Adaptive division of growth and development between hosts in helminths with two-host life cycles.

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.

Complex life-cycles in trophically transmitted helminths: Do the benefits of increased growth and transmission outweigh generalism and complexity costs?

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.

Life-cycle complexity in helminths: What are the benefits?

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.

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.

Ungulate Helminth Transmission and Two Evolutionary Puzzles.

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.

A new R package and web application for detecting bilateral asymmetry in parasitic infections.

When parasites invade paired structures of their host non-randomly, the resulting asymmetry may have both pathological and ecological significance. To facilitate the detection and visualisation of asymmetric infections we have developed a free software tool, Analysis of Symmetry of Parasitic Infections (ASPI). This tool has been implemented as an R package (https://cran.r-project.org/package=aspi) and a web application (https://wayland.shinyapps.io/aspi). ASPI can detect both consistent bias towards one side, and inconsistent bias in which the left side is favoured in some hosts and the right in others. Application of ASPI is demonstrated using previously unpublished data on the distribution of metacercariae of species of Diplostomum von Nordmann, 1832 in the eyes of ruffe Gymnocephalus cernua (Linnaeus). Invasion of the lenses appeared to be random, with the proportion of metacercariae in the left and right lenses showing the pattern expected by chance. However, analysis of counts of metacercariae from the humors, choroid and retina revealed asymmetry between eyes in 38% of host fish.

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

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

Complex life cycles: why refrain from growth before reproduction in the adult niche?

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.

Exploitation of the same trophic link favors convergence of larval life-history strategies in complex life cycle helminths.

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.

Living in intermediate hosts: evolutionary adaptations in larval helminths.

In the complex life cycles of helminths, life in intermediate hosts poses special problems not covered by standard life history strategy theory. While under selection to reduce mortality and to increase growth, there is the additional problem of transmission between hosts. This review attempts to harmonise classical knowledge of the overall life cycle patterns with recent evolutionary theory as to how larval helminths exploit intermediate host tissues and avoid the gut to maximise fitness in terms of growth and mortality. It also considers the evolutionary rules by which trophically transmitted larvae are expected to increase their transmission rates to the next host.

When to go: optimization of host switching in parasites with complex life cycles.

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

When should a trophically transmitted parasite manipulate its host?

We investigate evolution of two categories of adaptive host manipulation by trophically transmitted helminths: (1) predation suppression decreases the host's mortality before the helminth is capable of establishing in its next host; (2) predation enhancement increases the existing host's mortality after it can establish in its next host. If all parasite mortality is purely random (time-independent), enhancement must increase predation by the next host sufficiently more (depending on manipulative costs) than it increases the average for all forms of host mortality; thus if host and parasite die only through random predation, manipulation must increase the "right" predation more than the "wrong" predation. But if almost all parasites die in their intermediate host through reaching the end of a fixed life span, enhancement can evolve if it increases the right predation, regardless of how much it attracts wrong predators. Although enhancement is always most favorable when it targets the right host, suppression aids survival to the time when establishment in the next host is possible: it is most favorable if it reduces all aspects of host (and hence parasite) mortality. If constrained to have selective effects, suppression should reduce the commonest form of mortality.

Spatial and temporal variations in parasite prevalence and infracommunity structure in herring (Clupea harengus L.) caught to the west of the British Isles and in the North and Baltic Seas: implications for fisheries science.

Herring Clupea harengus L. viscera were examined for endoparasitic infections as part of a multidisciplinary stock identification project (WESTHER, EU Contract no. Q5RS-2002-01 056) which applied a range of stock discrimination techniques to the same individual fishes to obtain comparable results for multivariate analysis. Spawning and non-spawning adults, and juvenile herring were caught, over 3 years, by commercial and research vessels from numerous locations to the west of the UK and Ireland, along with control samples of spawning fish from the eastern Baltic Sea, and juveniles from sites in the eastern and western North Sea, and the north of Norway. The metacercariae of two renicolid digeneans (Cercaria pythionike and Cercaria doricha), one larval nematode (Anisakis simplex s.s.) and one larval cestode (Lacistorhynchus tenuis) were selected as tag species. Results were compared with those from herring collected between 1973 and 1982, which suggested remarkable stability in the parasite fauna of herring in the study area. These species were used to compare the parasite infracommunities of spawning herring. A significant variation in infracommunity structure was observed between different spawning grounds. These results suggest that the parasite fauna of herring are spatially variable but remain temporally stable in both the short and long term. Significant differences in prevalence and abundance of infections and comparisons of parasite infracommunity enabled the separation of putative herring stocks west of the British Isles. Distinctive patterns of parasite infection in two different spawning groups off the north coast of Scotland suggest that this area is occupied by two spawning populations, one recruiting from the west of Scotland, the other from outside this area, and most likely from the eastern North Sea. The distribution patterns of L. tenuis, C. doricha and C. pythionike suggest the potential for fish that spawn in three distinct International Council for the Exploration of the Seas (ICES) management units to be present in mixed aggregations found over the Malin Shelf, with significant implications for management in this area.

Echinorhynchus salmonis Müller, 1784 absent in Britain and Ireland: re-identification of museum specimens.

Collections of 'Echinorhynchus salmonis' from Britain and Ireland deposited in The Natural History Museum, London (1921.7.19.3-12 and 1952.10.30.122-127) were re-identified as Acanthocephalus clavula and Acanthocephalus lucii respectively. The amphipod, Pontoporeia affinis, European intermediate host of E. salmonis, does not occur in the British Isles, so it is concluded that E. salmonis is absent from British and Irish freshwater fishes.