species composition of helminth component communities differed between the two hosts due to difference in the degree of environmental variation across their geographic ranges. We conclude that patterns of spatial variation in helminth species composition are driven mainly by host spatial behaviour and, to a lesser extent, by environment-associated factors.

Localized removal affects white‐tailed deer space use and contacts

ABSTRACTTransmission and impact of infectious diseases can be altered if host social structure is disrupted by disease outbreaks or lethal management. Specifically, if remnants of depopulated groups join or increase contact with neighboring groups, between‐group transmission may increase even as population density decreases. We tested whether this phenomenon could apply to diseases of white‐tailed deer (Odocoileus virginianus) by using a before‐after‐control‐impact design. We monitored space use and contacts among adult female and juvenile deer in southern Illinois during 2011–2014; midway through each study season, we removed all members except 1 collared deer from centrally located groups and left control groups intact. After group removal, remnant adult females shortened duration of contacts with neighboring groups, whereas remnant juveniles responded with greater shifts in space use and appeared to join neighboring groups. Together, our study points to potential age‐specific responses of deer to social disruption, with evidence that juveniles respond in ways that could shift disease transmission dynamics toward frequency dependence. These findings highlight the need for focused research into the importance of social disruption in disease dynamics, and lend support for complete group removal (if possible) when culling for disease management. © 2016 The Wildlife Society.

Analysis of a temperature- and rainfall-dependent model for malaria transmission dynamics

A new non-autonomous model is designed and used to assess the impact of variability in temperature and rainfall on the transmission dynamics of malaria in a population. In addition to adding age-structure in the host population and the dynamics of immature malaria mosquitoes, a notable feature of the new model is that recovered individuals do not revert to wholly-susceptible class (that is, recovered individuals enjoy reduced susceptibility to new malaria infection). In the absence of disease-induced mortality, the disease-free solution of the model is shown to be globally-asymptotically stable when the associated reproduction ratio is less than unity. The model has at least one positive periodic solution when the reproduction ratio exceeds unity (and the disease persists in the community in this case). Detailed uncertainty and sensitivity analysis, using mean monthly temperature and rainfall data from KwaZulu-Natal province of South Africa, shows that the top three parameters of the model that have the most influence on the disease transmission dynamics are the mosquito carrying capacity, transmission probability per contact for susceptible mosquitoes and human recovery rate. Numerical simulations of the model show that, for the KwaZulu-Natal province, malaria burden increases with increasing mean monthly temperature and rainfall in the ranges ([17–25]°C and [32–110] mm), respectively (and decreases with decreasing mean monthly temperature and rainfall values). In particular, transmission is maximized for mean monthly temperature and rainfall in the ranges [21–25]°C and [95–125] mm. This occurs for a six-month period in KwaZulu-Natal (hence, this study suggests that anti-malaria control efforts should be intensified during this period). It is shown, for the fixed mean monthly temperature of KwaZulu-Natal, that malaria burden decreases whenever the amount of rainfall exceeds a certain threshold value. It is further shown (through sensitivity analysis and numerical simulations) that incorporating host age-structure and reduced susceptibility due to prior malaria infection has marginal effect on the transmission dynamics of the disease.

Host behaviour-parasite feedback: an essential link between animal behaviour and disease ecology.

Animal behaviour and the ecology and evolution of parasites are inextricably linked. For this reason, animal behaviourists and disease ecologists have been interested in the intersection of their respective fields for decades. Despite this interest, most research at the behaviour-disease interface focuses either on how host behaviour affects parasites or how parasites affect behaviour, with little overlap between the two. Yet, the majority of interactions between hosts and parasites are probably reciprocal, such that host behaviour feeds back on parasites and vice versa. Explicitly considering these feedbacks is essential for understanding the complex connections between animal behaviour and parasite ecology and evolution. To illustrate this point, we discuss how host behaviour-parasite feedbacks might operate and explore the consequences of feedback for studies of animal behaviour and parasites. For example, ignoring the feedback of host social structure on parasite dynamics can limit the accuracy of predictions about parasite spread. Likewise, considering feedback in studies of parasites and animal personalities may provide unique insight about the maintenance of variation in personality types. Finally, applying the feedback concept to links between host behaviour and beneficial, rather than pathogenic, microbes may shed new light on transitions between mutualism and parasitism. More generally, accounting for host behaviour-parasite feedbacks can help identify critical gaps in our understanding of how key host behaviours and parasite traits evolve and are maintained.

Social structure and Escherichia coli sharing in a group-living wild primate, Verreaux's sifaka.

BackgroundEpidemiological models often use information on host social contacts to predict the potential impact of infectious diseases on host populations and the efficiency of control measures. It can be difficult, however, to determine whether social contacts are actually meaningful predictors of transmission. We investigated the role of host social structure in the transmission of Escherichia coli in a wild population of primates, Verreaux’s sifakas (Propithecus verreauxi). Using multilocus sequence typing (MLST), we compared genetic similarities between E. coli isolates from different individuals and groups to infer transmission pathways.ResultsCorrelation of social and transmission networks revealed that membership to the same group significantly predicted sharing of E. coli MLST sequence types (ST). Intergroup encounter rate and a measure of space-use sharing provided equally potent explanations for type sharing between social groups when closely related STs were taken into account, whereas animal age, sex and dispersal history had no influence. No antibiotic resistance was found, suggesting low rates of E. coli spillover from humans into this arboreal species.ConclusionsWe show that patterns of E. coli transmission reflect the social structure of this group-living lemur species. We discuss our results in the light of the species’ ecology and propose scent-marking, a type of social contact not considered in previous epidemiological studies, as a likely route of transmission between groups. However, further studies are needed to explicitly test this hypothesis and to further elucidate the relative roles of direct contact and environmental transmission in pathogen transfer.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-016-0059-y) contains supplementary material, which is available to authorized users.

Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees

Social transmission and host developmental stage are thought to profoundly affect the structure of bacterial communities associated with honey bees and bumble bees, but these ideas have not been explored in other bee species. The halictid bees Megalopta centralis and M. genalis exhibit intrapopulation social polymorphism, which we exploit to test whether bacterial communities differ by host social structure, developmental stage, or host species. We collected social and solitary Megalopta nests and sampled bees and nest contents from all stages of host development. To survey these bacterial communities, we used 16S rRNA gene 454 pyrosequencing. We found no effect of social structure, but found differences by host species and developmental stage. Wolbachia prevalence differed between the two host species. Bacterial communities associated with different developmental stages appeared to be driven by environmentally acquired bacteria. A Lactobacillus kunkeei clade bacterium that is consistently associated with other bee species was dominant in pollen provisions and larval samples, but less abundant in mature larvae and pupae. Foraging adults appeared to often reacquire L. kunkeei clade bacteria, likely while foraging at flowers. Environmental transmission appears to be more important than social transmission for Megalopta bees at the cusp between social and solitary behavior.

Evolution of conflict and cooperation of nematodes associated with solitary and social sweat bees

Parasites and mutualists can wield great influence on the fitness of social organisms, yet the effect that the host’s social structure has on the evolution of parasites, commensals, and mutualists (collectively referred to here as symbionts) is poorly known. Evolutionary theory suggests that host social structure may select for more cooperative symbiont strains in comparison to symbionts of solitary hosts. We compared the productivity of one social and one solitary bee species (Halictus ligatus and Augochlora pura) in the family Halictidae with and without the presence of their nematode symbionts (Acrostichus halicti and Acrostichus puri, respectively). We measured the number of offspring produced, the number of cells provisioned, and nesting activity (for Au. pura) to test the hypothesis that symbionts specific to a social host exhibit greater cooperation than symbionts specific to a solitary host. Infected and uninfected nests of both species did not differ in any fitness estimates indicating that: (1) Acrostichus species are commensals, or at least lack large fitness effects on their hosts, and (2) the transition from association with a solitary host to association with a social host that lives in small colonies does not have detectable effects on the evolution of conflict and cooperation in this system. This is the first comparative study to test the idea that host social structure may influence the evolution of symbionts; future work should compare closely related mutualists and parasites of more advanced eusocial insects to mutualists and parasites of solitary insects.

Cleptoparasites, social parasites and a common host: Chemical insignificance for visiting host nests, chemical mimicry for living in

Social insect colonies contain attractive resources for many organisms. Cleptoparasites sneak into their nests and steal food resources. Social parasites sneak into their social organisations and exploit them for reproduction. Both cleptoparasites and social parasites overcome the ability of social insects to detect intruders, which is mainly based on chemoreception. Here we compared the chemical strategies of social parasites and cleptoparasites that target the same host and analyse the implication of the results for the understanding of nestmate recognition mechanisms. The social parasitic wasp Polistes atrimandibularis (Hymenoptera: Vespidae), and the cleptoparasitic velvet ant Mutilla europaea (Hymenoptera: Mutillidae), both target the colonies of the paper wasp Polistes biglumis (Hymenoptera: Vespidae). There is no chemical mimicry with hosts in the cuticular chemical profiles of velvet ants and pre-invasion social parasites, but both have lower concentrations of recognition cues (chemical insignificance) and lower proportions of branched alkanes than their hosts. Additionally, they both have larger proportions of alkenes than their hosts. In contrast, post-invasion obligate social parasites have proportions of branched hydrocarbons as large as those of their hosts and their overall cuticular profiles resemble those of their hosts. These results suggest that the chemical strategies for evading host detection vary according to the lifestyles of the parasites. Cleptoparasites and pre-invasion social parasites that sneak into host colonies limit host overaggression by having few recognition cues, whereas post-invasion social parasites that sneak into their host social structure facilitate social integration by chemical mimicry with colony members.

Natural simian immunodeficiency virus transmission in mandrills: a family affair?

Understanding how pathogens spread and persist in the ecosystem is critical for deciphering the epidemiology of diseases of significance for global health and the fundamental mechanisms involved in the evolution of virulence and host resistance. Combining long-term behavioural and epidemiological data collected in a naturally infected mandrill population and a Bayesian framework, the present study investigated unknown aspects of the eco-epidemiology of simian immunodeficiency virus (SIV), the recent ancestor of HIV. Results show that, in contrast to what is expected from aggressive and sexual transmission (i.e. the two commonly accepted transmission modes for SIV), cases of SIVmnd-1 subtype were significantly correlated among related individuals (greater than 30% of the observed cases). Challenging the traditional view of SIV, this finding suggests the inheritance of genetic determinants of susceptibility to SIV and/or a role for behavioural interactions among maternal kin affecting the transmission of the virus, which would highlight the underappreciated role of sociality in the spread of infectious diseases. Outcomes of this study also provide novel insights into the role of host social structure in the evolution of pathogens.

Multi-strain persistence induced by host age structure

In this paper, we formulate an age-structured epidemic model with two competing strains. The model incorporates disease-induced mortality so that the population cannot be assumed to be in a stationary demographic state. We derive explicit expressions of the basic and invasion reproduction numbers for strain one and two, respectively. Analytical results of the model show that the existence and local stability of boundary equilibria can be determined by the reproduction numbers to some extent. Subsequently, under the condition that both invasion reproduction numbers are larger than one, the coexistence of two competing strains is rigorously proved by the theory of uniform persistence of infinite dimensional dynamical systems. However, the results for the corresponding age-independent model show that the two competing strains cannot coexist. This implies that age-structure can lead to the coexistence of the strains. Numerical simulations are further conducted to confirm and extend the analytic results.

Using Hostages to Improve the Quality of Financial Disclosure

Abstract In a well-functioning stock market, issuing firms publicly disclose all relevant information to investors and prices approximate the true value of those firms. This disclosure generates liquidity as investors large and small engage in trading. While it is tempting to take this “good equilibrium” for granted, the current banking crisis suggests a “bad equilibrium” in which disclosure is suspect so banks stop lending to each other and small investors flee the market. In this paper, we argue that a good equilibrium was in place when the New York Stock Exchange (NYSE) operated as a non-profit organization. We argue that far from being an outdated and elitist holdover, the mutual form allowed underwriters, who dominated NYSE membership, to extract hostages from managers of firms listed on the NYSE. That is, managers were expected to invest personal funds in shares of other listed firms, including new issuers (“IPOs”). Since the hostage arrangement was tied to the non-profit form of the NYSE, we predict a decline in information quality after the NYSE became a for-profit firm in March 2006. By comparing the bid-ask spread before and after demutualization, we show that information quality did indeed decline. This finding holds after controlling for market-level variation measured by the bid-ask spread of the NASDAQ National Market. We believe our results can help shed light on the current banking crisis, which originated in areas of the financial system that lack a hostage structure.

THE GEOGRAPHIC STRUCTURE OF SELECTION ON A COEVOLVING INTERACTION BETWEEN SOCIAL PARASITIC WASPS AND THEIR HOSTS HAMPERS SOCIAL EVOLUTION

Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multiyear study, we monitored the fate of the annual breeding attempts of the solitary nesting foundresses of Polistes biglumis wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.

Seasonality, cohort-dependence and the development of immunity in a natural host–nematode system

Acquired immunity is known to be a key modulator of the dynamics of many helminth parasites in domestic and human host populations, but its relative importance in natural populations is more controversial. A detailed long-term dataset on the gastrointestinal nematode Trichostrongylus retortaeformis in a wild population of European rabbits (Oryctolagus cuniculus) shows clear evidence of seasonal acquired immunity in the age-structured infection profiles. By fitting a hierarchy of demographic infection-immunity models to the observed age-structured infection patterns, we are able to quantify the importance of different components (seasonality, immunity and host age structure) of the parasite dynamics. We find strong evidence that the hosts' immunocompetence waxes and wanes with the seasons, but also contains a lifelong cohort factor, possibly acting through a maternal effect dependent on the host's month of birth. These observations have important and broad implications for the ecology of parasite infection in seasonal natural herbivore systems.

Subthreshold and superthreshold coexistence of pathogen variants: The impact of host age-structure

It is well known that in the most general epidemic models with multiple pathogen variants a competitive exclusion principle is valid, such that the variant with the highest reproduction number eliminates the rest. Mechanisms such as super-infection, coinfection, and cross-immunity can lead to pathogen polymorphism where multiple strains coexist. It is also known that variability of infectivity with host age can destabilize the endemic equilibrium and cause oscillations. In this article we show that the hosts’ chronological age can itself lead to coexistence of microparasites in the most basic model where competitive exclusion will occur without the age structure. Moreover, the host age-structure leads to multiple subthreshold dominance equilibria, and both weakly and strongly subthreshold coexistence. We find that the two pathogens cannot cooperate to persist subthreshold if neither one of them can persist subthreshold by itself. If, however, one of them can persist subthreshold by itself, it can cause the two pathogens to coexist in a strongly subthreshold equilibrium. The second strain that persists subthreshold through the mediation of the first always has a lower virulence. Our results show that age structure in infectivity can permit the coexistence of competing pathogens when the incidence is of proportionate mixing type (frequency-dependent transmission) and at least one of the strains is virulent.

Why are dengue virus serotypes so distantly related? Enhancement and limiting serotype similarity between dengue virus strains.

Dengue virus, the causative agent of dengue fever, has four major serotypes characterized by large genetic and immunological distances. We propose that the unusually large distances between the serotypes can be explained in the light of a process of antibody-dependent enhancement (ADE) leading to increased mortality. Antibody-dependent enhancement results from a new infection with a particular serotype in an individual with acquired immunity to a different serotype. Classical dengue fever causes negligible mortality, but ADE leads to the risk of developing the significantly more dangerous dengue haemorrhagic fever (DHF) and dengue shock syndrome (DSS). A mathematical model is presented that describes the epidemiological dynamics of two serotypes of a pathogen where there is the possibility of co-infection and reinfection by a different serotype, along with increased mortality as a result of enhancement. We show that if there is no or slightly increased mortality after reinfection (enhancement), serotypes with a small immunological distance can stably coexist. This suggests that a cloud of serotypes with minor serological differences will constitute the viral population. By contrast, if enhancement is sufficiently great, a substantial immunological distance is necessary for two serotypes to stably coexist in the population. Therefore, high mortality owing to enhancement leads to an evolutionarily stable viral community comprising a set of distantly separated serotypes.

Parasitism and Generation Cycles in a Salt-Marsh Planthopper

1. In warm climates many insects exhibit discrete generations, in the absence of obvious factors that could synchronize their age structure. It has been hypothesized that parasitoid wasps might be responsible for these oscillations in the host age structure, known as generation cycles. 2. We examine the role of the parasitoid Anagrus delicatus in the dynamics of the salt-marsh planthopper Prokelisia marginata. In particular, we evaluate the hypothesis that Anagrus contributes to the formation of generation cycles in the hopper, in the subtropical climate of Florida. 3. Two kinds of evidence are presented

Host-age Structure and Parasitism in a Laboratory System of Two Hymenopterous Parasitoids and Larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae)

Host-age structure of Zabrotes subfasciatus (Boheman) on larval parasitism by two hymenopterous parasitoids, Heterospilus prosopidis Viereck (Braconidae) and Anisopteromalus calandrae (Howard) (Pteromalidae), were examined in a series of laboratory experiments. Ages of the hosts offered to the parasitoids were varied and the number of host larvae successfully parasitized was monitored. The sex ratio of the resulting parasitoids was also monitored. A life-history refuge from parasitism by both parasitoids was found, consisting of the egg stage and the small, young larvae. The refuge length differed for both parasitoids. Host individuals were not parasitized efficiently by A. calandrae for the first 14-16 days, whereas they were not parasitized at all by H. prosopidis for the first 12 days. Host individuals were protected from attack during these refuge periods for up to 60% of their larval period. Host-age refuges were important in the stability of these two host–parasitoid systems. Stability increased with increasing length of the refuge period. The shorter refuge period in the H. prosopidis –host system may lead to further instability by creating asynchrony between the host and parasitoid life cycles. The age of the larval host also determined the sex ratio of the parasitoid populations. This factor may further destabilize the H. prosopidis populations, while having a lesser effect on A. calandrae .