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Parasitic worms (i.e., helminths) commonly infect multiple hosts in succession. With every transmission step, they risk not infecting the next host and thus dying before reproducing. Given this risk, what are the benefits of complex life cycles? Using a dataset for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we tested whether hosts at the start of a life cycle increase transmission and whether hosts at the end of a life cycle enable growth to larger, more fecund sizes. Helminths with longer life cycles, that is, more successive hosts, infected conspicuously smaller first hosts, slightly larger final hosts, and exploited trophic links with lower predator–prey mass ratios. Smaller first hosts likely facilitate transmission because of their higher abundance and because parasite propagules were the size of their normal food. Bigger definitive hosts likely increase fecundity because parasites grew larger in big hosts, particularly endotherms. Helminths with long life cycles attained larger adult sizes through later maturation, not faster growth. Our results indicate that complex helminth life cycles are ubiquitous because growth and reproduction are highest in large, endothermic hosts that are typically only accessible via small intermediate hosts, that is, the best hosts for growth and transmission are not the same.

Parasitic worms (helminths) with complex life cycles divide growth and development between successive hosts. Using data from 597 species of acanthocephalans, cestodes, and nematodes with two‐host life cycles, we found that helminths with larger intermediate hosts were more likely to infect larger, endothermic definitive hosts, although some evolutionary shifts in definitive host mass occurred without changes in intermediate host mass. Life‐history theory predicts parasites to shift growth to hosts in which they can grow rapidly and/or safely. Accordingly, helminth species grew relatively less as larvae and more as adults if they infected smaller intermediate hosts and/or larger, endothermic definitive hosts. Growing larger than expected in one host, relative to host mass/endothermy, was not associated with growing less in the other host, implying a lack of cross‐host trade‐offs. Rather, some helminth orders had both large larvae and large adults. Within these taxa, however, size at maturity in the definitive host was unaffected by changes to larval growth, as predicted by optimality models. Parasite life‐history strategies were mostly (though not entirely) consistent with theoretical expectations, suggesting that helminths adaptively divide growth and development between the multiple hosts in their complex life cycles.

Helminth parasites are part of almost every ecosystem, with more than 300 000 species worldwide. Helminth infection dynamics are expected to be altered by climate change, but predicting future changes is difficult owing to lacking thermal sensitivity data for greater than 99.9% of helminth species. Here, we compiled the largest dataset to date on helminth temperature sensitivities and used the Metabolic Theory of Ecology to estimate activation energies (AEs) for parasite developmental rates. The median AE for 129 thermal performance curves was 0.67, similar to non-parasitic animals. Although exceptions existed, related species tended to have similar thermal sensitivities, suggesting some helminth taxa are inherently more affected by rising temperatures than others. Developmental rates were more temperature-sensitive for species from colder habitats than those from warmer habitats, and more temperature sensitive for species in terrestrial than aquatic habitats. AEs did not depend on whether helminth life stages were free-living or within hosts, whether the species infected plants or animals, or whether the species had an endotherm host in its life cycle. The phylogenetic conservatism of AE may facilitate predicting how temperature change affects the development of helminth species for which empirical data are lacking or difficult to obtain.

Why do so many parasitic worms have complex life-cycles? A complex life-cycle has at least two hypothesized costs: (i) worms with longer life-cycles, i.e. more successive hosts, must be generalists at the species level, which might reduce lifetime survival or growth, and (ii) each required host transition adds to the risk that a worm will fail to complete its life-cycle. Comparing hundreds of trophically transmitted acanthocephalan, cestode, and nematode species with different life-cycles suggests these costs are weaker than expected. Helminths with longer cycles exhibit higher species-level generalism without impaired lifetime growth. Further, risk in complex life-cycles is mitigated by increasing establishment rates in each successive host. Two benefits of longer cycles are transmission and production. Longer cycles normally include smaller (and thus more abundant) first hosts that are likely to consume parasite propagules, as well as bigger (and longer-lived) definitive hosts, in which adult worms grow to larger and presumably more fecund reproductive sizes. Additional factors, like host immunity or dispersal, may also play a role, but are harder to address. Given the ubiquity of complex life-cycles, the benefits of incorporating or retaining hosts in a cycle must often exceed the costs.

Parasitic worms (i.e. helminths) commonly infect multiple hosts in succession before reproducing. At each life cycle step, worms may fail to infect the next host, and this risk accumulates as life cycles include more successive hosts. Risk accumulation can be minimized by having high establishment success in the next host, but comparisons of establishment probabilities across parasite life stages are lacking. We compiled recovery rates (i.e. the proportion of parasites recovered from an administered dose) from experimental infections with acanthocephalans, cestodes and nematodes. Our data covered 127 helminth species and 16 913 exposed hosts. Recovery rates increased with life cycle progression (11%, 29% and 46% in first, second and third hosts, respectively), because larger worm larvae had higher recovery, both within and across life stages. Recovery declined in bigger hosts but less than it increased with worm size. Higher doses were used in systems with lower recovery, suggesting that high doses are chosen when few worms are expected to establish infection. Our results indicate that growing in the small and short-lived hosts at the start of a complex life cycle, though dangerous, may substantially improve parasites' chances of completing their life cycles.

Parasitic worms with complex life cycles have several developmental stages, with each stage creating opportunities to infect additional host species. Using a data set for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we confirmed that worms with longer life cycles (i.e., more successive hosts) infect a greater diversity of host species and taxa (after controlling for study effort). Generalism at the stage level was highest for middle life stages, the second and third intermediate hosts of long life cycles. By simulating life cycles in real food webs, we found that middle stages had more potential host species to infect, suggesting that opportunity constrains generalism. However, parasites usually infected fewer host species than expected from simulated cycles, suggesting that generalism has costs. There was no trade-off in generalism from one stage to the next, but worms spent less time growing and developing in stages where they infected more taxonomically diverse hosts. Our results demonstrate that life-cycle complexity favors high generalism and that host use across life stages is determined by both ecological opportunity and life-history trade-offs.

1. Parasites are important selective agents with the potential to limit gene flow between host populations by shaping local host immunocompetence. 2. We report on a contact zone between lake and river three‐spined sticklebacks (Gasterosteus aculeatus) that offers the ideal biogeographic setting to explore the role of parasite‐mediated selection on reproductive isolation. A waterfall acts as a natural barrier and enforces unidirectional migration from the upstream river stickleback population to the downstream river and lake populations. 3. We assessed population genetic structure and parasite communities over four years. In a set of controlled experimental infections, we compared parasite susceptibility of upstream and downstream fish by exposing laboratory‐bred upstream river and lake fish, as well as hybrids, to two common lake parasite species: a generalist trematode parasite, Diplostomum pseudospathaceum, and a host‐specific cestode, Schistocephalus solidus. 4. We found consistent genetic differentiation between upstream and downstream populations across four sampling years, even though the downstream river consisted of ~10% first‐generation migrants from the upstream population as detected by parentage analysis. Fish in the upstream population had lower genetic diversity and were strikingly devoid of macroparasites. Through experimental infections, we demonstrated that upstream fish and their hybrids had higher susceptibility to parasite infections than downstream fish. Despite this, naturally sampled upstream migrants were less infected than downstream residents. Thus, migrants coming from a parasite‐free environment may enjoy an initial fitness advantage, but their descendants seem likely to suffer from higher parasite loads. 5. Our results suggest that adaptation to distinct parasite communities can influence stickleback invasion success and may represent a barrier to gene flow, even between close and connected populations. publishedVersion

Compared with uninfected individuals, infected animals can exhibit altered phenotypes. The changes often appear beneficial to parasites, leading to the notion that modified host phenotypes are extended parasite phenotypes, shaped by parasite genes. However, the phenotype of a parasitized individual may reflect parasitic manipulation, host responses to infection or both, and disentangling the contribution of parasite genes versus host genes to these altered phenotypes is challenging. Using a tapeworm (Schistocephalus solidus) infecting its copepod first intermediate host, I performed a full-factorial, cross-infection experiment with five host and five parasite genotypes. I found that a behavioural trait modified by infection, copepod activity, was affected by both host and parasite genotype. There was no clear evidence for host genotype by parasite genotype interactions. Several observations indicated that host behaviour was chiefly determined by parasite genes: (i) all infected copepods, regardless of host or parasite genotype, exhibited behavioural changes, (ii) parasitism reduced the differences among copepod genotypes, and (iii) within infected copepods, parasite genotype had twice as large an effect on behaviour as host genotype. I conclude that the altered behaviour of infected copepods primarily represents an extended parasite phenotype, and I discuss how genetic variation in parasitic host manipulation could be maintained.

Grazing mammals, ungulates, pose two evolutionary puzzles as helminth hosts. First, why do some helminths infect intermediate hosts prior to infecting ungulates, given that grazers could directly consume propagules on vegetation? Second, ungulates are large and long-lived, so why are they occasionally intermediate instead of definitive hosts, as in taeniid cestodes? We comprehensively surveyed helminth life cycles and transmission involving ungulates. We identified six transmission routes and found that ungulate helminth parasitism has evolved some 25 times. Direct egg transmission to ungulates is rare, and we suggest this is due to a transmission barrier caused by ungulate faecal avoidance. Our survey confirmed that ungulates are almost always definitive hosts, and we discuss the exceptional cases when they are not.

SUMMARYComplex life cycles are common in free-living and parasitic organisms alike. The adaptive decoupling hypothesis postulates that separate life cycle stages have a degree of developmental and genetic autonomy, allowing them to be independently optimized for dissimilar, competing tasks. That is, complex life cycles evolved to facilitate functional specialization. Here, I review the connections between the different stages in parasite life cycles. I first examine evolutionary connections between life stages, such as the genetic coupling of parasite performance in consecutive hosts, the interspecific correlations between traits expressed in different hosts, and the developmental and functional obstacles to stage loss. Then, I evaluate how environmental factors link life stages through carryover effects, where stressful larval conditions impact parasites even after transmission to a new host. There is evidence for both autonomy and integration across stages, so the relevant question becomes how integrated are parasite life cycles and through what mechanisms? By highlighting how genetics, development, selection and the environment can lead to interdependencies among successive life stages, I wish to promote a holistic approach to studying complex life cycle parasites and emphasize that what happens in one stage is potentially highly relevant for later stages.

Schistocephalus solidus is one of the few cestodes that can be bred in vitro. Worms have typically been bred in pairs, so the parents of each offspring can clearly be assigned. From a genetic perspective, it would be useful to be able to mate an individual worm to multiple partners while still being able to distinguish among different parents. As each adult S. solidus possesses numerous reproductive complexes, cutting worms and breeding the pieces separately would facilitate such breeding designs. We halved worms before in vitro breeding and evaluated whether this affected outcrossing rates and reproductive output. Cutting did not influence clutch mass, i.e. egg number and size, or outcrossing rates, but eggs from cut worms had a lower hatching rate than eggs from uncut worms. We found that when two anterior worm halves were bred together, they produced fewer, smaller eggs with higher hatching rates, compared to two posterior halves. Moreover, once we controlled for this effect of 'worm half', the two halves of an individual worm tended to reproduce similarly under comparable circumstances. We conclude that cutting plerocercoids increases the flexibility with which this tapeworm can be experimentally bred without dramatically affecting the production of viable, outcrossed eggs.

Classical theory on mating system evolution suggests that simultaneous hermaphrodites should either outcross if they have high inbreeding depression (ID) or self-fertilize if they have low ID. However, a mixture of selfing and outcrossing persists in many species. Previous studies with the tapeworm Schistocephalus solidus have found worms to self-fertilize some of their eggs despite ID. The probability for selfing to spread depends on the relative fitness of selfers, as well as the genetic basis for ID and whether it can be effectively purged. We bred S. solidus through two consecutive generations of selfing and recorded several fitness correlates over the whole life cycle. After one round of selfing, ID was pronounced, particularly in early-life traits, and the conservatively estimated lifetime fitness of selfed progeny was only 9% that of the outcrossed controls. After a second generation of selfing, ID remained high but was significantly reduced in several traits, which is consistent with the purging of deleterious recessive alleles (the estimated load of lethal equivalents dropped by 48%). Severe ID, even if it can be rapidly purged, likely prevents transitions toward pure selfing in this parasite, although we also cannot exclude the possibility that low-level selfing has undetected benefits.

Parasitologists have worked out many complex life cycles over the last ~150 yr, yet there have been few efforts to synthesize this information to facilitate comparisons among taxa. Most existing host-parasite databases focus on particular host taxa, do not distinguish final from intermediate hosts, and lack parasite life-history information. We summarized the known life cycles of trophically transmitted parasitic acanthocephalans, cestodes, and nematodes. For 973 parasite species, we gathered information from the literature on the hosts infected at each stage of the parasite life cycle (8,510 host-parasite species associations), what parasite stage is in each host, and whether parasites need to infect certain hosts to complete the life cycle. We also collected life-history data for these parasites at each life cycle stage, including 2,313 development time measurements and 7,660 body size measurements. The result is the most comprehensive data summary available for these parasite taxa. In addition to identifying gaps in our knowledge of parasite life cycles, these data can be used to test hypotheses about life cycle evolution, host specificity, parasite life-history strategies, and the roles of parasites in food webs.

SUMMARY Trophically-transmitted parasites generally need to undergo a period of development in the intermediate host beforereachinginfectivity.During this vulnerable period, manipulationof the hostto reducesusceptibility to predation wouldbeadvantageous for parasites, because it increases the probability of surviving until infectivity and thus the probability oftransmission. We tested this ‘predation suppression’ hypothesis in 2 parasite species that use copepods as first hosts: thetapeworm Schistocephalus solidus and the nematode Camallanus lacustris. In a series of prey choice experiments, we foundthatcopepodsharbouringuninfective,still-developingwormlarvaewerelessfrequentlyconsumedbysticklebackpredatorsthan uninfected copepods. The levels of predation suppression were similar in the two parasite species, suggestive ofconvergentevolution.Additionally,copepodsharbouring2wormsofagivenspecieswerenotmoresusceptibletopredationthan those with 1 worm, suggesting that excessive larval parasite growth does not increase host susceptibility to predation.Our results support the idea that parasites can suppress intermediate host susceptibility to predation while uninfective, butwe also note that the available studies suggest that this effect is weaker than the frequently observed enhancement of hostpredation by infective helminth larvae.Key words: anti-predator behaviour, convergent evolution, Gasterosteus aculeatus, growth costs, host manipulation,Macrocyclops albidus, predation enhancement, predation suppression, transmission.

In organisms with complex life cycles, fi tness often increases with body size at the transition from larva to adult. Th e translation of larval size into fi tness, however, can depend on the source of size variation, with size, per se, not always increasing adult success. In parasitic worms, many factors infl uence larval growth, but little is known about the consequences of this growth variation. We examined how the size of the tapeworm Schistocephalus solidus in its copepod fi rst intermediate host aff ects infection success and growth in the stickleback second host. Moreover, we assessed whether the conspicuous growth variation caused by copepod size is fi tness-relevant. Using larvae of the same age, we found that larger worms had a substantially higher infection probability and they tended to still be slightly larger after several months of growth in fi sh. However, big larvae from bigger copepods did not have higher fi tness, suggesting that being large relative to the host, but not necessarily large in general, is important. Th ese fi ndings clarify some aspects of the life history strategy of S. solidus (e.g. why there is a fl at ontogenetic reaction norm across copepod stages), but also raise questions (e.g. why growth costs have been hard to document). More generally, our results indicate that larval size can correlate with fi tness in helminths, but that not all size variation is predictive of success in the next host.

SUMMARYComplex life cycle helminths use their intermediate hosts as both a source of nutrients and as transportation. There is an assumed trade-off between these functions in that parasite growth may reduce host survival and thus transmission. The virulence of larval helminths can be assessed by experimentally increasing infection intensities and recording how parasite biomass and host mortality scale with intensity. I summarize the literature on these relationships in larval helminths and I provide an empirical example using the nematodeCamallanus lacustrisin its copepod first host. In all species studied thus far, includingC. lacustris, overall parasite volume increases with intensity. Although a few studies observed host survival to decrease predictably with intensity, several studies found no intensity-dependent mortality or elevated mortality only at extreme intensities. For instance, no intensity-dependent mortality was observed in male copepods infected withC. lacustris, whereas female survival was reduced only at high intensities (>3) and only after worms were fully developed. These observations suggest that at low, natural intensity levels parasites do not exploit intermediate hosts as much as they presumably could and that increased growth would not obviously entail survival costs.

Switching from one host to the next is a critical life-history transition in parasites with complex life cycles. Growth and mortality rates are thought to influence the optimal time and size at transmission, but these rates are difficult to measure in parasites. The parasite life cycle, in particular the trophic link along which transmission occurs, may be a reasonable proxy for these rates, leading to the hypothesis that life cycle should shape life-history strategy. We compiled data on the size and age at infectivity for trophically transmitted helminths (i.e., acanthocephalans, cestodes, and nematodes), and then categorized species into trophic links (e.g., planktonic crustaceans to fish, insects to terrestrial vertebrates, etc.). Comparative analyses that explicitly included stabilizing selection within trophic links fit the data significantly better than random walk models, indicating that parasites with different life cycles have different optimal times/sizes for host switching. The major helminth groups have often independently evolved similar life cycles, and we show that this has frequently led to convergent and/or parallel evolution of size and age at infectivity. This suggests that for particular life cycles there are universal optimal transmission strategies, applicable to widely divergent taxa, although the cases of parallelism might indicate that lineage-specific constraints sometimes prevent evolution to a single adaptive peak.

The timing of habitat switching in organisms with complex life cycles is an important life history characteristic that is often influenced by the larval growth environment. Under starvation, longer developmental times are frequently observed, probably as a consequence of developmental thresholds, but prolonged ontogeny sometimes also occurs under good conditions, as organisms may take advantage of the large potential gains in body size. I investigated whether variation in growth conditions affects the larval development time of a complex life cycle tapeworm (Schistocephalus solidus) in its copepod first host. Moreover, I reviewed patterns of developmental plasticity in larval tapeworms to assess the generality of my findings. Copepod starvation weakly retarded parasite growth but did not affect development. Worms grew bigger in larger copepods, but they developed at a similar rate in large and small hosts. Thus, S. solidus does not delay ontogeny under good conditions nor does it fail to reach a developmental threshold under poor conditions. Although unusual in comparison to free-living organisms, such inflexibility is common in tapeworms. Plasticity, namely prolonged ontogeny, has been mainly observed at high infection intensities. For S. solidus, there were large cross-environment genetic correlations for development, suggesting there may be genetic constraints on the evolution of developmental plasticity.

For organisms with a complex life cycle, a large larval size is generally beneficial, but it may come at the expense of prolonged development. Individuals that grow fast may avoid this tradeoff and switch habitats at both a larger size and younger age. A fast growth rate itself can be costly, however, as it requires greater resource intake. For parasites, fast larval growth is assumed to increase the likelihood of host death before transmission to the next host occurs. Using the tapeworm Schistocephalus solidus in its copepod first intermediate host, I investigated potential constraints in the parasite’s larval life history. Fast-growing parasites developed infectivity earlier, indicating there is no functional tradeoff between size and developmental time. There was significant growth variation among full-sib worm families, but fast-growing sibships were not characterized by lower host survival or more predation-risky host behavior. Parental investment also had little effect on larval growth rates. The commonly assumed constraints on larval growth and development were not observed in this system, so it remains unclear what prevents worms from exploiting their intermediate hosts more aggressively. Electronic supplementary material The online version of this article (doi:10.1007/s00442-009-1507-6) contains supplementary material, which is available to authorized users.

It is generally assumed that resistance to parasitism entails costs. Consequently, hosts evolving in the absence of parasites are predicted to invest less in costly resistance mechanisms than hosts consistently exposed to parasites. This prediction has, however, rarely been tested in natural populations. We studied the susceptibility of three naïve, three parasitized and one recently isolated Asellus aquaticus isopod populations to an acanthocephalan parasite. We found that parasitized populations, with the exception of the isopod population sympatric with the parasite strain used, were less susceptible to the parasite than the naïve populations. Exposed but uninfected (resistant) isopods from naïve populations, but not from parasitized populations, exhibited greater mortality than controls, implying that resistance entails survival costs primarily for naïve isopods. These results suggest that parasites can drive the evolution of host resistance in the wild, and that co-existence with parasites may increase the cost-effectiveness of defence mechanisms.

Trophically transmitted parasites often alter their intermediate host's phenotype, thereby predisposing the hosts to increased predation. This is generally considered a parasite strategy evolved to enhance transmission to the next hosts. However, the adaptive value of host manipulation is not clear as it may be associated with costs, such as increased susceptibility to predators that are unsuitable next hosts for the parasites. We examined the ratio between the benefits and costs of host manipulation for transmission success of Acanthocephalus lucii (Acanthocephala), a parasite that alters the hiding behaviour and pigmentation of its isopod hosts. We experimentally compared the susceptibility of infected and uninfected isopods to predation by perch ( Perca fluvialis ; definitive host of the parasite) and dragonfly larvae (dead end). We found that the parasite predisposed the isopods to predation by both predators. However, the increased predation vulnerability of the infected isopods was higher towards perch. This suggests that, despite the costs due to non-host predation, host manipulation may still be advantageous for the parasite.

In benthic habitats, predators can generally not be detected visually, so olfaction may be particularly important for inducing anti-predation behaviors in prey organisms. Manipulative parasites infecting benthic hosts could suppress these responses so as to increase the probability of predation and thus trophic transmission. We studied how infection with the acanthocephalan Echinorhynchus borealis affects the response of the benthic amphipod Pallasea quadrispinosa to water conditioned by burbot (Lota lota), the parasite's definitive host. In normal lake water, refuge use by infected and uninfected amphipods was similar, but when exposed to burbot-conditioned water, uninfected amphipods spent much more time hiding than infected amphipods. Thus, rather than affecting ambient hiding behavior, E. borealis infection seems to alter host response to a predator. A group of amphipods sampled from a postglacial spring that is devoid of fish predators exhibited only a weak response to burbot-conditioned water, perhaps suggesting these anti-predator behaviors are costly to maintain. The hiding behavior of spring and infected amphipods was very similar. If the reduced refuge use by the spring amphipods reflects adaptation to a predator-free environment, this indicates that E. borealis severely weakens its host's anti-predator behavior. Presumably this increases the likelihood of parasite transmission.

Intermediate host exploitation by parasites is presumably constrained by the need to maintain host viability until transmission occurs. The relationship between parasitism and host survival, though, likely varies as the energetic requirements of parasites change during ontogeny. An experimental infection of an acanthocephalan (Acanthocephalus lucii) in its isopod intermediate host (Asellus aquaticus) was conducted to investigate host survival and growth throughout the course of parasite development. Individual isopods were infected by exposure to fish feces containing parasite eggs. Isopods exposed to A. lucii had reduced survival, but only early in the infection. Mean infection intensity was high relative to natural levels, but host mortality was not intensity dependent. Similarly, a group of naturally infected isopods harboring multiple cystacanths did not have lower survival than singly infected isopods. Isopods that were not exposed to the parasite exhibited sexual differences in survival and molting, but these patterns were reversed or absent in exposed isopods, possibly as a consequence of castration. Further, exposed isopods seemed to have accelerated molting relative to unexposed controls. Infection had no apparent effect on isopod growth. The effects of A. lucii on isopod survival and growth undermine common assumptions concerning parasite-induced host mortality and the resource constraints experienced by developing parasites.

Sexual differences in life history traits, such as size dimorphism, presumably arise via sexual selection and are most readily observed in adults. For complex life-cycle parasites, however, sexual selection may also have consequences for larval traits, e.g., growth in intermediate hosts. Two acanthocephalan species (Acanthocephalus lucii and Echinorhynchus borealis) were studied to determine, whether larval life histories differ between males and females. The size of female A. lucii cystacanths had a much stronger relationship with intermediate host size than males, suggesting females invest more in growth and are consequently more limited by resources. No relationship between host size and cystacanth size was observed for E. borealis. For both species, female cystacanths survived longer in a culture medium composed entirely of salts, which could suggest that females have greater energy reserves than males. A comparative analysis across acanthocephalan species indicated that sexual size dimorphism at the adult stage correlates with cystacanth dimorphism. However, the relationship was not isometric; cystacanths do not reach the same level of sexual dimorphism as adults, possibly due to resource constraints. Our results suggest that larval life histories diverge between males and females in some acanthocephalans, and this is seemingly a consequence of sexual selection acting on adults.

Non-random species associations occur in naturally sampled parasite communities. The processes resulting in predictable community structure (e.g. particular host behaviours, cross-immunity, interspecific competition) could be affected by traits that vary within a parasite species, like growth or antigenicity. We experimentally infected three-spined sticklebacks with a large tapeworm (Schistocephalus solidus) that impacts the energy needs, foraging behaviour and immune reactions of its host. The tapeworms came from two populations, characterized by high or low growth in sticklebacks. Our goal was to evaluate how this parasite, and variation in its growth, affects the acquisition of other parasites. Fish infected with S. solidus were placed into cages in a lake to expose them to the natural parasite community. We also performed a laboratory experiment in which infected fish were exposed to a fixed dose of a common trematode parasite. In the field experiment, infection with S. solidus affected the abundance of four parasite species, relative to controls. For two of the four species, changes occurred only in fish harbouring the high-growth S. solidus; one species increased in abundance and the other decreased. These changes did not appear to be directly linked to S. solidus growth though. The parasite exhibiting elevated abundance was the same trematode used in the laboratory infection. In that experiment, we found a similar infection pattern, suggesting that S. solidus affects the physiological susceptibility of fish to this trematode. Associations between S. solidus and other parasites occur and vary in direction. However, some of these associations were contingent on the S. solidus population, suggesting that intraspecific variability can affect the assembly of parasite communities.

The acanthocephalan Echinorhynchus bothniensis Zdzitowiecki and Valtonen, 1987 differs from most other species in the genus Echinorhynchus Zoega in Muller, 1776 by infecting mysids (order Mysida) instead of amphipods (order Amphipoda) as intermediate hosts. Here we report on the occurrence of E. bothniensis in mysids (Mysis segerstralei Audzijonytė et Vainola) and in its fish definitive hosts in a high Arctic lake. Out of 15 907 sampled mysids, 4.8% were infected with a mean intensity of 1.05 worms (range 1-5), although there was notable variation between samples taken in different years and sites. Larger mysids appear more likely to be infected. Of five fish species sampled, charr,Salvelinus alpinus (Linnaeus), and a benthic-feeding whitefish morph, Coregonus lavaretus (Linnaeus), were the most heavily infected (mean abundances of 80 and 15, respectively). The adult parasite population in fish exhibited a female-biased sex ratio (1.78 : 1). Although E. bothniensis is rather unique in infecting mysids, many aspects of its natural history mirror that of other acanthocephalan species.

The utility of mitochondrial DNA as a molecular marker for evolutionary studies is well recognized. However, several problems can arise when using mitochondrial DNA, one of which is the presence of nuclear mitochondrial pseudogenes, or Numts. Pseudogenes of cytochrome oxidase I were preferentially amplified from Acanthocephalus lucii (Acanthocephala) using a universal PCR approach. To verify the presence and abundance of pseudogenes, length heterogeneity analysis of the PCR fragments was performed. PCR products obtained with universal primers often contained fragments of different sizes. Cloned sequences from universal PCR products nearly always contained sequence abnormalities such as indels and/or stop codons. Based on these sequences, new primers were developed to specifically target mitochondrial DNA. Sequences obtained with these specific primers lacked abnormalities. Phylogenetic analysis produced a single most parsimonious tree in which pseudogenes obtained with universal primers grouped together as did putative mitochondrial DNA sequences obtained with specific primers. The pattern of codon bias observed in the pseudogenes suggests a single nuclear integration event from the mitochondria. This is the first reported occurrence of pseudogenes in an acanthocephalan, and it demonstrates the potential dangers associated with the use of universal primers.

Many studies have shown that photic behavior of amphipods is subject to parasitic manipulation. However, all these investigations have focused on but one property of light (i.e., intensity). This study investigated the possibility that variable wavelength sensitivity, as a potentially important component of amphipod ecology, is subject to parasitic manipulation. The photic behavior of freshwater amphipods Hyalella azteca, infected with the duck acanthocephalan Corynosoma constrictum, was tested. The phototactic responses of infected and uninfected amphipods to various wavelengths in the visible spectrum were compared, and to delineate the effects of intensity and wavelength on behavior, the preferences of amphipods for environments characterized by various combinations of light intensity and wavelength were determined. Response to blue light (400-450 nm) was little affected by infection. Amphipod response to higher red region wavelengths (600-700 nm) was altered by infection. Infected amphipods were significantly less responsive to green region light (500-550 nm), which could lead to increased wandering throughout the water column, thereby facilitating increased parasite transmission through increased predation risk. This study reinforces the subtlety with which parasites can alter their host's behavior, presumably resulting in an increased probability of being transmitted from the intermediate host to a definitive host.

Helminths often occupy defined niches in the gut of their definitive hosts. In the dioecious acanthocephalans, adult males and females usually have similar gut distributions, but sexual site segregation has been reported in at least some species. We studied the intestinal distribution of the acanthocephalan Echinorhynchus borealis von Linstow, 1901 (syn. of E. cinctulus Porta, 1905) in its definitive host, burbot (Lota lota Linnaeus). Over 80% of female worms were found in the pyloric caeca, whereas the majority of males were in the anterior two-thirds of the intestine. This difference was relatively consistent between individual fish hosts. Worms from different parts of the gut did not differ in length, so site segregation was not obviously related to worm growth or age. We found proportionally more males in the caeca when a larger fraction of the females were found there, suggesting mating opportunities influence gut distribution. However, this result relied on a single parasite infrapopulation and is thus tentative. We discuss how mating strategies and/or sexual differences in life history might explain why males and females occupy different parts of the burbot gut.

SUMMARYHost manipulation is a common strategy of parasites employed to increase their fitness by changing the phenotype of their hosts. Whether host manipulation might be affected by environmental factors such as resource availability, has received little attention. We experimentally infected laboratory-bred copepods with the cestodeSchistocephalus solidus, submitted infected and uninfected copepods to either a high or a low food treatment, and measured their behaviour. Infection reduced host activity and speed in both feeding treatments. However, the difference between the infected and uninfected copepods was smaller under low food conditions, because uninfected, but not infected, copepods moved slower under these conditions. We suggest that these differences are mediated by the physical condition of copepods rather than changes in how strongly the parasite manipulated host behaviour. Additionally, we measured three fitness-relevant traits (growth, development and infection rate in the next host) of the parasite to identify potential trade-offs with host manipulation. The largest parasites in copepods appeared the least manipulative, i.e. their hosts showed the smallest behavioural alterations, but this may again reflect variation in copepod condition, rather than life history trade-offs between parasite growth and host manipulation. Our results point to the possibility that parasite transmission depends on environmental conditions.

The acanthocephalan Echinorhynchus salmonis Muller, 1784 is a common parasite of salmonid fish, but it has rarely been reported from an intermediate host. Samples of benthic amphipods, Monoporeia affinis (Lindstrom), were taken from multiple, deep sites (usually below 70 m) in the Gulf of Bothnia over the course of more than a decade and examined for acanthocephalans. Overall, only 0.44% of 23 296 amphipods were infected, all with just a single worm. This prevalence is consistent with several previous reports of acanthocephalans in deep-water, benthic amphipods, but it appears low compared to that often reported for acanthocephalan species infecting littoral amphipods. Parasite occurrence did not exhibit a clear regional pattern (i.e. northern vs southern sites) nor did it have any relationship with site depth. At sites sampled over multiple years, parasite abundance was consistently low (mostly < 0.01), though two spikes in abundance (over 0.06) were also observed, indicating that infection can be substantially higher at particular times or in particular places. The median density of E. salmonis in samples containing the parasite was estimated as 8.4 cystacanths per m(2).

SUMMARYSimultaneous hermaphrodites maximize their fitness by optimizing their investment into male or female functions. Allocation of resources to male function (tissues, traits, and/or behaviours increasing paternity) is predicted to increase as density, and the associated level of sperm competition, increases. We tested whether the simultaneous hermaphroditic cestodeSchistocephalus solidususes cues of potential partner densities in its fish intermediate host to improve its male reproductive success in the final host. We had two worms, one originating from a multiple infection in the fish intermediate host and one from a single infection, sequentially compete to fertilize the eggs of a third worm. The fertilization rates of the two competitors nearly always differed from the 50–50 null expectation, sometimes considerably, implying there was a ‘winner’ in each experimental competition. However, we did not find a significant effect of density in the fish host (singlevsmultiple) or mating order on paternity. Additional work will be needed to identify the traits and environmental conditions that explain the high variance in male reproductive success observed in this experiment.

Classical theory on mating system evolution suggests that simultaneous hermaphrodites should either outcross if they have high inbreeding depression (ID) or self-fertilize if they have low ID. However, a mixture of selfing and outcrossing persists in many species. Previous studies with the tapeworm Schistocephalus solidus have found worms to self-fertilize some of their eggs despite ID. The probability for selfing to spread depends on the relative fitness of selfers, as well as the genetic basis for ID and whether it can be effectively purged. We bred S. solidus through two consecutive generations of selfing and recorded several fitness correlates over the whole life cycle. After one round of selfing, ID was pronounced, particularly in early-life traits, and the conservatively estimated lifetime fitness of selfed progeny was only 9% that of the outcrossed controls. After a second generation of selfing, ID remained high but was significantly reduced in several traits, which is consistent with the purging of deleterious recessive alleles (the estimated load of lethal equivalents dropped by 48%). Severe ID, even if it can be rapidly purged, likely prevents transitions toward pure selfing in this parasite, although we also cannot exclude the possibility that low-level selfing has undetected benefits.

Parents can influence the phenotype of their offspring through various mechanisms, besides the direct effect of heredity. Such parental effects are little explored in parasitic organisms, perhaps because in many parasites, per capita investment into offspring is low. I investigated whether parental identity, beyond direct genetic effects, could explain variation in the performance of the tapeworm Schistocephalus solidus in its first intermediate host, a copepod. I first determined that two breeding worms could be separated from one another after ~48 h of in vitro incubation and that the isolated worms continued producing outcrossed eggs, that is, rates self-fertilization did not increase after separation. Thus, from a breeding pair, two sets of genetically comparable eggs can be collected that have unambiguous parental identities. In an infection experiment, I found that the development of larval worms tended to vary between the two parental worms within breeding pairs, but infection success and growth rate in copepods did not. Accounting for this parental effect decreased the estimated heritability for development by nearly half. These results suggest that larval performance is not simply a function of a worm's genotype; who mothered or fathered an offspring can also affect offspring fitness, contradicting the perhaps naive idea that parasites simply produce large quantities of uniformly low-quality offspring.

Organisms with complex life cycles occupy distinct niches as larvae and adults. One presumed advantage of this is the ability to exploit different resources successively throughout ontogeny. Various taxa, however, have evolved nonfeeding, nongrowing adult stages. We show theoretically that this counterintuitive no-growth strategy is favored when the optimal larval size is greater than or equal to the optimal adult size for reproduction. We empirically investigated this in a group of parasitic worms (helminths). Helminths are transmitted trophically between hosts before reproducing in large, high-trophic-level hosts, and most undergo considerable growth as adults in their final host. Some well-studied tapeworm species (Schistocephalus, Ligula, and Digramma species) are notable exceptions; they reproduce semelparously without any growth in their final habitat (the gut of piscivorous birds). Using cross-species comparative analyses, we show that these tapeworms that do not grow in their final host (1) attain larval sizes in their last intermediate host (fishes) that are comparable to or larger than the adult sizes reached by tapeworms that do grow in the same adult niche (also piscivorous birds) and (2) are large, even as larvae, relative to the mass of their final hosts. These results are consistent with the idea that a massive larval size can make adult growth superfluous, and we discuss whether this likely applies to other complex life cycle taxa with nonfeeding, nongrowing adults.

Parasitology, 136 (8), ISSN:0031-1820, ISSN:1469-8161

Parasitology, 136 (2), ISSN:0031-1820, ISSN:1469-8161

Parasitology, 135 (5), ISSN:0031-1820, ISSN:1469-8161

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.

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.