Geographic variation in life cycle strategies of a progenetic trematode

Numerous parasite species have evolved complex life cycles with multiple, subsequent hosts. In trematodes, each transmission event in multi-host life cycles selects for various adaptations, one of which is facultative life cycle abbreviation. This typically occurs through progenesis, i.e., precocious maturity and reproduction via self-fertilization within the second intermediate host. Progenesis eliminates the need for the definitive host and facilitates life cycle completion. Adopting a progenetic cycle may be a conditional strategy in response to environmental cues related to low probability of transmission to the definitive host. Here, the effects of environmental factors on the reproductive strategy of the progenetic trematode Stegodexamene anguillae were investigated using comparisons among populations. In the 3-host life cycle, S. anguillae sexually reproduces within eel definitive hosts, whereas in the progenetic life cycle, S. anguillae reproduces by selfing within the metacercaria cyst in tissues of small fish intermediate hosts. Geographic variation was found in the frequency of progenesis, independent of eel abundance. Progenesis was affected by abundance and length of the second intermediate fish host as well as encystment site within the host. The present study is the first to compare life cycle strategies among parasite populations, providing insight into the often unrecognized plasticity in parasite developmental strategies and transmission.     

The evolution of complex life cycles when parasite mortality is size- or time-dependent

In complex cycles, helminth larvae in their intermediate hosts typically grow to a fixed size. We define this cessation of growth before transmission to the next host as growth arrest at larval maturity (GALM). Where the larval parasite controls its own growth in the intermediate host, in order that growth eventually arrests, some form of size- or time-dependent increase in its death rate must apply. In contrast, the switch from growth to sexual reproduction in the definitive host can be regulated by constant (time-independent) mortality as in standard life history theory. We here develop a step-wise model for the evolution of complex helminth life cycles through trophic transmission, based on the approach of Parker et al. [2003a. Evolution of complex life cycles in helminth parasites. Nature London 425, 480-484], but which includes size- or time-dependent increase in mortality rate. We assume that the growing larval parasite has two components to its death rate: (i) a constant, size- or time-independent component, and (ii) a component that increases with size or time in the intermediate host. When growth stops at larval maturity, there is a discontinuous change in mortality to a constant (time-independent) rate. This model generates the same optimal size for the parasite larva at GALM in the intermediate host whether the evolutionary approach to the complex life cycle is by adding a new host above the original definitive host (upward incorporation), or below the original definitive host (downward incorporation). We discuss some unexplored problems for cases where complex life cycles evolve through trophic transmission.     

WHEN TO GO: OPTIMIZATION OF HOST SWITCHING IN PARASITES WITH COMPLEX LIFE CYCLES

Many trophically transmitted parasites have complex life cycles: they pass through at least one intermediate host before reproducing in their final host. Despite their economic and theoretical importance, the evolution of such cycles has rarely been investigated. Here, combining a novel modeling approach with experimental data, we show for the first time that an optimal transfer time between hosts exists for a "model parasite," the tapeworm Schistocephalus solidus , from its first (copepod) to its second (fish) intermediate host. When transferring between hosts around this time, (1) parasite performance in the second intermediate host, (2) reproductive success in the final host, and (3) fitness in the next generation is maximized. At that time, the infected copepod's behavior changes from predation suppression to predation enhancement. The optimal time for switching manipulation results from a trade-off between increasing establishment probability in the next host and reducing mortality in the present host. Our results show that these manipulated behavioral changes are adaptive for S. solidus , rather than an artifact, as they maximize parasite fitness.     

Spatial covariation between infection levels and intermediate host densities in two trematode species

Both theoretical arguments and empirical evidence suggest that parasite transmission depends on host density. In helminths with complex life cycles, however, it is not clear which host, if any, is the most important. Here, the relationships between the abundance of metacercariae in second intermediate hosts, and the local density of both the first and second intermediate hosts of two trematode species, are investigated. Samples of the snail Potamopyrgus antipodarum, the amphipod Paracalliope fluviatilis and the isopod Austridotea annectens were collected from ten stations in a New Zealand lake. In the trematode Coitocaecum parvum, neither the density of the snail first intermediate host nor that of the amphipod second intermediate host correlated with infection levels in amphipods. In contrast, in the trematode Microphallus, infection levels in isopod second intermediate hosts were positively associated with isopod density and negatively associated with the density of snail first intermediate hosts. These relationships are explained by a negative correlation between snail and isopod densities, mediated in part by their different use of macrophyte beds in the lake. Overall, the results suggest that, at least for Microphallus, local infection levels depend on local intermediate host densities.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle

Many diseases are caused by parasites with complex life cycles that involve several hosts. If parasites cope better with only one of the different types of immune systems of their host species, we might expect a trade-off in parasite performance in the different hosts, that likely influences the evolution of virulence. We tested this hypothesis in a naturally co-evolving host-parasite system consisting of the tapeworm Schistocephalus solidus and its intermediate hosts, a copepod, Macrocyclops albidus, and the three-spined stickleback Gasterosteus aculeatus. We did not find a trade-off between infection success in the two hosts. Rather, tapeworms seem to trade-off adaptation towards different parts of their hosts' immune systems. Worm sibships that performed better in the invertebrate host also seem to be able to evade detection by the fish innate defence systems, i.e. induce lower levels of activation of innate immune components. These worm variants were less harmful for the fish host likely due to reduced costs of an activated innate immune system. These findings substantiate the impact of both hosts' immune systems on parasite performance and virulence.     

Inertia of parasite infection versus host biomass fluctuation

Infection by parasites with complex life cycles such as trematodes depends on many environmental factors which may result in a time-lag between host biomass fluctuations and parasite density in hosts. A cockle (marine bivalve, second intermediate host) population and its associated parasite community were monitored over 15 years. A time-shift correlation analysis suggests that trematode abundance in cockles responds to cockle biomass after a long delay (8 year time-lag). Thus, these parasites can sustainably support a deficit of their intermediate host.     

Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions?

The complex life cycles of parasites are thought to have evolved from simple one-host cycles by incorporating new hosts. Nevertheless, complex developmental routes present parasites with a sequence of highly unlikely transmission events in order to complete their life cycles. Some trematodes like Coitocaecum parvum use facultative life cycle abbreviation to counter the odds of trophic transmission to the definitive host. Parasites adopting life cycle truncation possess the ability to reproduce within their intermediate host, using progenesis, without the need to reach the definitive host. Usually, both abbreviated and normal life cycles are observed in the same population of parasites. Here, we demonstrate experimentally that C. parvum can modulate its development in its amphipod intermediate host and adopt either the abbreviated or the normal life cycle depending on current transmission opportunities or the degree of intra-host competition among individual parasites. In the presence of cues from its predatory definitive host, the parasite is significantly less likely to adopt progenesis than in the absence of such cues. An intermediate response is obtained when the parasites are exposed to cues from non-host predators. The adoption of progenesis is less likely, however, when two parasites share the resource-limited intermediate host. These results show that parasites with complex developmental routes have transmission strategies and perception abilities that are more sophisticated than previously thought.     

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Climate change is expected to alter the dynamics of host–parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the ‘shelter effect’. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid‐summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature‐dependent parasite life history components in a single measure of fitness, R₀. It allows quantitative predictions of climate change impacts, and is easily generalized to many host–parasite systems.     

Evolution of trophic transmission in parasites: why add intermediate hosts?

Although multihost complex life cycles (CLCs) are common in several distantly related groups of parasites, their evolution remains poorly understood. In this article, we argue that under particular circumstances, adding a second host to a single-host life cycle is likely to enhance transmission (i.e., reaching the target host). For instance, in several situations, the propagules of a parasite exploiting a predator species will achieve a higher host-finding success by encysting in a prey of the target predator than by other dispersal modes. In such a case, selection should favor the transition from a single- to a two-host life cycle that includes the prey species as an intermediate host. We use an optimality model to explore this idea, and we discuss it in relation to dispersal strategies known among free-living species, especially animal dispersal. The model found that selection favored a complex life cycle only if intermediate hosts were more abundant than definitive hosts. The selective value of a complex life cycle increased with predation rates by definitive hosts on intermediate hosts. In exploring trade-offs between transmission strategies, we found that more costly trade-offs made it more difficult to evolve a CLC while less costly trade-offs between traits could favor a mixed strategy.     

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.     

The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths

Parasitic worms (helminths) frequently have complex life cycles in which they are transmitted trophically between two or more successive hosts. Sexual reproduction often takes place in high trophic-level (TL) vertebrates, where parasites can grow to large sizes with high fecundity. Direct infection of high TL hosts, while advantageous, may be unachievable for parasites constrained to transmit trophically, because helminth propagules are unlikely to be ingested by large predators. Lack of niche overlap between propagule and definitive host (the trophic transmission vacuum) may explain the origin and/or maintenance of intermediate hosts, which overcome this transmission barrier. We show that nematodes infecting high TL definitive hosts tend to have more successive hosts in their life cycles. This relationship was modest, though, driven mainly by the minimum TL of hosts, suggesting that the shortest trophic chains leading to a host define the boundaries of the transmission vacuum. We also show that alternative modes of transmission, like host penetration, allow nematodes to reach high TLs without intermediate hosts. We suggest that widespread omnivory as well as parasite adaptations to increase transmission probably reduce, but do not eliminate, the barriers to the transmission of helminths through the food web.     

Is the host or the parasite the most locally adapted in an amphipod-acanthocephalan relationship? A case study in a biological invasion context

Manipulative endoparasites with complex life cycles can alter their intermediate host immunity and behaviour in ways that increase survival probability within the host body cavity and enhance successful transmission to the definitive host. These parasitic manipulations are variable among and within parasite species and may result from co-evolutionary processes, in which the parasite is constrained for adaptation to the local intermediate host. Hence, arrival of a new host species in a local host population may promote local parasite maladaptation. This study tested the occurrence of local adaptation in two distantly located populations of the acanthocephalan parasite Pomphorhynchus laevis and its effect on the immunity and behaviour of its gammarid intermediate host Gammarus roeseli. This was done in France (an area for which G. roeseli is a recent invader) and Hungary (an area from which G. roeseli was believed to be native). As expected, we found no alteration in G. roeseli's immune defence and behaviour associated with infection by P. laevis in localities, where the gammarid is invasive. Unexpectedly, we found similar results in Hungarian populations, where the parasite was even more exposed to the host immune response. Whilst these results suggest maladaptation of the parasite to the gammarid in both countries, they also suggest that the gammarid host might be locally adapted to the parasite. Genetic analyses were performed on both the parasite and the host and the results suggest that the two subsets of populations we studied harbour rather isolated host-parasite systems, both probably deriving from a common ancestral population. We propose that G. roeseli is also of recent acquisition in Hungary, and that a recent co-evolutionary history between P. laevis and G. roeseli in association with a long generation time in the parasite has constrained parasite adaptations in Europe or even favoured host adaptation to the parasite.     

Infection with an acanthocephalan manipulates an amphipod's reaction to a fish predator's odours

Many parasites with complex life cycles increase the chances of reaching a final host by adapting strategies to manipulate their intermediate host's appearance, condition or behaviour. The acanthocephalan parasite Pomphorhynchus laevis uses freshwater amphipods as intermediate hosts before reaching sexual maturity in predatory fish. We performed a series of choice experiments with infected and uninfected Gammarus pulex in order to distinguish between the effects of visual and olfactory predator cues on parasite-induced changes in host behaviour. When both visual and olfactory cues, as well as only olfactory cues were offered, infected and uninfected G. pulex showed significantly different preferences for the predator or the non-predator side. Uninfected individuals significantly avoided predator odours while infected individuals significantly preferred the side with predator odours. When only visual contact with a predator was allowed, infected and uninfected gammarids behaved similarly and had no significant preference. Thus, we believe we show for the first time that P. laevis increases its chance to reach a final host by olfactory-triggered manipulation of the anti-predator behaviour of its intermediate host.     

Lack of seasonal variation in the life-history strategies of the trematode Coitocaecum parvum: no apparent environmental effect

Parasites with complex life cycles have developed numerous and very diverse adaptations to increase the likelihood of completing this cycle. For example, some parasites can abbreviate their life cycles by skipping the definitive host and reproducing inside their intermediate host. The resulting shorter life cycle is clearly advantageous when definitive hosts are absent or rare. In species where life-cycle abbreviation is facultative, this strategy should be adopted in response to seasonally variable environmental conditions. The hermaphroditic trematode Coitocaecum parvum is able to mature precociously (progenesis), and produce eggs by selfing while still inside its amphipod second intermediate host. Several environmental factors such as fish definitive host density and water temperature are known to influence the life-history strategy adopted by laboratory raised C. parvum. Here we document the seasonal variation of environmental parameters and its association with the proportion of progenetic individuals in a parasite population in its natural environment. We found obvious seasonal patterns in both water temperature and C. parvum host densities. However, despite being temporally variable, the proportion of progenetic C. parvum individuals was not correlated with any single parameter. The results show that C. parvum life-history strategy is not as flexible as previously thought. It is possible that the parasite's natural environment contains so many layers of heterogeneity that C. parvum does not possess the ability to adjust its life-history strategy to accurately match the current conditions.     

The life cycle of Brachylaima ruminae n. sp. (Trematoda: Brachylaimidae), a parasite of rodents

The life cycle of Brachylaima ruminae n.sp. (Trematoda: Brachylaimidae), a duodenal parasite of rodents on the Mediterranean island of Formentera (Spain) is elucidated. The new species follows a terrestrial triheteroxenous life cycle. Eggs passed in the faeces of the definitive host must be ingested by a specific first intermediate host, the land snail Rumina decollata. Branched cercariogenous sporocysts develop in the digestive gland. Microcercous cercariae come out through the terminal birth pores of the branches. Cercariae shed by the snail are terrestrial, crawling on humid substratum. They contact the second intermediate host, another land snail, principally the species R. decollata and less frequently slugs and Helicids. Cercariae enter via the excretory pore and kidney duct to their specific final location, the kidney. Unencysted metacercariae develop in the kidney (also, less frequently, in the pedal glands) to the mature, infective stage. Infective metacercariae infest the definitive host when ingested together with the snail.     

Evolutionary consequence of a change in life cycle complexity: A link between precocious development and evolution toward female‐biased sex allocation in a hermaphroditic parasite

The evolutionary consequences of changes in the complex life cycles of parasites are not limited to the traits that directly affect transmission. For instance, mating systems that are altered due to precocious sexual maturation in what is typically regarded as an intermediate host may impact opportunities for outcrossing. In turn, reproductive traits may evolve to optimize sex allocation. Here, we test the hypothesis that sex allocation evolved toward a more female‐biased function in populations of the hermaphroditic digenean trematode Alloglossidium progeneticum that can precociously reproduce in their second hosts. In these precocious populations, parasites are forced to self‐fertilize as they remain encysted in their second hosts. In contrast, parasites in obligate three‐host populations have more opportunities to outcross in their third host. We found strong support that in populations with precocious development, allocation to male resources was greatly reduced. We also identified a potential phenotypically plastic response in a body size sex allocation relationship that may be driven by the competition for mates. These results emphasize how changes in life cycle patterns that alter mating systems can impact the evolution of reproductive traits in parasites.     

Evolution of complex life cycles in trophically transmitted helminths. I. Host incorporation and trophic ascent

Links between parasites and food webs are evolutionarily ancient but dynamic: life history theory provides insights into helminth complex life cycle origins. Most adult helminths benefit by sexual reproduction in vertebrates, often high up food chains, but direct infection is commonly constrained by a trophic vacuum between free‐living propagules and definitive hosts. Intermediate hosts fill this vacuum, facilitating transmission to definitive hosts. The central question concerns why sexual reproduction, and sometimes even larval growth, is suppressed in intermediate hosts, favouring growth arrest at larval maturity in intermediate hosts and reproductive suppression until transmission to definitive hosts? Increased longevity and higher growth in definitive hosts can generate selection for larger parasite body size and higher fecundity at sexual maturity. Life cycle length is increased by two evolutionary mechanisms, upward and downward incorporation, allowing simple (one‐host) cycles to become complex (multihost). In downward incorporation, an intermediate host is added below the definitive host: models suggest that downward incorporation probably evolves only after ecological or evolutionary perturbations create a trophic vacuum. In upward incorporation, a new definitive host is added above the original definitive host, which subsequently becomes an intermediate host, again maintained by the trophic vacuum: theory suggests that this is plausible even under constant ecological/evolutionary conditions. The final cycle is similar irrespective of its origin (upward or downward). Insights about host incorporation are best gained by linking comparative phylogenetic analyses (describing evolutionary history) with evolutionary models (examining selective forces). Ascent of host trophic levels and evolution of optimal host taxa ranges are discussed.