Parasite evolution of host manipulation strategies with fluctuating ecological dynamics.

Trophically transmitted parasites often infect an intermediate prey host and manipulate their behaviour to make predation more likely, thus facilitating parasite transmission to the definitive host. However, it is unclear when such a manipulation strategy should be expected to evolve. We develop the first evolutionary invasion model to explore the evolution of manipulation strategies that are in a trade-off with parasite production of free-living spores. We find that the size of the susceptible prey population together with the threat of predation drives manipulation evolution. We find that it is only when the susceptible prey population is large and the threat of predation is relatively small that selection favours manipulation strategies over spore production. We also confirm that the system exhibits cyclic population dynamics, and this can influence the qualitative direction of selection.

Parasites alter food-web topology of a subarctic lake food web and its pelagic and benthic compartments.

We compared three sets of highly resolved food webs with and without parasites for a subarctic lake system corresponding to its pelagic and benthic compartments and the whole-lake food web. Key topological food-web metrics were calculated for each set of compartments to explore the role parasites play in food-web topology in these highly contrasting webs. After controlling for effects from differences in web size, we observed similar responses to the addition of parasites in both the pelagic and benthic compartments demonstrated by increases in trophic levels, linkage density, connectance, generality, and vulnerability despite the contrasting composition of free-living and parasitic species between the two compartments. Similar effects on food-web topology can be expected with the inclusion of parasites, regardless of the physical characteristics and taxonomic community compositions of contrasting environments. Additionally, similar increases in key topological metrics were found in the whole-lake food web that combines the pelagic and benthic webs, effects that are comparable to parasite food-web analyses from other systems. These changes in topological metrics are a result of the unique properties of parasites as infectious agents and the links they participate in. Trematodes were key contributors to these results, as these parasites have distinct characteristics in aquatic systems that introduce new link types and increase the food web's generality and vulnerability disproportionate to other parasites. Our analysis highlights the importance of incorporating parasites, especially trophically transmitted parasites, into food webs as they significantly alter key topological metrics and are thus essential for understanding an ecosystem's structure and functioning.

Distinct evolutionary lineages of Schistocephalus parasites infecting co-occurring sculpin and stickleback fishes in Alaska.

Sculpins (coastrange and slimy) and sticklebacks (ninespine and threespine) are widely distributed fishes cohabiting 2 south-central Alaskan lakes (Aleknagik and Iliamna), and all these species are parasitized by cryptic diphyllobothriidean cestodes in the genus Schistocephalus. The goal of this investigation was to test for host-specific parasitic relationships between sculpins and sticklebacks based upon morphological traits (segment counts) and sequence variation across the NADH1 gene. A total of 446 plerocercoids was examined. Large, significant differences in mean segment counts were found between cestodes in sculpin (mean = 112; standard deviation [s.d.] = 15) and stickleback (mean = 86; s.d. = 9) hosts within and between lakes. Nucleotide sequence divergence between parasites from sculpin and stickleback hosts was 20.5%, and Bayesian phylogenetic analysis recovered 2 well-supported clades of cestodes reflecting intermediate host family (i.e. sculpin, Cottidae vs stickleback, Gasterosteidae). Our findings point to the presence of a distinct lineage of cryptic Schistocephalus in sculpins from Aleknagik and Iliamna lakes that warrants further investigation to determine appropriate evolutionary and taxonomic recognition.

Endoparasitic helminth fauna and diet of Geophagus sveni (Pisces) in Upper Paraná River basin.

In freshwater ecosystems, parasite infection patterns are influenced by factors including spatial-temporal variations, host diet, and habitat. Fish often change diets, affecting their parasite communities. This study focused on non-native host fish Geophagus sveni, aiming to characterize diet and endoparasitic helminth fauna patterns in the invaded area, investigating spatial and seasonal possible differences of endoparasite infections and correlating with host diet, in São José dos Dourados River and Tietê River areas. The host fish were collected in these areas during the dry and rainy season using gillnets. The endoparasites were collected and preserved in alcohol and identified using taxonomic methods, and stomach contents were examined for diet analysis. Parasitism descriptors were calculated and evaluated spatially and seasonally by ANOVA and the Kruskal-Wallis tests. PERMANOVA assessed G. sveni diet differences, and RDA correlated the endohelminth abundance with the host diet. Two endoparasites were recorded: metacercariae of Austrodiplostomum compactum (Trematoda) and larvae and adults of Raphidascaris (Sprentascaris) lanfrediae (Nematoda). Spatial differences were observed for the mean abundance and prevalence of R. (S.) lanfrediae and A. compactum prevalence. Seasonal variations of parasitic descriptors occurred for the nematode in the Tietê River area. The detritus and aquatic insects were the most consumed items by G. sveni. Detritus consumption positively correlates with nematode abundance. The findings indicate that factors such as artificial channels and rainfall, which can influence resource availability, may affect the fish's diet and potentially influence the structure of its endoparasite community. The study emphasizes the importance of understanding trophic chain-transmitted parasites and calls for further research in Neotropical environments.

Parasites in kelp-forest food webs increase food-chain length, complexity, and specialization, but reduce connectance.

We explored whether parasites are important in kelp forests by examining their effects on a high-quality, high-resolution kelp-forest food web. After controlling for generic effects of network size, parasites affected kelp-forest food web structure in some ways consistent with other systems. Parasites increased the trophic span of the web, increasing top predator vulnerability and the longest chain length. Unique links associated with parasites, such as concomitant predation (consumption of parasites along with their hosts by predators) increased the frequency of network motifs involving mutual consumption and decreased niche contiguity of free-living species. However, parasites also affected kelp-forest food web structure in ways not seen in other systems. Kelp-forest parasites are richer and more specialized than other systems. As a result, parasites reduced diet generality and decreased connectance in the kelp forest. Although mutual consumption motifs increased in frequency, this motif type was still a small fraction of all possible motifs, so their increase in frequency was not enough to compensate for the decrease in connectance caused by adding many specialist parasite species.

Predation and parasitism as determinants of animal personalities.

Within the same population, proactive (i.e. bolder, more exploratory, active and aggressive) and reactive (i.e. more timid, less exploratory, less active and more passive) individuals could be hypothetically maintained due a trade-off between foraging and vigilance behaviours, provided that both phenotypes differ in their state (e.g. metabolic rates, body condition or energetic needs). Yet, recent findings indicate that among-individual variation in intrinsic state can explain only a small proportion of variation in behaviour, meaning that other mechanisms, such as the presence of trophically transmitted parasites, might contribute to maintaining inter-individual behavioural differences. Empirical evidence, indeed, suggests strong relationships between certain animal personality traits and parasitic load within host populations. However, the direction of causation between these traits remains unclear: are different behaviours in infected hosts in contrast to uninfected ones the result of manipulation by parasites to increase host predation, or are some personalities inherently more susceptible to infection than others? To better understand the role of parasites in shaping behavioural differences within host populations and examine to what extent parasite manipulation and/or intrinsic differences in parasite susceptibility contribute to maintaining behavioural differences, we used a simulation approach and analysed the change in the frequencies of proactive and reactive individuals over time under different predation and starvation scenarios, when individual phenotype either affected a host's risk of infection or not. We found that in the absence of parasites, predation pressure strongly affected the expression of host personality, but the trade-off between foraging and vigilance behaviours alone could not explain the maintenance of inter-individual behavioural differences without temporal variation in predation pressure. By contrast, in the presence of parasites, the two host phenotypes could coexist within populations even when individuals experienced no temporal variations in predation risk, but only when proactive and reactive hosts were equally susceptible to parasitism. Our findings, thus, indicate that parasites can play an important role in maintaining genetic diversity in their host populations in addition to generating behavioural differences though manipulation.

The plot thickens: Ovipleistophora diplostomuri infects two additional species of Florida crayfish.

Ovipleistophora (Microsporidia) is a globally distributed genus of obligate parasites that infect fish, Crustacea, and trematodes. We report on two additional crayfish hosts, Procambarus pictus (Simms Creek, Florida) and Procambarus fallax (Santa Fe River, Florida), that exhibited signs of high-intensity microsporidian infection in the musculature. Sequence data (SSU) for the isolates were 99.79% and 99.97% similar to Ovipleistophora diplostomuri parasitizing Procambarus bivittatus. Additional screening of regional fish species (Lepomis macrochirus) revealed additional microsporidian diversity (Potaspora) but did not include Ovipleistophora. Detecting Clade V isolates in multiple host groups provides further evidence for trophic transmission among Clade V microsporidia.

Hepatozoon parasites (Apicomplexa: Hepatozoidae) in fish Hoplias aimara (Characiformes, Erythrinidae) from the Eastern Amazon, Brazil.

This study reports the occurrence of parasites belonging to the Hepatozoon genus in fish Hoplias aimara from the Eastern Amazon. Fish (n = 54) were sampled from the Falsino River, located in the Amapá National Forest (FLONA), in the state of Amapá, northern Brazil. Fresh liver preparations were examined in the field between a slide and a coverslip under a light microscope. Cysts containing Hepatozoon cystozoites were observed in the liver of 5 (9%) out of 54 H. aimara individuals. The cysts were ovoid (mean dimensions 10.28 × 9.8 µm), presenting up to four elongated cystozoites (mean dimensions 11.04 × 1.68 µm), containing 1 to 4 residual bodies of different sizes. A single liver sample containing cysts was submitted to DNA extraction and PCR analyses based on a fragment of the 18S rRNA gene. The sequencing revealed a 465 bp fragment exhibiting 99% query coverage, 0.0 E-value, and 98.7% identity with Hepatozoon caimani (MF322538 and MF322539), detected in caimans (Caiman yacare) from Brazil. This is the first report of the occurrence of cysts containing Hepatozoon cystozoites in free-living fishes.

Trade-Offs with Growth Limit Host Range in Complex Life-Cycle Helminths.

AbstractParasitic 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.

Parasite prevalence in intermediate hosts increases with waterbody age and abundance of final hosts.

Prevalence of a parasite may be influenced by age of the habitat (= time available for hosts and parasites to colonize habitats), assemblage composition of host and non-host species, or biotic and abiotic habitat features. For a trophically transmitted parasite, the intermediate host may be consumed by both final hosts and 'dead-end' predators that are incompetent to host the parasite. We tested biotic and abiotic factors that might influence parasite prevalence in a freshwater host-parasite system using a dataset collected from 36 water bodies in the vicinity of Edmonton, Alberta, Canada. In this system, eggs of thorny-headed worms (Acanthocephala: Polymorphus spp.) are eaten by intermediate-host amphipods (Gammarus lacustris Sars), which are then consumed by final vertebrate hosts (certain aquatic birds and muskrats) and various non-host waterbird species. We found that acanthocephalan prevalence in amphipods was positively correlated with waterbody age and with abundance of final-host species. In contrast, abundance of the intermediate host G. lacustris was less important and was negatively correlated with parasite prevalence ('encounter-dilution effect'). Similarly, parasite prevalence showed a marginally significant and negative correlation with abundance of 'dead-end' Gammarus-eating birds. We conclude that in our study system, time available for colonization and abundance of final hosts are more important for parasite prevalence in intermediate hosts than is abundance of intermediate and dead-end hosts.

Ovipleistophora diplostomuri, a parasite of fish and their trematodes, also infects the crayfish Procambarus bivittatus.

Ovipleistophora diplostomuri (Microsporidia) is an obligate parasite of fish and trematodes in the US. In April 2019, an individual crayfish, Procambarus bivittatus (Escambia River, Florida), with a high-intensity microsporidian infection was delivered to the Emerging Pathogens Institute. Histological analysis determined that infection was restricted to the muscle tissue. Molecular diagnostics (PCR) provided 952 bp of the parasite SSU (18S) sequence. The isolate was 99.16% similar to O. diplostomuri identified from blue gill and their trematode parasites in Washington, USA. This discovery increases our understanding of Microsporidia within aquatic trophic networks, supporting the theory that the Ovipleistophora share complex relationships with vertebrates, invertebrates and helminth parasites.

Novel infections of Corynosoma enhydri and Profilicollis sp. (Acanthocephala: Polymorphidae) identified in sea otters Enhydra lutris.

Infectious disease is a major cause of mortality for sea otters Enhydra lutris, a keystone species of continued concern for conservationists. Parasitic infection has long been identified as a cause of mortality in otters in both Alaska and California, USA. Corynosoma enhydri (Acanthocephala) is the only parasite that uses sea otters as its primary definitive host and is highly prevalent in otter populations; however, it is generally considered unimportant both pathologically and ecologically, although this assumption is based on limited empirical knowledge. Research has instead focused on Profilicollis infections (P. major, P. kenti, P. altmani) as a significant source of otter mortality due to associated enteritis and peritonitis, which are threats to otter health. Here we describe acanthocephalan infections in sea otters by Profilicollis spp. and C. enhydri, from a survey comparing C. enhydri infections between northern sea otters E. lutris kenyoni (n = 12) and southern sea otters E. lutris nereis (n = 19). We report a novel infection of C. enhydri in a pup approximately 1 mo of age, which shows that the early introduction to solid food at around 3 wk by their mothers may lead to subsequent infection via infected prey items. We also document the first 2 known cases of Profilicollis infection in northern sea otters, which may present an unknown threat to the Alaskan population, or may be an interesting example of accidental infection.

Food web structure selects for parasite host range.

Complex life cycle parasites, including helminths, use intermediate hosts for development and definitive hosts for reproduction, with interactions between the two host types governed by food web structure. I study how a parasite's intermediate host range is controlled by the diet breadth of definitive host species and the cost of parasite generalism, a putative fitness cost that assumes host range trades off against fitness derived from a host species. In spite of such costs, a benefit to generalism may occur when the definitive host exhibits a large diet breadth, enhancing transmission of generalist parasites via consumption of a broad array of infected intermediate hosts. I develop a simple theoretical model to demonstrate how different host range infection strategies are differentially selected for across a gradient of definitive host diet breadth according to the cost of generalism. I then use a parasitic helminth-host database in conjunction with a food web database to show that diet breadth of definitive hosts promotes generalist infection strategies at the intermediate host level, indicating relatively low costs of parasite generalism among helminths.

Tapeworm manipulation of copepod behaviour: parasite genotype has a larger effect than host genotype.

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.

Inter-population variation in the intensity of host manipulation by the fish acanthocephalan Pomphorhynchus tereticollis: are differences driven by predation risk?

Many trophically-transmitted parasites induce behavioural alteration in their intermediate hosts that tend to increase host vulnerability to predation. Inter-population variability in parasite-induced alterations is expected to arise from variable local opportunities for trophic transmission. Yet, this hypothesis has not been investigated so far. We addressed the issue in four populations of the fish parasite Pomphorhynchus tereticollis (Acanthocephala), using variable fish biomass density as a proxy for transmission opportunities. We found variation in the intensity of parasite-induced changes in phototaxis and refuge use among populations. Two of the populations with the lowest predator biomass exhibited the highest levels of behavioural manipulation and prevalence, as expected at low transmission opportunities. They also exhibited micro-habitat segregation between infected and uninfected gammarids in the field. In addition, infection had variable effects on two physiological defence systems, immunity and antioxidant capacity, and on total protein content. Overall, our study brings partial support to the prediction that host manipulation and prevalence should be higher at low predator biomass. Although stronger evidence should be sought by increasing population replicates, our study points to the importance of the ecological context, specifically transmission opportunities brought about by predation pressure, for the evolution of parasite manipulation in trophically-transmitted parasites.

Revealing trophic transmission pathways of marine tapeworms.

Parasites are important components of natural systems, and among their various roles, parasites strongly influence the flow of energy between and within food webs. Over 1000 tapeworm species are known to parasitise elasmobranchs, although full life cycles are resolved for fewer than 10 of them. The lack in resolution stems from the inability to distinguish larval from adult stages using morphology alone. Molecular elucidation of trophic transmission pathways is the next step in understanding the role of hosts and parasites within food webs. We investigated the parasite assemblage of New Zealand's rough skate, Zearaja nasuta. Skates and their prey items (obtained from the skates' stomachs) were dissected for the recovery of adult and larval tapeworms, respectively. A fragment of the 28S rDNA region was amplified for worm specimens with the aim to confirm species identity of parasites within rough skates and to uncover trophic transmission pathways that exploit the predation links between rough skates and their prey. We identified seven species of tapeworms from four tapeworm orders. Four trophic transmission pathways were resolved between three prey items from skates stomachs and skates, and one pathway between larval tapeworm sequence from a New Zealand sole and skate, i.e. a genetic match was found between larval tapeworms in prey and adult worms in skates. We report the first case of an adult trypanorhynch parasitising rough skate. These findings contribute to our limited understanding of cestode life cycles as well as providing insights into the importance of predator-prey relationships for parasite transmission.

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

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

Winning the arms race: host-parasite shared evolutionary history reduces infection risks in fish final hosts.

Parasite manipulation of intermediate hosts evolves to increase parasite trophic transmission to final hosts, yet counter selection should act on the final host to reduce infection risk and costs. However, determining who wins this arms race and to what extent is challenging. Here, for the first time, comparative functional response analysis quantified final host consumption patterns with respect to intermediate host parasite status. Experiments used two evolutionarily experienced fish hosts and two naive hosts, and their amphipod intermediate hosts of the acanthocephalan parasite Pomphorhynchus tereticollis The two experienced fish consumed significantly fewer infected than non-infected prey, with lower attack rates and higher handling times towards the former. Conversely, the two naive fish consumed similar numbers of infected and non-infected prey at most densities, with similar attack rates and handling times towards both. Thus, evolutionarily experienced final hosts can reduce their infection risks and costs via reduced intermediate host consumption, with this not apparent in naive hosts.

Cannibalism and Infectious Disease: Friends or Foes?

Cannibalism occurs in a majority of both carnivorous and noncarnivorous animal taxa from invertebrates to mammals. Similarly, infectious parasites are ubiquitous in nature. Thus, interactions between cannibalism and disease occur regularly. While some adaptive benefits of cannibalism are clear, the prevailing view is that the risk of parasite transmission due to cannibalism would increase disease spread and, thus, limit the evolutionary extent of cannibalism throughout the animal kingdom. In contrast, surprisingly little attention has been paid to the other half of the interaction between cannibalism and disease, that is, how cannibalism affects parasites. Here we examine the interaction between cannibalism and parasites and show how advances across independent lines of research suggest that cannibalism can also reduce the prevalence of parasites and, thus, infection risk for cannibals. Cannibalism does this by both directly killing parasites in infected victims and by reducing the number of susceptible hosts, often enhanced by the stage-structured nature of cannibalism and infection. While the well-established view that disease should limit cannibalism has held sway, we present theory and examples from a synthesis of the literature showing how cannibalism may also limit disease and highlight key areas where conceptual and empirical work is needed to resolve this debate.

A life cycle database for parasitic acanthocephalans, cestodes, and nematodes.

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.