Evolution of complex life cycles in helminth parasites.

Links between parasites and food webs are evolutionarily ancient but dynamic: life history theory provides insights into helminth complex life cycle origins. Most adult helminths benefit by sexual reproduction in vertebrates, often high up food chains, but direct infection is commonly constrained by a trophic vacuum between free-living propagules and definitive hosts. Intermediate hosts fill this vacuum, facilitating transmission to definitive hosts. The central question concerns why sexual reproduction, and sometimes even larval growth, is suppressed in intermediate hosts, favouring growth arrest at larval maturity in intermediate hosts and reproductive suppression until transmission to definitive hosts? Increased longevity and higher growth in definitive hosts can generate selection for larger parasite body size and higher fecundity at sexual maturity. Life cycle length is increased by two evolutionary mechanisms, upward and downward incorporation, allowing simple (one-host) cycles to become complex (multihost). In downward incorporation, an intermediate host is added below the definitive host: models suggest that downward incorporation probably evolves only after ecological or evolutionary perturbations create a trophic vacuum. In upward incorporation, a new definitive host is added above the original definitive host, which subsequently becomes an intermediate host, again maintained by the trophic vacuum: theory suggests that this is plausible even under constant ecological/evolutionary conditions. The final cycle is similar irrespective of its origin (upward or downward). Insights about host incorporation are best gained by linking comparative phylogenetic analyses (describing evolutionary history) with evolutionary models (examining selective forces). Ascent of host trophic levels and evolution of optimal host taxa ranges are discussed.

Parasites with complex life cycles have developed numerous phenotypic strategies, closely associated with developmental events, to enable the exploitation of different ecological niches and facilitate transmission between hosts. How these environmental shifts are regulated from a metabolic and physiological standpoint, however, still remain to be fully elucidated. We examined the transcriptomic response of Schistocephalus solidus, a trophically transmitted parasite with a complex life cycle, over the course of its development in an intermediate host, the threespine stickleback, and the final avian host. Results from our differential gene expression analysis show major reprogramming events among developmental stages. The final host stage is characterized by a strong activation of reproductive pathways and redox homoeostasis. The attainment of infectivity in the fish intermediate host-which precedes sexual maturation in the final host and is associated with host behaviour changes-is marked by transcription of genes involved in neural pathways and sensory perception. Our results suggest that un-annotated and S.solidus-specific genes could play a determinant role in host-parasite molecular interactions required to complete the parasite's life cycle. Our results permit future comparative analyses to help disentangle species-specific patterns of infection from conserved mechanisms, ultimately leading to a better understanding of the molecular control and evolution of complex life cycles.

Geoff A. Parker

Complex life cycles are a hallmark characteristic of many parasites; however, little is known about the process by which life cycles become more complex through the addition of hosts. Paratenic hosts are present in the life cycles of several phylogenetically distinct groups of helminths; this suggests that they may play a key role during this process. This study examined the development of metacercariae of Halipegus eccentricus within intermediate microcrustacean and odonate paratenic hosts. Then a comparative approach was used to evaluate how life history traits of H. eccentricus within the anuran definitive hosts differ between metacercariae of the same age that developed within an intermediate ostracod host or a paratenic odonate host. The results of this study indicate that metacercariae of H. eccentricus do not grow at the same rate in different intermediate hosts, and significant differences exist in growth within intermediate and paratenic hosts. Individuals from odonate paratenic hosts always had larger bodies and suckers than those of metacercariae of the same age that develop within microcrustacean intermediate hosts. Furthermore, metacercariae from odonates were more successful in establishing and migrating in definitive anuran hosts. Last, individuals from paratenic hosts began reproducing earlier within anuran definitive hosts than age-matched worms that develop within the intermediate hosts. Collectively these results suggest that the variation in body and sucker sizes within odonate and microcrustacean hosts may carry over to the definitive host and in the case of H. eccentricus using the paratenic host increases transmission and alters other life history traits within definitive hosts. These results indicate that using a paratenic host can affect the success of parasites in subsequent hosts, and therefore these hosts may provide benefits other than just increasing transmission by bridging an ecological gap.

In many organisms, genotypic selection may be a less effective means of adapting to unpredictable environments than is selection for phenotypic plasticity. To determine whether genotypic selection is important in the evolution of complex life cycles of amphibians that breed in seasonally ephemeral habitats, we examined whether mortality risk from habitat drying in natural populations of small-mouthed salamanders (Ambystoma texanum) corresponded to length of larval period when larvae from the same populations were grown in a common laboratory environment. Comparisons were made at two levels of organization within the species: 1) among geographic races that are under strongly divergent selection regimes associated with the use of pond and stream habitats and 2) among populations within races that use the same types of breeding habitats. Morphological evidence indicates that stream-breeding A. texanum evolved from pond-breeding populations that recently colonized streams. Larvae in streams incur heavy mortality from stream drying, so the upper bound on length of larval period is currently set by the seasonal duration of breeding sites. We hypothesized that selection would reduce length of larval period of pond-breeders that colonize streams if their larval periods are inherently longer than those of stream-breeders. The results of laboratory experiments support this hypothesis. When grown individually in a common environment, larvae from stream populations had significantly shorter larval periods than larvae from pond populations. Within races, however, length of larval period did not correlate significantly with seasonal duration of breeding sites. When males of both races were crossed to a single pond female, offspring of stream males had significantly shorter larval periods than offspring of pond males. Collectively, these data suggest that differences in complex life cycles among pond and stream-breeders are due to genotypic selection related to mortality from habitat drying. Stream larvae in the common-environment experiment were significantly smaller at metamorphosis than pond larvae. Yet, the evolution of metamorphic size cannot be explained readily by direct selection: there are no intuitively obvious advantages of being relatively small at metamorphosis in streams. A positive phenotypic correlation was observed between size at metamorphosis and length of larval period in most laboratory populations. A positive additive genetic correlation between these traits was demonstrated recently in another amphibian. Thus, we suspect that metamorphic size of stream-breeders evolved indirectly as a consequence of selection to shorten length of larval period.

A popular theoretical model for explaining the evolution of complex life cycles (CLCs) was provided by Earl Werner. The theory predicts the size at which an individual should switch stages to maximise growth rate relative to mortality rate across the life history. Werner's theory assumes that body size does not change during the transition from one phase to another (e.g. from larva to adult)—a key assumption that has not been tested systematically but could alter the predictions of the model. We quantified how growth rate and mass change across larval stages and metamorphosis for 105 species of fish, amphibians, insects, crustaceans and molluscs. Across all taxonomic groups, we found support for Werner's assumption that growth rates are maintained or increase around transitions. We found that changes in growth and mass were greatest during metamorphosis, and change in growth correlated with development time. Importantly, most species either gained or lost mass when switching to a new stage—a direct contradiction of Werner's assumption. When we explored the consequences of energy loss and gain in a numerical model, we found that individuals should switch stages at a larger and smaller size, respectively, relative to what Werner's standard theory predicts. Our results suggest that while there is support for Werner's assumption regarding growth rates, mass changes profoundly alter the timing of transitions that are predicted to maximise fitness, and therefore the original model omits an important component that may contribute to the evolution of CLCs. Future studies should test for conditions that alter the costs of transitions, so that we can have a better understanding of how mass loss or gain affects fitness. Read the free Plain Language Summary for this article on the Journal blog.

Molecular paleoecology is the application of molecular data to test hypotheses made by paleoecological scenarios. Here, we use gene regulatory analysis to test between two competing paleoecological scenarios put forth to explain the evolution of complex life cycles. The first posits that early bilaterians were holobenthic, and the evolution of macrophagous grazing drove the exploitation of the pelagos by metazoan eggs and embryos, and eventually larvae. The alternative hypothesis predicts that early bilaterians were holopelagic, and new adult stages were added on when these holopelagic forms began to feed on the benthos. The former hypothesis predicts that the larvae of protostomes and deuterostomes are not homologous, with the implication that larval-specific structures, including the apical organ, are the products of convergent evolution, whereas the latter hypothesis predicts homology of larvae, specifically homology of the apical organ. We show that in the sea urchin, Strongylocentrotus purpuratus, the transcription factors NK2.1 and HNF6 are necessary for the correct spatial expression profiles of five different cilia genes. All of these genes are expressed exclusively in the apical plate after the mesenchyme-blastula stage in cells that also express NK2.1 and HNF6. In addition, abrogation of SpNK2.1 results in embryos that lack the apical tuft. However, in the red abalone, Haliotis rufescens, NK2.1 and HNF6 are not expressed in any cells that also express these same five cilia genes. Nonetheless, like the sea urchin, the gastropod expresses both NK2.1 and FoxA around the stomodeum and foregut, and FoxA around the proctodeum. As we detected no similarity in the development of the apical tuft between the sea urchin and the abalone, these molecular data are consistent with the hypothesis that the evolution of mobile, macrophagous metazoans drove the evolution of complex life cycles multiple times independently in the late Precambrian.

Parasitologists have worked out many complex life cycles over the last ~150yr, 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.

When can multiple parasites with complex life cycles coexist under conflicts of host manipulation?

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Regulation of Polyp-to-Jellyfish Transition in Aurelia aurita

The spatial genetic structure (and gene flow) of parasites with complex life cycles, such as digeneans, has been attributed mainly to the dispersion ability of the most mobile host, which most often corresponds to the definitive host (DH). In this study, we compared the genetic structure and diversity of adult Neolebouria georgenascimentoi in two fish species (DHs) that are extensively distributed along the south-eastern Pacific (SEP). The analysis was based on the cytochrome oxidase subunit I gene sequences of parasites collected between 23°S and 45°S. In total, 202 sequences of N.georgenascimentoi in Pinguipes chilensis isolated from nine sites and 136 sequences of Prolatilus jugularis from five sites were analysed. Our results showed that N.georgenascimentoi is a species complex that includes three different parasite species; however, in this study, only lineage 1 and 2 found in P.chilensis and P.jugularis, respectively, were studied because they are widely distributed along the coastline. Lineage 1 parasites had two common haplotypes with wide distribution and unique haplotypes in northern sites. Lineage 2 had only one common haplotype with wide distribution and a large number of unique haplotypes with greater genetic diversity. Both lineages have experienced recent population expansion. Only lineage 1 exhibited a genetic structure that was mainly associated with a biogeographical break at approximately 30°S along the SEP. Our finding suggests that host access to different prey (=intermediate hosts) could affect the genetic structure of the parasite complex discovered here. Consequently, difference between these patterns suggests that factors other than DH dispersal are involved in the genetic structure of autogenic parasites.

The complexity of the life-cycle of many parasitic helminths has driven the evolution of several well-documented adaptations serving to facilitate the completion of each difficult step in the cycle. In some trematode taxa, selection has even favoured the truncation of the life-cycle: progenetic larval stages (metacercariae) are capable of producing eggs inside their usual intermediate hosts, eliminating the need to be transmitted by predation to a definitive host. In some species, progenesis is shown by all individuals, whereas in other species both the normal and truncated life-cycles coexist in the same populations. Here, the strategies chosen by normal and progenetic metacercariae of the trematode Coitocaecum parvum are investigated and compared. Normal metacercariae, i.e. metacercariae that only develop into adults following ingestion by a suitable fish definitive host, were not capable of manipulating the behaviour of their amphipod intermediate host in ways that could facilitate their capture by fish. These metacercariae were associated with increased mortality in amphipods. Progenetic metacercariae, on the other hand, showed lower virulence levels than normal metacercariae. At the time of their death, amphipods harbouring progenetic metacercariae contained close to the maximum number of eggs that can be produced by progenetic metacercariae, suggesting that the parasite lowers its virulence to keep its host alive long enough to maximize egg output. The maintenance of the 2 strategies in the C. parvum population suggests that they may have equal fitness payoffs: progenesis and low virulence guarantee the production of at least some eggs, whereas the normal life-cycle and its associated higher virulence in the intermediate host provides a low probability of much higher fecundity.

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Manipulation of host-resource dynamics impacts transmission of trophic parasites