Temperature-Dependent Pre-Bloodmeal Period and Temperature-Driven Asynchrony between Parasite Development and Mosquito Biting Rate Reduce Malaria Transmission Intensity

A mosquito needs to bite at least twice for malaria transmission to occur: once to acquire parasites and, after these parasites complete their development in their mosquito host, once to transmit the parasites to the next vertebrate host. Here we investigate the relationship between temperature, parasite development, and biting frequency in a mosquito-rodent malaria model system. We show that the pre-bloodmeal period (the time lag between mosquito emergence and first bloodmeal) increases at lower temperatures. In addition, parasite development time and feeding exhibit different thermal sensitivities such that mosquitoes might not be ready to feed at the point at which the parasite is ready to be transmitted. Exploring these effects using a simple theoretical model of human malaria shows that delays in infection and transmission can reduce the vectorial capacity of malaria mosquitoes by 20 to over 60%, depending on temperature. These delays have important implications for disease epidemiology and control, and should be considered in future transmission models.     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum

Transmission of parasites to new hosts crucially depends on the timing of production of transmission stages and their capacity to start an infection. These parameters may be influenced by genetic factors, but also by the environment. We tested the effects of temperature and host genotype on infection probability and latency in experimental populations of the ciliate Paramecium caudatum, after exposure to infectious forms of its bacterial parasite Holospora undulata. Temperature had a significant effect on the expression of genetic variation for transmission and maintenance of infection. Overall, low temperature (10 degrees C) increased levels of (multiple) infection, but arrested parasite development; higher temperatures (23 and 30 degrees C) accelerated the onset of production of infectious forms, but limited transmission success. Viability of infectious forms declined rapidly at 23 and 30 degrees C, thereby narrowing the time window for transmission. Thus, environmental conditions can generate trade-offs between transmission relevant parameters and alter levels of multiple infection or parasite-mediated selection, which may affect evolutionary trajectories of parasite life history or virulence.     

The spread of fecally transmitted parasites in socially-structured populations

Mammals are infected by a wide array of gastrointestinal parasites, including parasites that also infect humans and domesticated animals. Many of these parasites are acquired through contact with infectious stages present in soil, feces or vegetation, suggesting that ranging behavior will have a major impact on their spread. We developed an individual-based spatial simulation model to investigate how range use intensity, home range overlap, and defecation rate impact the spread of fecally transmitted parasites in a population composed of social groups (i.e., a socially structured population). We also investigated the effects of epidemiological parameters involving host and parasite mortality rates, transmissibility, disease-related mortality, and group size. The model was spatially explicit and involved the spillover of a gastrointestinal parasite from a reservoir population along the edge of a simulated reserve, which was designed to mimic the introduction pathogens into protected areas. Animals ranged randomly within a "core" area, with biased movement toward the range center when outside the core. We systematically varied model parameters using a Latin hypercube sampling design. Analyses of simulation output revealed a strong positive association between range use intensity and the prevalence of infection. Moreover, the effects of range use intensity were similar in magnitude to effects of group size, mortality rates, and the per-contact probability of transmission. Defecation rate covaried positively with gastrointestinal parasite prevalence. Greater home range overlap had no positive effects on prevalence, with a smaller core resulting in less range overlap yet more intensive use of the home range and higher prevalence. Collectively, our results reveal that parasites with fecal-oral transmission spread effectively in socially structured populations. Future application should focus on parameterizing the model with empirically derived ranging behavior for different species or populations and data on transmission characteristics of different infectious organisms.     

Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.     

Different transmission strategies of a parasite in male and female hosts

We investigated whether a parasite with two routes of transmission responds to the different transmission opportunities offered by male and female hosts by using different transmission strategies in the two sexes. The parasite Ascogregarina culicis, which infects the mosquito Aedes aegypti, can be transmitted as its host’s pupa transforms into an adult or when a female lays its eggs. As the latter transmission route is missing in males, we expected, and found, that the parasite releases a greater proportion of its infectious forms during emergence when it is within a male than when it infects a female. The transmission route, which influences the parasite’s dispersal and the evolution of its virulence, was also affected by the dose of infection and the parasite’s previous transmission route. Our results emphasize the complexity underlying the development of parasites and show their ability to tune their strategy to their environment.     

Experimental evolution of parasite life-history traits in Strongyloides ratti (Nematoda)

Evolutionary ecology predicts that parasite life-history traits, including a parasite's survivorship and fecundity within a host, will evolve in response to selection and that their evolution will be constrained by trade-offs between traits. Here, we test these predictions using a nematode parasite of rats, Strongyloides ratti, as a model. We performed a selection experiment by passage of parasite progeny from either early in an infection ('fast' lines) or late in an infection ('slow' lines). We found that parasite fecundity responded to selection but that parasite survivorship did not. We found a trade-off mediated via conspecific density-dependent constraints; namely, that fast lines exhibit higher density-independent fecundity than slow lines, but fast lines suffered greater reduction in fecundity in the presence of density-dependent constraints than slow lines. We also found that slow lines both stimulate a higher level of IgG1, which is a marker for a Th2-type immune response, and show less of a reduction in fecundity in response to IgG1 levels than for fast lines. Our results confirm the general prediction that parasite life-history traits can evolve in response to selection and indicate that such evolutionary responses may have significant implications for the epidemiology of infectious disease.     

Modelling the effect of temperature on transmission of dengue

The main entomological parameters involved in the rate of dengue virus transmission include the longevity of female mosquitoes, the time interval between bites and the extrinsic incubation period of the virus. Field and laboratory data provide estimates for these parameters, but their interactions with other factors (e.g. host population density and environmental parameters) make their integration into a transmission model quite complex. To estimate the impact of these parameters on transmission, we developed a model of virus transmission by a vector population which predicts the number of potentially infective bites under a range of temperatures and entomological parameters, including the daily survival rate of females, the interval between bites and the extrinsic incubation period. Results show that in a stable population, an increase in mosquito longevity disproportionately enhances the number of potential transmissions (e.g. by as much as five times when the survival rate rises from 0.80 to 0.95). Halving the length of the biting interval with a 10-°C rise in temperature increases the transmission rate by at least 2.4 times. Accordingly, the model can predict changes in dengue transmission associated with short-term variation in seasonal temperature and also with potentially long-lasting increases in global temperatures.     

Intensity of transmission and spread of gene mutations linked to chloroquine and sulphadoxine-pyrimethamine resistance in falciparum malaria

The number of malaria parasite clones per infection-multiplicity of parasite clones-is affected by the transmission intensity, multiplicity increases with increasing transmission. This affects the frequency of parasites' sexual recombination and, if several mutations in different genes are involved, can break down drug resistant genotypes. Therefore, the effects of malaria transmission intensity on the spread of drug resistance could vary depending on the number of genes involved. Here we show that, compared to low transmission, intermediate-high transmission is associated with a 20-100-fold lower risk for the mutations linked to chloroquine resistance and a 6-17 times higher risk for those linked to sulphadoxine-pyrimethamine resistance. This is consistent with the hypothesis of a multigenic basis for chloroquine resistance and a monogenic basis for that of sulphadoxine-pyrimethamine. Reducing transmission intensity could slow the spread of resistance. However, a reduction below a critical threshold (e.g. when parasite prevalence in children 2-9 years old is around 60-80%) could, paradoxically, accelerate the spread of resistance to chloroquine and possibly to other drug combinations whose basis is multigenic. Our findings have important implications for malaria control because increasing drug resistance has a substantial impact on mortality.     

The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation

Numerous parasites with complex life cycles are able to manipulate the behaviour of their intermediate host in a way that increases their trophic transmission to the definitive host. Pomphorhynchus laevis, an acanthocephalan parasite, is known to reverse the phototactic behaviour of its amphipod intermediate host, Gammarus pulex, leading to an increased predation by fish hosts. However, levels of behavioural manipulation exhibited by naturally-infected gammarids are extremely variable, with some individuals being strongly manipulated whilst others are almost not affected by infection. To investigate parasite age and parasite intensity as potential sources of this variation, we carried out controlled experimental infections on gammarids using parasites from two different populations. We first determined that parasite intensity increased with exposure dose, but found no relationship between infection and host mortality. Repeated measures confirmed that the parasite alters host behaviour only when it reaches the cystacanth stage which is infective for the definitive host. They also revealed, we believe for the first time, that the older the cystacanth, the more it manipulates its host. The age of the parasite is therefore a major source of variation in parasite manipulation. The number of parasites within a host was also a source of variation. Manipulation was higher in hosts infected by two parasites than in singly infected ones, but above this intensity, manipulation did not increase. Since the development time of the parasite was also different according to parasite intensity (it was longer in doubly infected hosts than in singly infected ones, but did not increase more in multi-infected hosts), individual parasite fitness could depend on the compromise between development time and manipulation efficiency. Finally, the two parasite populations tested induced slightly different degrees of behavioural manipulation.     

Dynamics of Hen Flea Ceratophyllus gallinae Subpopulations in Blue Tit Nests

The hen flea is a common parasite in bird nests, in particular, in tit species, and imposes considerable fitness costs for the host. These costs are expected to lead to selection for increased host defense, which in turn should select for better-adapted parasites. Our understanding of the coevolution of this host–parasite system is currently limited by the insufficient knowledge of both the timing of flea generations and their reproductive behavior within the nesting period of their hosts. In the present study we (1) followed the demography of experimental flea subpopulations during the host's breeding cycle, (2) assessed the importance of time–temperature effects in the nest by recording temperatures within the nest material, and (3) investigated the influence of variation in host timing and duration of the breeding period on flea development. We found the following. (1) Fleas completed either one or two generations within the birds' nesting cycle, leading to two well-defined periods of cocoon formation. (2) Within-nest temperatures during the warm period of the host breeding cycle—i.e., the incubation and nestling periods—depended on both outdoor temperatures and heat production from the breeding birds. Day-degree availability, a measure of physiological time, during the host incubation was significantly explained by the duration of incubation period and its timing in the season. Similarly, day-degrees during the warmer nestling period were significantly explained by its duration and its timing in the season. (3) The number of flea larvae found in the nests correlated with the host's timing and duration of the warm period available for their development; this was not the case, however, for the number of adult fleas. These results underline the importance of time–temperature effects as determinants of flea demography within the nests. The life-cycle and time–temperature effects are discussed in the light of potential host selection on parasite behavior and life histories.     

Effect of Temperature on Embryonation of Ascaris suum Eggs in an Environmental Chamber

The influence of temperature on the development and embryonation of Ascaris suum eggs was studied using coarse sand medium in an environmental chamber with 50% humidity. The time required for development and embryonation of eggs was examined under 3 different temperature conditions, 5℃, 25℃, and 35℃. A. suum eggs did not develop over 1 month at the temperature of 5℃. However, other temperature conditions, 25℃ and 35℃, induced egg development to the 8-cell-stage at days 5-6 after incubation. All eggs examined developed to the 8-cell stage at day 6 after incubation in the sand medium at 25℃. The higher temperature, 35℃, slightly accelerated the A. suum egg development compared to 25℃, and the development to the 8-cell stage occurred within day 5 after incubation. The formation of larvae in A. suum eggs at temperatures of 35℃ and 25℃ appeared at days 17 and 19 after incubation, respectively. These findings show that 35℃ condition shortens the time for the development of A. suum eggs to the 8-cell-stage in comparison to 25℃, and suggest the possibility of accelerated transmission of this parasite, resulting from global warming and ecosystem changes.     

Simulated climate change,epidemic size,and host evolution across host–parasite populations

Climate change is causing warmer and more variable temperatures as well as physical flux in natural populations, which will affect the ecology and evolution of infectious disease epidemics. Using replicate seminatural populations of a coevolving freshwater invertebrate‐parasite system (host: Daphnia magna, parasite: Pasteuria ramosa), we quantified the effects of ambient temperature and population mixing (physical flux within populations) on epidemic size and population health. Each population was seeded with an identical suite of host genotypes and dose of parasite transmission spores. Biologically reasonable increases in environmental temperature caused larger epidemics, and population mixing reduced overall epidemic size. Mixing also had a detrimental effect on host populations independent of disease. Epidemics drove parasite‐mediated selection, leading to a loss of host genetic diversity, and mixed populations experienced greater evolution due to genetic drift over the season. These findings further our understanding of how diversity loss will reduce the host populations’ capacity to respond to changes in selection, therefore stymying adaptation to further environmental change.     

Dispersal increases local transmission of avian malarial parasites

The relationships between dispersal and local transmission rate of parasites are essential to understanding host–parasite coevolution and the emergence and spread of novel disease threats. Here we show that year‐round transmission, as opposed to summer transmission, has repeatedly evolved in malarial parasites (genera Plasmodium and Haemoproteus) of a migratory bird. Year‐round transmission allows parasites to spread in sympatric host's wintering areas, and hence to colonize distantly located host's breeding areas connected by host‐migration movements. Widespread parasites had higher local prevalence, revealing increased transmission, than geographically restricted parasites. Our results show a positive relationship between dispersal and local transmission of malarial parasites that is apparently mediated by frequent evolutionary changes in parasite transmission dynamics, which has important implications for the ecology and evolution of infectious diseases.     

Climate changes influence free‐living stages of soil‐transmitted parasites of European rabbits

Climate warming has been suggested to augment the risk of infectious disease outbreaks by extending the seasonal window for parasite growth and by increasing the rate of transmission. Understanding how this occurs in parasite‐host systems is important for appreciating long‐term and seasonal changes in host exposure to infection and to reduce species extinction caused by diseases. We investigated how free‐living stages of two soil‐transmitted helminths of the European rabbit (Oryctolagus cuniculus) responded to experimental changes in temperature by performing laboratory experiments with environmental chambers and field manipulations using open‐top‐chambers. This study was motivated by our previous observations that air temperature has increased over the last 30 years in our field site and that during this period intensity of infection of Graphidium strigosum but not Trichostrongylus retortaeformis was positively associated with this temperature increase. Laboratory and field experiments showed that both parasites accelerated egg development and increased hatching rate and larval survival in response to accumulating thermal energy. Both parasites behaved similarly when exposed to diverse temperature regimes, decadal trends, and monthly fluctuations, however, T. retortaeformis was more successful than G. strigosum by showing higher rates of egg hatching and larval survival. Across the months, the first day of hatching occurred earlier in warmer conditions suggesting that climate warming can lengthen the period of parasite growth and host exposure to infective stages. Also, T. retortaeformis hatched earlier than G. strigosum. These findings showed that seasonal changes in intensity, frequency, and duration of daily temperature are important causes of variability in egg hatching and larva survival. Overall, this study emphasizes the important role of climate warming and seasonality on the dynamics of free‐living stages in soil‐transmitted helminths and their contribution to enhance host exposure to parasitic infections. Yet, the ability to infect might ultimately depend on how hosts interact with parasites.     

Ecological,evolutionary, and conservation implications of incubation temperature‐dependent phenotypes in birds

Incubation is a vital component of reproduction and parental care in birds. Maintaining temperatures within a narrow range is necessary for embryonic development and hatching of young, and exposure to both high and low temperatures can be lethal to embryos. Although it is widely recognized that temperature is important for hatching success, little is known about how variation in incubation temperature influences the post‐hatching phenotypes of avian offspring. However, among reptiles it is well known that incubation temperature affects many phenotypic traits of offspring with implications for their future survival and reproduction. Although most birds, unlike reptiles, physically incubate their eggs, and thus behaviourally control nest temperatures, variation in temperature that influences embryonic development still occurs among nests within a population. Recent research in birds has primarily been limited to populations of megapodes and waterfowl; in each group, incubation temperature has substantial effects on hatchling phenotypic traits important for future development, survival, and reproduction. Such observations suggest that incubation temperature (and incubation behaviours of parents) is an important but underappreciated parental effect in birds and may represent a selective force instrumental in shaping avian reproductive ecology and life‐history traits. However, much more research is needed to understand how pervasive phenotypic effects of incubation temperature are among birds, the sources of variation in incubation temperature, and how effects on phenotype arise. Such insights will not only provide foundational information regarding avian evolution and ecology, but also contribute to avian conservation.     

Castrating parasites and colonial hosts

Trajectories of life-history traits such as growth and reproduction generally level off with age and increasing size. However, colonial animals may exhibit indefinite, exponential growth via modular iteration thus providing a long-lived host source for parasite exploitation. In addition, modular iteration entails a lack of germ line sequestration. Castration of such hosts by parasites may therefore be impermanent or precluded, unlike the general case for unitary animal hosts. Despite these intriguing correlates of coloniality, patterns of colonial host exploitation have not been well studied. We examined these patterns by characterizing the responses of a myxozoan endoparasite, Tetracapsuloides bryosalmonae, and its colonial bryozoan host, Fredericella sultana, to 3 different resource levels. We show that (1) the development of infectious stages nearly always castrates colonies regardless of host condition, (2) castration reduces partial mortality and (3) development of transmission stages is resource-mediated. Unlike familiar castrator-host systems, this system appears to be characterized by periodic rather than permanent castration. Periodic castration may be permitted by 2 key life history traits: developmental cycling of the parasite between quiescent (covert infections) and virulent infectious stages (overt infections) and the absence of germ line sequestration which allows host reproduction in between bouts of castration.     

Effect of temperature on argyrophil impregnation: development of a high temperature rapid argyrophil procedure

Our studies on the effects of temperature on the demonstration of neurosecretory granules using argyrophil stains indicate an inverse relationship between the time needed for staining and temperature of the silver and reducing solutions. Careful monitoring of the temperature of silver solutions during the Grimelius procedure and its modifications show long incubation times serve in large part only to bring the solutions to reaction temperature. Tissue sections added when this temperature has been reached will stain with the same intensity as sections impregnated for the entire incubation period. We have modified the argyrophil procedure so that double-impregnation with solutions preheated to 60-70 C and development in Bodian's reducer prepared with preheated water rapidly demonstrates secretory granules. Our method does not require a microwave oven and much shorter incubation periods are required than with usual procedures. It is not necessary to incubate sections in hot solutions for extended periods of time, which can lead to detachment of sections, nonspecific staining and decomposition of the silver solution. Rinsing after impregnation and before development greatly increases contrast of argyrophil cells by reducing background staining. Our procedure results in more reliable staining of argyrophil and argentaffin cells and takes only ten minutes.     

Effect of Temperature on Argyrophil Impregnation: Development of A High Temperature Rapid Argyrophil Procedure

Out studies on the effects of temperature on the demonstration of neurosecretory granules using argyrophil stains indicate an inverse relationship between the time needed for staining and temperature of the silver and reducing solutions. Careful monitoring of the temperature of silver solutions during the Grimelius procedure and its modifications show long incubation times serve in large part only to bring the solutions to reaction temperature. Tissue sections added when this temperature has been reached will stain with the same intensity as sections impregnated for the entire incubation period. We have modified the argyrophil procedure so that double-impregnation with solutions preheated to 60-70 C and development in Bodian's reducer prepared with preheated water rapidly demonstrates secretory granules. Our method does not require a microwave oven and much shorter incubation periods are required than with usual procedures. It is not necessary to incubate sections in hot solutions for extended periods of time, which can lead to detachment of sections, nonspecific staining and decomposition of the silver solution. Rinsing after impregnation and before development greatly increases contrast of argyrophil cells by reducing background staining. Our procedure results in more reliable staining of argyrophil and argentaffin cells and takes only ten minutes.     

Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events

Levels of parasitism and the dynamics of helminth systems is subject to the impact of environmental conditions such that we may expect long term increases in temperature will increase the force of infection and the parasite's basic reproduction number, R0. We postulate that an increase in the force of infection will only lead to an increase in mean intensity of adults when adult parasite mortality is not determined by acquired immunity. Preliminary examination of long term trends of parasites of rabbits and grouse confirm these predictions. Parasite development rate increases with temperature and while laboratory studies indicate this is linear some recent studies indicate that this may be non-linear and would have an important impact on R0. Warming would also reduce the selective pressure for the development of arrestment and this would increase R0 so that in systems like the grouse and Trichostrongylus tenuis this would increase the instability and lead to larger disease outbreaks. Extreme climatic events that act across populations appear important in synchronizing transmission and disease outbreaks, so it is speculated that climate disruption will lead to increased frequency and intensity of disease outbreaks in parasite populations not regulated by acquired immunity.