Competitive Growth Strategies in Intermediate Hosts: Experimental Tests of a Parasite life-History Model Using the Cestode, Schistocephalus solidus

In parasites with a complex life cycle, the fitness of an individual depends on its probability of reaching the final host and on its fecundity. Because larval growth in intermediate hosts may affect both transmission and adult size, selection should optimize growth patterns that are conditional on the presence and number of conspecific competitors. A recent model predicts that the total parasite volume per host should increase with intensity if larvae are able to vary growth depending on the number of conspecifics in the host (Life History Strategy hypothesis, i.e. LHS). Further, we would here expect growth rates to increase with intensity. By contrast, under the simplest alternative hypothesis of Resource Constraints (i.e. RC), the total parasite volume should remain constant. We experimentally infected copepods Macrocyclops albidus with the cestode Schistocephalus solidus to achieve 1, 2 or 3 parasites per host taking care that hosts had similar quality status at each infection level, and compared larval growth trajectories at the three intensity levels. The asymptotic total parasite volume was larger in double and triple infections than in single infections. Furthermore, the asymptotic total parasite volume was significantly larger in triple than in double infections but only in larger copepods that were less constrained by a host-size ceiling effect. These results, together with the fact that growth rates increased with intensity, support the LHS hypothesis: procercoids of a tapeworm may “count” their conspecific competitors in their first intermediate host to harvest its resources strategically until the next step in their complex life cycle. Co-ordinating editor: A. Biere     

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.     

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.     

果实大小对油茶象幼虫生长的影响

为了明确小果油茶果实大小对油茶象幼虫生长发育的限制作用,采用Logistic方程对油茶象老熟幼虫体质量与其寄主果实体积大小的关系进行了拟合.结果表明: 油茶象幼虫体质量随果实体积增大而增长,符合Logistic模型;油茶象幼虫体质量增长符合边际效应递减原则,可分为快速增长阶段(<3.216 cm³,每果1头;<4.747 cm³,每果2头)和渐进增长阶段(>3.216 cm³,每果1头;>4.747 cm³,每果2头);油茶象寄生的最小果实阈值为1.500 cm³(每果1头)或2.539 cm³(每果2头).明确了落果中油茶象老熟幼虫逃逸的时间格局,果实收集后幼虫逃逸数量逐天递减,逃逸高峰期集中在6:00—10:00,占43.9%,尤以7:00—8:00为甚,占21.1%;幼虫体质量越大,逃逸越早.寄主果实大小对油茶象幼虫生长发育具有限制作用,亲代雌虫选择大果实产卵是增加后代适合度的一种行为适应策略.
     

Competition and host size mediate larval anuran interactions with trematode parasites

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Proximate factors affecting the larval life history of Acanthocephalus lucii (Acanthocephala)

The growth and eventual size of larval helminths in their intermediate hosts presumably has a variety of fitness consequences. Therefore, elucidating the proximate factors affecting parasite development within intermediate hosts should provide insight into the evolution of parasite life histories. An experimental infection that resulted in heavy intensities of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) permitted the examination of parasite developmental responses to variable levels of resource availability and intraspecific competition. Isopods were infected by exposure to egg-containing fish feces, and larval infrapopulations were monitored throughout the course of A. lucii development. The relative rate of parasite growth slowed over time, and indications of resource constraints on developing parasites, e.g., crowding effects, were only observed in late infections. Consequently, the factors likely representative of resource availability to larval parasites (host size and molting rate) primarily affected parasite size in late infections. Moreover, at this stage of infection, competitive interactions, gauged by variation in worm size, seemed to be alleviated by greater resources, i.e., larger hosts that molted more frequently. The relatively rapid, unconstrained growth of young parasites may be worse for host viability than the slower, resource-limited growth of larger parasites.     

Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites

Co-infecting parasite genotypes typically compete for host resources limiting their fitness. The intensity of such competition depends on whether parasites are reproducing in a host, or using it primarily as a transmission vehicle while not multiplying in host tissues (referred to as 'competition hypothesis'). Alternatively, simultaneous attack and co-infection by several parasite genotypes might facilitate parasite infection because such a diverse attack could present an additional challenge to host immune defence (referred to as 'facilitation hypothesis'). We tested the competition hypothesis by comparing the production of transmission stages (cercariae) from snails infected with one or two genotypes of the trematode Diplostomum pseudospathaceum. We found that cercarial production did not differ between the two groups of snails, suggesting lower per genotype production in double infections, and competition for host resources. Second, we tested the facilitation hypothesis by comparing parasite infection success on fishes (proportion of parasites establishing in the host) using cercariae originating from single-infected snails, double-infected snails and artificial mixtures of the single genotypes. In both cases, we found higher infection success when fishes were challenged with two parasite genotypes instead of one, supporting the facilitation hypothesis. Our results suggest that constraints defining the success of multiple genotype infections in parasites with multiple host life cycles include both between-genotype resource competition in the host and performance of host immune defences against a diverse parasite challenge.     

Parasites of coral reef fish larvae: its role in the pelagic larval stage

The pelagic larval stage is a critical component of the life cycle of most coral reef fishes, but the adaptive significance of this stage remains controversial. One hypothesis is that migrating through the pelagic environment reduces the risk a larval fish has of being parasitised. Most organisms interact with parasites, often with significant, detrimental consequences for the hosts. However, little is known about the parasites that larval fish have upon settlement, and the factors that affect the levels of parasitism. At settlement, coral reef fishes vary greatly in size and age (pelagic larval duration), which may influence the degree of parasitism. We identified and quantified the parasites of pre-settlement larvae from 44 species of coral reef fishes from the Great Barrier Reef and explored their relationship with host size and age at settlement, and phylogeny. Overall, less than 50% of the larval fishes were infected with parasites, and over 99% of these were endoparasites. A Bayesian phylogenetic regression was used to analyse host-parasite (presence and intensity) associations. The analysis showed parasite presence was not significantly related to fish size, and parasite intensity was not significantly related to fish age. A phylogenetic signal was detected for both parasite presence and intensity, indicating that, overall, closely related fish species were likely to have more similar susceptibility to parasites and similar levels of parasitism when compared to more distantly related species. The low prevalence of infection with any parasite type and the striking rarity of ectoparasites is consistent with the ‘parasite avoidance hypothesis’, which proposes that the pelagic phase of coral reef fishes results in reduced levels of parasitism.

     

Larval competition within seeds: From the behaviour process to the ecological outcome in the seed beetle Callosobruchus maculatus

Abstract Environmental conditions experienced by organisms during development can have profound impacts on adult fitness and behaviour. Internally feeding larvae unable to leave the seed selected by their mother face limitations of resource suitability and competition. The host seed may guide the larval behaviour within the seed leading to differential intensity of competition and determining its process and outcome, which varies in strains of the legume seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae). However, the intensity, process and outcome of larval competition in different hosts have yet to be simultaneously considered, the objective of the present study. Here we assessed the intensity, process and outcome of intrastrain larval competition as related to host type, and how they are interrelated. Larval competition was faced with two distinct strategies – scramble and contest competition depending on the insect strain and host seed species. The intensity of competition did not show any straight link with the process and outcome of competition. Only a single strain showed a contest competition process with likely interference between larvae, while the four other strains studied showed the process of scramble competition. The process of scramble competition, however, led to variable outcomes in mung beans based on larval competition curves. Such differences were not apparent on cowpea seeds and either the plateau or the peak expected on the larval fitness curves were not reached preventing the distinction of the competition outcome, a likely consequence of the egg laying behaviour of these strains limiting the maximum number of eggs laid per seed. Seed host species rather than seed size are the likely cause of the differences observed from the initial expectation. The strain showing the process of contest competition increased larval fitness with density of larvae emerged per seed regardless of the host species, an unexpected outcome based on theoretical models. In this case the egg laying behaviour of the adult female is probably the main fitness determinant of its progeny.     

Virulence of Corynosoma constrictum (Acanthocephala: Polymorphidae) in Hyalella azteca (Amphipoda) throughout parasite ontogeny

Development and growth of parasites depend on resources provided by the host and the parasite's ability to use them. Identifying specific costs incurred by the host provides insight for assessment of parasite energy budgets, which differ among taxa and ontogenetic stages. Data from this study were analyzed using an accelerated failure-time model with intensity as a covariate. Results indicated significantly reduced survival of amphipods, Hyalella azteca, infected with the acanthocephalan Corynosoma constrictum compared with uninfected controls. Male and female amphipod survivorship and infection intensity did not differ; however, amphipods with high-intensity infections (> 16 larvae) died earlier compared with amphipods with low-intensity infections (< 3 larvae). The majority of infected amphipods died between 12 and 24 days postexposure, a period of rapid larval development. It is hypothesized that host death may be due either to an increase in overall larval nutritional demands or to parasite-mediated depletion of a specific host substance. Results from this study suggest that developing C. constrictum satisfies energy requirements by depriving amphipod hosts of resources normally used for somatic growth and maintenance.     

Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila-Macrocheles system

Costs of resistance are expected to contribute to the maintenance of genetic variation for resistance in natural host populations. In the present study, we experimentally test for genetic trade-offs between parasite resistance and larval competitive ability expressed under varying levels of crowding and temperature. Artificial selection for increased behavioral resistance was applied against an ectoparasitic mite (Macrocheles subbadius) in replicate lines of the fruit fly Drosophila nigrospiracula. We then measured correlated responses to selection in larval competitive ability by contrasting replicate selected and control (unselected) lines in the absence of parasitism. Experiments were conducted under variable environmental conditions: two temperatures and three levels of larval density. Our results reveal a negative genetic correlation between resistance and larval-adult survival under conditions of moderate and severe intra-specific competition. At both low and high temperature, percent emergence was significantly higher among control lines than selected lines. This divergence in larval competitive ability was magnified under high levels of competition, but only at low temperature. Hence, the interaction between selection treatment and larval density was modified by temperature. As predicted, larvae experiencing medium and high levels of competition exhibited an overall reduction in female body size compared to larvae at low levels of competition. Female flies emerging from selected lines were significantly smaller than those females from control lines, but this effect was only significant under conditions of moderate to severe competition. These results provide evidence of environment-dependent trade-offs between ectoparasite resistance and larval competitive ability, a potential mechanism maintaining genetic polymorphism for resistance.     

Molecular genetic data provide support for a model of transmission dynamics in an Australian reptile tick, Bothriocroton hydrosauri

Bothriocroton hydrosauri is a three-host ixodid tick that infests large reptiles in southeastern Australia, where its most common host is a large scincid lizard Tiliqua rugosa . Based on previous ecological and behavioural studies of this system, we propose a 'ripple' model of tick population dynamics, where only a few female ticks succeed in producing surviving offspring. These females then are the centres of ripples of their progeny spreading into the broader landscape. The model predicts higher relatedness among larvae than among nymphs or adults on a host, and significant spatial autocorrelation in larvae extending further than for the later life stages. The model also predicts that adult ticks are likely to encounter related partners and that this will generate inbreeding within the population. We tested those predictions using nine polymorphic microsatellite loci on a sample of 848 ticks (464 larvae, 140 nymphs and 244 adults) collected from 98 lizard hosts from near Bundey Bore Station in South Australia. Our data support the predictions and indicate that the dynamics of transmission among hosts play an important role in parasite population structure.     

Crowding and disease: effects of host density on response to infection in a butterfly–parasite interaction

Abstract. 1. Hosts experiencing frequent variation in density are thought to benefit from allocating more resources to parasite defence when density is high (‘density‐dependent prophylaxis’). However, high density conditions can increase intra‐specific competition and induce physiological stress, hence increasing host susceptibility to infection (‘crowding‐stress hypothesis’). 2. We studied monarch butterflies (Danaus plexippus) and quantified the effects of larval rearing density on susceptibility to the protozoan parasite Ophryocystis elektroscirrha. Larvae were inoculated with parasite spores and reared at three density treatments: low, moderate, and high. We examined the effects of larval density on parasite loads, host survival, development rates, body size, and wing melanism. 3. Results showed an increase in infection probability with greater larval density. Monarchs in the moderate and high density treatments also suffered the greatest negative effects of parasite infection on body size, development rate, and adult longevity. 4. We observed greater body sizes and shorter development times for monarchs reared at moderate densities, and this was true for both unparasitised and parasite‐treated monarchs. We hypothesise that this effect could result from greater larval feeding rates at moderate densities, combined with greater physiological stress at the highest densities. 5. Although monarch larvae are assumed to occur at very low densities in the wild, an analysis of continent‐wide monarch larval abundance data showed that larval densities can reach high levels in year‐round resident populations and during the late phase of the breeding season. Treatment levels used in our experiment captured ecologically‐relevant variation in larval density observed in the wild.     

Evolution of larval competitiveness and associated life‐history traits in response to host shifts in a seed beetle

Resource competition is frequently strong among parasites that feed within small discrete resource patches, such as seeds or fruits. The properties of a host can influence the behavioural, morphological and life‐history traits of associated parasites, including traits that mediate competition within the host. For seed parasites, host size may be an especially important determinant of competitive ability. Using the seed beetle, Callosobruchus maculatus, we performed replicated, reciprocal host shifts to examine the role of seed size in determining larval competitiveness and associated traits. Populations ancestrally associated with either a small host (mung bean) or a large one (cowpea) were switched to each other's host for 36 generations. Compared to control lines (those remaining on the ancestral host), lines switched from the small host to the large host evolved greater tolerance of co‐occurring larvae within seeds (indicated by an increase in the frequency of small seeds yielding two adults), smaller egg size and higher fecundity. Each change occurred in the direction predicted by the traits of populations already adapted to cowpea. However, we did not observe the expected decline in adult mass following the shift to the larger host. Moreover, lines switched from the large host (cowpea) to the small host (mung bean) did not evolve the predicted increase in larval competitiveness or egg size, but did exhibit the predicted increase in body mass. Our results thus provide mixed support for the hypothesis that host size determines the evolution of competition‐related traits of seed beetles. Evolutionary responses to the two host shifts were consistent among replicate lines, but the evolution of larval competition was asymmetric, with larval competitiveness evolving as predicted in one direction of host shift, but not the reverse. Nevertheless, our results indicate that switching hosts is sufficient to produce repeatable and rapid changes in the competition strategy and fitness‐related traits of insect populations.     

The effects of group size, leaf size, and density on the performance of a leaf-mining moth

1. The effects of two factors, leaf size and group size, on the performance of the Tupelo leafminer, Antispila nysaefoliella (Lepidoptera: Heliozelidae), were examined by fitting growth models to mine expansion data using nonlinear mixed-effects models. 2. The rate of mine expansion served as a proxy for larval performance because of its correlation with both feeding activity and growth rate and is also the means by which a larva achieves its final mine size (or total consumption). 3. Leaf size was used as a measure of resource availability, and was expected to reduce the impact of resource competition and enhance larval performance. 4. In contrast to the unidirectional effects expected for leaf size (i.e. more resources should enhance performance), the direction for the effects of group size was expected to depend on the mechanism(s) driving the effect. For example, if there is resource competition among larvae in a group, then this could increase the feeding rates of some larvae or reduce the total consumption of others. However, if leaf mining induces host plant chemical defences, then larger groups might elicit a greater defensive response by the host plant (at the leaf), and hence, be characterized by reduced feeding and growth rates. 5. To investigate these interactions, two growth models, the Gompertz model and a modified version of the von Bertalanffy growth equation, were fitted to time series of the sizes of individual leaf mines using nonlinear mixed-effects models. Linear and nonlinear associations of each factor (group size or leaf size) with model parameters were then evaluated using a hierarchical testing procedure by determining: (i) whether inclusion of the factor produced a better-fit model, and (ii) if it did, the form of that relationship (i.e. linear or nonlinear). 6. Three patterns were detected with these analyses. (i) Leaf size had a significant positive, linear relationship with mine expansion rate. (ii) Group size had a significant quadratic relationship with mine expansion rate. (iii) The effects of leaf and group size on the maximum mine size were opposite to those found with growth rate.     

Population dynamic consequences of parasitised-larval competition in stage-structured host–parasitoid systems

Parasitism can influence many aspects of the host's behaviour and physiology, which in turn can have a profound impact on their population and evolutionary ecology. In many host–parasite interactions there is often a time lag between infection and the death of the host, yet little is known, experimentally or theoretically, about the effects that intra-class competition between parasitised and unparasitised hosts have on the host–parasite population dynamics.
In this article we address this gap in our understanding using a stage-structured mathematical model for a host–parasitoid interaction, which has been parameterised for the Plodia–Venturia experimental system.
In the case where parasitised larvae do not compete and do not cannibalise unparasitised larvae, our model predicts a wide range of host–parasitoid dynamics, ranging from host–parasitoid generation cycles, to host generation cycles with parasitoid half-generation cycles, to host–parasitoid equilibria, to host generation cycles with parasitoid extinction.
However, when parasitised larvae can compete with their unparasitised larvae counterparts, the host–parasitoid population dynamics can dramatically change. In particular, we show that high levels of competition exerted by unparasitised larvae upon parasitised larvae is more likely to lead to parasitoid extinction.
In addition, we demonstrate that unparasitised host larvae that are sufficiently susceptible to intra-class competition, or parasitised host larvae that are sufficiently strong competitors, can have a stabilising effect on the host–parasitoid population dynamics.
The implications of these theoretical results are discussed in light of our understanding of host–parasitoid interactions and host–parasite systems in general.     

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.     

Predictable modification of body size and competitive ability following a host shift by a seed beetle

Interfertile populations of the seed beetle Callosobruchus maculatus differ genetically in several behavioral, morphological, and life-history traits, including traits that affect the intensity of larval competition within seeds. Previous studies have suggested that this variation depends on differences in host size. I performed a selection experiment in which replicate beetle lines were either maintained on a small, ancestral host (mung bean) or switched to a larger, novel host (cowpea). After 40 generations, I estimated survival, development time, and adult mass on each host, both in the presence and absence of larval competition. The shift to cowpea substantially reduced body size; irrespective of rearing host, adults from the cowpea lines were more than 10% lighter than those from the mung bean lines. Switching to cowpea also improved survival and reduced development time on this host, but without decreasing performance on the ancestral host. The most striking effect of the shift to a larger host was a reduction in larval competitiveness. When two even-aged larvae co-existed within a seed, the probability that both survived to adult emergence was > or = 65% if larvae were from the cowpea lines but < or = 12% if they were from the mung bean lines. The adverse effects of competition on development time and adult mass were also less severe in the cowpea lines than in the mung bean lines. By rapidly evolving smaller size and reduced competitiveness, the cowpea lines converged toward populations chronically associated with cowpea. These results suggest that evolutionary trajectories can be predictable, and that host-specific selection can play a major role in the diversification of insect life histories. Because host shifts by small, endophagous insects are comparable to the colonization of new habitats, adaptive responses may often include traits (such as larval competitiveness) that are not directly related to host use.     

Evolution of complex life cycles in trophically transmitted helminths. II. How do life‐history stages adapt to their hosts?

We review how trophically transmitted helminths adapt to the special problems associated with successive hosts in complex cycles. In intermediate hosts, larvae typically show growth arrest at larval maturity (GALM). Theoretical models indicate that optimization of size at GALM requires larval mortality rate to increase with time between infection and GALM: low larval growth or paratenicity (no growth) arises from unfavourable growth and mortality rates in the intermediate host and low transmission rates to the definitive host. Reverse conditions favour high GALM size or continuous growth. Some support is found for these predictions. Intermediate host manipulation involves predation suppression (which decreases host vulnerability before the larva can establish in its next host) and predation enhancement (which increases host vulnerability after the larva can establish in its next host). Switches between suppression and enhancement suggest adaptive manipulation. Manipulation conflicts can occur between larvae of different ages/species a host individual. Larvae must usually develop to GALM before becoming infective to the next host, possibly due to trade‐offs, e.g. between growth/survival in the present host and infection ability for the next host. In definitive hosts, if mortality rate is constant, optimal growth before switching to reproduction is set by the growth/morality rate ratio. Rarely, no growth occurs in definitive hosts, predicted (with empirical support) when larval size on infection exceeds growth/mortality rate. Tissue migration patterns and residence sites may be explained by variations in growth/mortality rates between host gut and soma, migration costs and benefits of releasing eggs in the gut.