Individual variations in infectiousness explain long-term disease persistence in wildlife populations

Viral disease persistence in species without a reservoir host is of importance for public health and disease management. But how can disease persistence be explained? We developed a spatially‐explicit individual‐based model that takes into account both ecological and viral traits as well as variable space to test disease persistence hypotheses under debate. We introduce a novel concept of modeling alternative disease courses at the individual level, causing transient infections or killing infected animals, with the lethally infected having a variable life‐expectancy. We systematically distinguish between disease invasion and persistence. We use classical swine fever (CSF), an economically very important livestock disease in a social host, the wild boar, as a reference system to test and rank the persistence hypotheses under debate. Parameter values for host population demographics and CSF epidemiology reflect current knowledge. Sensitivity analysis of the model parameters revealed that the most important factor for disease persistence is a disease profile with mostly transient, i.e. surviving individuals requiring immunity, and some chronically, long‐term infected animals. Immune individuals can constantly produce susceptible offspring, while some chronically infected individuals act as ‘super spreaders’ in time. Thus, variations in the course of the disease at the individual level are important factors determining persistence, which is usually not taken into account in the prominent measure of epidemiology, i.e. the basic reproductive number R₀, which reflects the ‘reproductive potential’ of the infected sub‐population. We discuss our results with regard to the general issues of modeling epidemics and disease management issues.     

The impact of infection on host competition and its relationship to parasite persistence in a Daphnia microparasite system

Evolutionary studies often estimate fitness components with the aim to make predictions about the outcome of selection. Depending on the system and the question, different fitness components are used, but their usefulness for predicting the outcome of selection is rarely tested. Here we estimate host fitness components in different ways with the aim to test how well they agree with each other and how well they predict host fitness at the population level in the presence of the parasite. We use a Daphnia magna-microparasite system to study the competitive ability of host clones in the absence and presence of the parasite, the infection intensity of the parasite in individuals of twelve host clones (an estimate of both host resistance and parasite reproductive success), and parasite persistence in small host populations (an estimate of R ₀ of the parasite). Analysis of host competitive ability and parasite persistence reveals strong host genotype effects, while none are found for infection intensity. Host competitive ability further shows a genotype-specific change upon infection, which is correlated with the relative persistence of the parasite in the competing hosts. Hosts in which the parasite persists better suffer a competitive disadvantage in the parasite’s presence. This suggests that in this system, parasite-mediated selection can be predicted by parasite persistence, but not by parasite infection intensity.     

Widening the window of persistence in seasonal pathogen-host systems

Local instability of exploiter-victim systems is well-known in both theory and in nature. Victims can be too sparse to support exploiter reproduction (under-exploitation) or they can be too readily driven to extinction (over-exploitation). Exploiters of seasonal resources face the additional challenge of surviving periods when victims are rare or unavailable. We formulate a fully stochastic model of highly seasonal pathogen-host dynamics and explore the interactions between an entomopathogenic nematode and its lepidopteran host. Our model suggests that if nematode populations experience the high rates of mortality predicted by short-term laboratory experiments, the paired threats of under- and over-exploitation should preclude the long-term persistence of this exploiter-victim system. We measured nematode mortality rates in the field and found that long-term mortality is lower than that predicted by short-term experiments. Incorporation of this new data into our model produces long-term persistence of local nematode populations across a range of initial nematode densities.     

Individual heterogeneity and costly punishment: a volunteer's dilemma

Social control and the enforcement of social norms glue a society together. It has been shown theoretically and empirically that informal punishment of wrongdoers fosters cooperation in human groups. Most of this research has focused on voluntary and uncoordinated punishment carried out by individual group members. However, as punishment is costly, it is an open question as to why humans engage in the punishment of wrongdoers even in one-time-only encounters. While evolved punitive preferences have been advocated as proximate explanations for such behaviour, the strategic nature of the punishment situation has remained underexplored. It has been suggested to conceive of the punishment situation as a volunteer''s dilemma (VOD), where only one individual''s action is necessary and sufficient to punish the wrongdoer. Here, we show experimentally that implementing the punishment situation as a VOD sustains cooperation in an environment where punishers and non-punishers coexist. Moreover, we show that punishment-cost heterogeneity allows individuals to tacitly agree on only the strongest group member carrying out the punishment, thereby increasing the effectiveness and efficiency of social norm enforcement. Our results corroborate that costly peer punishment can be explained without assuming punitive preferences and show that centralized sanctioning institutions can emerge from arbitrary individual differences.     

Melatonin mediates seasonal adjustments in immune function.

In addition to seasonal changes in reproductive function, seasonal changes in immune function are mediated by the pineal hormone, melatonin. Melatonin affects immune function both indirectly, acting through other hormones, and directly by acting on components of the immune system. Melatonin also affects tumorigenesis and tumor development. We hypothesize that many of the indirect effects of melatonin on immune function are mediated through glucocorticoids, and appear to be part of an integrated series of adaptations to manage energy. Direct effects of melatonin on immune function appear to be mediated by melatonin receptors on lymphatic tissue or on immune cells in circulation. Winter is energetically demanding and stressful; thermoregulatory demands typically increase when food availability decreases. Individuals would enjoy a survival advantage if seasonally recurring stressors could be anticipated and countered by bolstering immune function. To summarize, melatonin may be part of an integrative system to coordinate reproductive, immunologic and other physiological processes to cope successfully with energetic stressors during winter.     

Small-scale spatial heterogeneity and seasonal variation in a population of a cave-dwelling Mediterranean mysid

Seasonal changes in small-scale spatial distribution patternsof abundance and composition of Hemimysis speluncola Ledoyer(1963) (Crustacea, Mysidacea) were studied in a population ofcave-dwelling mysids off the Medes Islands (NW MediterraneanSea). The distribution pattern was characterized all year roundby marked spatial segregation of juveniles, which occupied areascloser to the cave entrance, while adults were concentratedmainly in the innermost part of the cave. The small-scale spatialheterogeneity observed appears to be regulated by biologicalfactors, particularly social and reproductive behaviour. Nevertheless,a certain adaptation of the distribution of the swarms to hydrodynamicfactors suggests that physical factors may also play a role.The heterogeneous aggregation pattern recorded would clearlyappear to be an adaptive strategy by the population to enableit to thrive within its habitat. That adaptation is designedto reduce predation mortality, enhance mating efficiency andregulate the population generally. Marked seasonal fluctuationsin the density and composition of the population were recorded,with high density levels in winter and throughout the spring.Two methods were employed to quantify the population: haulswith plankton nets towed by divers and collection of faecalpellets. The patterns observed using both these methods weresimilar, although the latter method yielded total density valuesthat were an order of magnitude greater.     

The effects of background mortality on optimal reproduction in a seasonal environment

We consider optimal annual routines of reproductive behaviour in a seasonal environment. In our model the condition of the organism is adversely affected by hard work, but can recover during easy periods. Our analysis concentrates on the effects of background mortality (i.e., mortality that cannot be avoided) on the optimal strategy and how often an organism following this strategy breeds. In particular, we are concerned with whether reproduction occurs at specific times of year (entrained to the annual cycle), and if so then how many reproductive bouts occur per year. We find that an increase in background mortality can have various effects. If the animal is entrained to the annual cycle and has one breeding attempt per year, then breeding tends to occur earlier and there may be two breeding attempts per season. Another possible outcome is that breeding is no longer entrained. If the animal is entrained but sometimes skips reproduction so that it does not breed every year, then an increase in mortality may make it more likely that the animal breeds every year. We show that as background mortality increases the resultant increase in the frequency of breeding contributes to the increase in annual mortality. We also explore the effects of mortality on the timing of reproduction within a year, highlighting the tension between the interests of the parent and that of the young.     

Resource heterogeneity and persistence of exotic annuals in long-ungrazed Mediterranean-climate woodlands

Processes that promote weed invasion are often well-demonstrated, but mechanisms that facilitate ecological resistance to weed invasion in non-invaded communities, or promote weed persistence in invaded communities, are poorly understood. Yet it is these processes that must be addressed to achieve sustainable ecological restoration. We surveyed soil heterogeneity in 25 long-ungrazed, unfertilized York gum (Eucalyptus loxophleba Benth. subsp. loxophleba)—jam (Acacia acuminata Benth.) woodlands of the Western Australian wheatbelt to investigate differences in soil characteristics between patches locally-invaded or non-invaded by widespread exotic annuals. Based on studies in other ecosystems, we hypothesized that (1) weed persistence is associated with elevated soil resource levels, and (2) of these soil resources, phosphorus is the key contributor to weed persistence in Western Australian woodlands, that typically occur on phosphorus-impoverished soils. Our first hypothesis was partly supported, with soil nutrients associated with up to 40% of the variation in cover of exotic annuals. In particular, low concentrations of total nitrogen, nitrate and available phosphorus are likely to contribute to resistance to invasion in many non-invaded woodland patches, especially in gaps between trees. However, other non-invaded patches had comparable nutrient concentrations to invaded patches, suggesting this resistance may be weak at more productive sites or that patches have not reached a stable equilibrium. Inconsistent with our second hypothesis, exotic annuals were as strongly correlated with elevated total nitrogen and associated variables as they were with available phosphorus, probably reflecting a history of grazing without fertilization. We conclude that effectiveness of ‘bottom-up’ approaches to weed control is likely to differ among ecosystems according to interactions with disturbance history and attributes of the non-invaded community, even where the weed species or functional types are the same.     

The effect of seasonal host birth rates on disease persistence

In this paper, we add seasonality to the birth rate of an SIR model with density dependence in the death rate. We find that disease persistence can be explained by considering the average value of the seasonal term. If the basic reproductive ratio R(0)>1 with this average value then the disease will persist and if R(0)<1 with this average value then the disease will die out. However, if the underlying non-seasonal model displays oscillations towards the equilibrium then the dynamics of the seasonal model can become more complex. In this case, the seasonality can interact with the underlying oscillations, resonate and the population can display a range of complex behaviours including chaos. We discuss these results in terms of two examples, Cowpox in bank voles and Rabbit Haemorrhagic disease in rabbits.     

Virulence is context-dependent in a vertically transmitted aquatic host–microparasite system

Recent work has suggested that the outcomes of host–symbiont interactions can shift between positive, neutral and negative depending on both biotic and abiotic conditions. Even organisms traditionally defined as parasites can have positive effects on hosts under some conditions. For a given host–parasite system, the effects of infection on host fitness can depend on host vigour, route of transmission and environmental conditions. We monitored sublethal microsporidian infections in populations of Gammarus pseudolimnaeus (Amphipoda: Gammaridae) from four cool water streams in southwestern Michigan, USA. Our objectives were to: (i) infer the mechanism of transmission (horizontal, vertical or mixed) from observed effects of infection on host fitness, (ii) determine if the magnitude of the effects on host fitness is a function of parasite load (infection intensity) compared with simple presence or absence of infection, and (iii) determine if there is variation in parasite effects on host fitness in isolated populations. PCR and DNA sequence analyses revealed that there were two microsporidia present among the four host populations: Dictyocoela sp. and Microsporidium sp. PCR screening of a subset of infected hosts showed that Dictyocoela sp. accounted for 90% of infections and was present in all four G. pseudolimnaeus populations, while Microsporidium sp. was found in two populations but was only relatively common in one. We found very low prevalence in males (∼5%), but high prevalence in females (range: 37–85%). Female fitness was positively associated with infection in two streams, resulting from either higher fecundity or more reproductive bouts. Infection had a negative effect on the number of reproductive bouts in a third population, and no effect on fecundity in a fourth population. Infection intensity explained additional variation in fecundity in one population; females with intermediate infection intensity had higher fecundity than females with either light or heavy infection intensity. Given the high prevalence of infection in females compared with males and the generally weak negative fitness effects coupled with some positive fitness effects, it is likely that both Dictyocoela sp. and Microsporidium sp. are primarily vertically transmitted, feminizing microsporidia. Our results suggest that microsporidian effects on G. pseudolimnaeus fitness were context-dependent and varied with host sex and local environment.     

Mechanisms promoting the long-term persistence of a Wolbachia infection in a laboratory-adapted population of Drosophila melanogaster

Intracellular bacteria of the genus Wolbachia are widespread endosymbionts across diverse insect taxa. Despite this prevalence, our understanding of how Wolbachia persists within populations is not well understood. Cytoplasmic incompatibility (CI) appears to be an important phenotype maintaining Wolbachia in many insects, but it is believed to be too weak to maintain Wolbachia in Drosophila melanogaster, suggesting that Wolbachia must also have other effects on this species. Here we estimate the net selective effect of Wolbachia on its host in a laboratory-adapted population of D. melanogaster, to determine the mechanisms leading to its persistence in the laboratory environment. We found i) no significant effects of Wolbachia infection on female egg-to-adult survival or adult fitness, ii) no reduced juvenile survival in males, iii) substantial levels of CI, and iv) a vertical transmission rate of Wolbachia higher than 99%. The fitness of cured females was, however, severely reduced (a decline of 37%) due to CI in offspring. Taken together these findings indicate that Wolbachia is maintained in our laboratory environment due to a combination of a nearly perfect transmission rate and substantial CI. Our results show that there would be strong selection against females losing their infection and producing progeny free from Wolbachia.     

Temperature and population density determine reservoir regions of seasonal persistence in highland malaria

A better understanding of malaria persistence in highly seasonal environments such as highlands and desert fringes requires identifying the factors behind the spatial reservoir of the pathogen in the low season. In these ‘unstable’ malaria regions, such reservoirs play a critical role by allowing persistence during the low transmission season and therefore, between seasonal outbreaks. In the highlands of East Africa, the most populated epidemic regions in Africa, temperature is expected to be intimately connected to where in space the disease is able to persist because of pronounced altitudinal gradients. Here, we explore other environmental and demographic factors that may contribute to malaria''s highland reservoir. We use an extensive spatio-temporal dataset of confirmed monthly Plasmodium falciparum cases from 1995 to 2005 that finely resolves space in an Ethiopian highland. With a Bayesian approach for parameter estimation and a generalized linear mixed model that includes a spatially structured random effect, we demonstrate that population density is important to disease persistence during the low transmission season. This population effect is not accounted for in typical models for the transmission dynamics of the disease, but is consistent in part with a more complex functional form of the force of infection proposed by theory for vector-borne infections, only during the low season as we discuss. As malaria risk usually decreases in more urban environments with increased human densities, the opposite counterintuitive finding identifies novel control targets during the low transmission season in African highlands.     

The effect of spatial heterogeneity on the persistence of predator-prey interactions

The effect of spatially discontinuous environments on predator-prey systems is examined by using a computer simulation model. It is shown that increasing prey dispersal and decreasing predator dispersal do not necessarily have a stabilizing influence on the interaction, as had been concluded by previous workers. The stability of predator-prey interaction depends on the interaction of the dispersal process with normal reproduction and feeding of the predator and prey species.     

Genetics of sprouting: effects of long-term persistence in fire-prone ecosystems

Fire functional traits (postfire resprouting and seeding) are considered to be adaptations for persisting in fire-prone environments. Although ecological and evolutionary consequences of sprouting have been extensively discussed, within-species genetic variability and structure are unknown. Here we report levels and distribution patterns of genetic polymorphisms in postfire stands of the predominant sprouter Nothofagus antarctica . Fresh foliage of 50 individuals was collected following a spatially explicit sampling design for isozyme analysis from two replicates of each of four habitat types inhabited by the species in northwestern Patagonia, Argentina: matorral, high elevation, forest, and temporally flooded basins. Average polymorphism per population ranged from 44% to 78% and mean gene diversity per site H _S varied from 0.187 to 0.274. These results show that sprouter populations hold considerable genetic variation. Significant genetic structure over short distances (< 50 m) was found at all locations. Ancient fine-scale genetic structure is preserved by occasional seedling establishment that results in high co-ancestry coefficients. Sprouter populations growing in suboptimal habitats such as matorral, high elevation or basins consist of pairs of heterozygous genets that occur at larger spatial scales as a result of micro-environmental heterogeneity and/or local competition between near neighbour genotypes. In contrast, homozygous pairs of individuals for distinct isozyme loci occurred at larger spatial scales in forest stands. This indicates that biparental inbreeding due to local propagule establishment may take place to some extent in sprouters growing under favourable conditions. Our results show that sprouters follow a long-lasting genet persistence strategy which most probably is selected under unpredictable disturbance regimes, such as fire.     

On the effects of spatial heterogeneity on the persistence of interacting species

 The dynamics of two interacting theoretical populations inhabiting a heterogeneous environment are modelled by a system of two weakly coupled reaction–diffusion equations having spatially dependent reaction terms. Longterm persistence of both populations is guaranteed by an invasibility condition, which is itself expressed via the signs of certain eigenvalues of related linear elliptic operators with spatially dependent lowest order coefficients. The effects of change in these coefficients upon the eigenvalues are here exploited to study the effects of spatial heterogeneity on the persistence of interacting species through two particular ecological topics of interest. The first concerns when the location of favorable hunting grounds within the overall environment does or does not affect the success of a predator in predator–prey models, while the second concerns cases of competition models in which the outcome of competition in a spatially varying environment differs from that which would be expected in a spatially homogeneous environment. Received: 9 June 1997     

Day-to-day and seasonal fluctuations of urban mortality in Houston,Texas

Mortality, exclusive of that caused by accidents, for Houston, Texas, from 1971 to 1973 was studied for temporal patterns and for associations with daily maximum and minimum temperature, relative humidity, barometric pressure, and precipitation. The sensitive and unbiased method of spectral analysis permitted the consideration of time lags between events. The findings revealed significant seasonal difference in mortality with the highest being in winter and more interestingly, strong lagged associations were found between short-term upswings in mortality and specific weather conditions, such as those characterized by low air temperature and high barometric pressure. In combination these weather features are typical of winter anticyclones. The peaks in mortality were evident after cold spells within periods of two weeks. Furthermore, episodes of elevated mortality also were observed subsequent to heat waves such as those during the summer of 1971.