James C. Chubb

Evolution of complex life cycles in helminth parasites

The fundamental question of how complex life cycles—where there is typically more than one host—evolve in host–parasite systems remains largely unexplored. We suggest that complex cycles in helminths without penetrative infective stages evolve by two essentially different processes, depending on where in the cycle a new host is inserted. In ‘upward incorporation’, a new definitive host, typically higher up a food web and which preys on the original definitive host, is added. Advantages to the parasite are avoidance of mortality due to the predator, greater body size at maturity and higher fecundity. The original host typically becomes an intermediate host, in which reproduction is suppressed. In ‘downward incorporation’, a new intermediate host is added at a lower trophic level; this reduces mortality and facilitates transmission to the original definitive host. These two processes should also apply in helminths with penetrative infective stages, although the mathematical conditions differ.

Seasonal occurrence of helminths in freshwater fishes. Part III. Larval Cestoda and Nematoda.

Publisher Summary This chapter discusses the life cycles and seasonal occurrence of larval cestodes and nematodes. The life cycles of all the larval cestodes and nematodes are complex, and mostly require three hosts, an invertebrate first intermediate host, the fish second intermediate host, and a suitable definitive host, which, according to parasite species, can be a fish, an amphibian, a bird, or a mammal. Many of the larval stages in fishes are of economic importance, for example, Triaenophorus crassus , Diphyllobothrium dendriticum , Ligula intestinalis , Digramma interrupta , and Eustrongylides species, or present a public health problem if eaten by man in uncooked fish, for instance, Diphyllobothrium latum . Studies on helminths in lakes and reservoirs with thermal pollution from power stations have shown that in the heated areas there were increases in abundance of L. intestinalis , speeding up of the reproductive processes. There is an unfortunate scarcity of information about seasonal variations of helminths of freshwater fishes in the tropical regions of the world.

Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda.

Publisher Summary In an ideal study of the host–parasite relationship, the fishes should be divided into age classes and length groups because parasitization is not uniform through the population. However, this ideal is achieved relatively infrequently. Absence of such information can weaken explicit assessment of data for incidence and intensity of infection. This chapter discusses the arrangement of the families and considers the seasonal occurrence of Metacercariae and that of adult trematodes in fishes. There are marked differences in the biology of the two stages as the fishes are intermediate hosts for Metacercariae and definitive hosts for adult trematodes. The chapter relates the seasonal studies on Metacercariae and adult trematodes to the major climatic zones of the world. Thus, it summarizes the current knowledge in this field and highlights areas where further information should be collected to assist the understanding of the seasonal dynamics of the trematodes.

Seasonal Occurrence of Helminths in Freshwater Fishes Part I. Monogenea

Publisher Summary This chapter discusses the seasonal occurrence of monogeneans of freshwater fishes. The chapter considers monogeneans as one of five classes within the Phylum Platyhelminthes. The members of the class monogenoidea are ectoparasites of the gills, skin, and orifices of fishes, and, less frequently, of the oesophageal tracts and bladders of amphibians and turtles. The chapter discusses the subclass polyonchoinea of seasonal studies, including order dactylogyridea, order gyrodactylidea, and order tetraonchidea. The subclass oligonchoinea of seasonal studies includes order diclybothriidea and order mazocraeidea. The chapter also discusses the seasonal studies in world climatic zones. The distributions of plants and animals are influenced by climate. Climate is determined by and varies with latitude, longitude, and altitude. It is the end product of infinite and changing combinations of temperature, wind, rain, water currents, land and water masses, mountain ranges, and vegetational cover. The climate zones are divided into tropical, subtropical, mid-latitude or temperate, polar, and mountain climates.

Cestodes in South American freshwater teleost fishes: keys to genera and brief description of species

Keys to genera of cestodes in South American freshwater teleost fishes are provided, with diagnoses of genera and short descriptions of species. Two new genera are proposed, Chambriella gen.n. for Goezeella agostinhoi Pavanelli & Santos, 1992 and G paranaensis Pavanelli & Rego, 1989, and Brooksiella gen.n. for Amphoteromorphus praeputialis Rego, Santos & Silva, 1974. Nomimoscolex magna Rego, Santos & Silva, 1974, previously species inquirenda, is transferred to the genus Proteocephalus Weinland, 1858. Goezeella nupeliensis Pavanelli & Rego, 1989 is considered a species inquirenda. Species and host lists are included.

Seasonal Occurrence of Helminths in Freshwater Fishes Part IV. Adult Cestoda, Nematoda and Acanthocephala

Publisher Summary The life cycles of virtually all the adult cestodes, nematodes, and acanthocephalans are complex and require one or two intermediate hosts, of which the second in some instances is a fish, followed by the final development to sexual maturity and egg or larval release in the definitive fish host. The chapter focuses on the schemes of classification adopted and reports the seasonal studies of the cestode, nematode, and acanthocephalan adults of various species. The seasonal information is related to the major climatic zones of the world— namely, tropical, subtropical, mid-latitude, polar, and mountain. It is noted that there is a scarcity of information about seasonal patterns of occurrence of helminths of freshwater fishes in the tropical parts of the world. The chapter considers the complexities of the seasonal dynamics involved in the life cycles of the helminth species. The study of seasonal dynamics of occurrence of fish parasites leads naturally to the wider aspects of the concepts determining the population biology of host-parasite systems.

Optimal growth strategies of larval helminths in their intermediate hosts

We consider optimal growth of larval stages in complex parasite life cycles where there is no constraint because of host immune responses. Our model predicts an individuals asymptotic size in its intermediate host, with and without competition from conspecific larvae. We match observed variations in larval growth patterns in pseudophyllid cestodes with theoretical predictions of our model. If survival of the host is vital for transmission, larvae should reduce asymptotic size as intensity increases, to avoid killing the host. The life history strategy (LHS) model predicts a size reduction <1/intensity, thus increasing the parasite burden on the host. We discuss whether body size of competing parasites is an evolved LHS or simply reflects resource constraints (RC) on growth fixed by the host, leading to a constant total burden with intensity. Growth under competition appears comparable with “the tragedy of the commons”, much analysed in social sciences. Our LHS prediction suggests that evolution generates a solution that seems cooperative but is actually selfish.

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 hosts mortality before the helminth is capable of establishing in its next host; (2) predation enhancement increases the existing hosts 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.

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 copepods 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.

Competitive growth strategies in intermediate hosts: Experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus

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