Autonomy and integration in complex parasite life cycles

Benesh, Daniel P.

doi:10.1017/s0031182016001311

Cited by 24 publications

(19 citation statements)

References 338 publications

(380 reference statements)

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“…Thus, both "uncoupled" and "coupled" evolutionary scenarios take place. We also agree with Benesh [75] in conclusion, that holistic thinking about parasites with complex life cycles is needed because "stages may be linked through genetics (all stages share a genome), ontogeny (larval tissues become those of adults), selection (beneficial changes in one stage can favor correlated changes in others) and the environment (carryover and parental effects)". The data obtained in our study, we hope, will serve as useful resource in further studies of complex life cycle regulation and evolution.…”

Section: Discussionsupporting

confidence: 76%

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Molecular signatures of the rediae, cercariae and adult stages in the complex life cycles of parasitic flatworms (Digenea: Psilostomatidae)

et al. 2020

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Background Parasitic flatworms (Trematoda: Digenea) represent one of the most remarkable examples of drastic morphological diversity among the stages within a life cycle. Which genes are responsible for extreme differences in anatomy, physiology, behavior, and ecology among the stages? Here we report a comparative transcriptomic analysis of parthenogenetic and amphimictic generations in two evolutionary informative species of Digenea belonging to the family Psilostomatidae. Methods In this study the transcriptomes of rediae, cercariae and adult worm stages of Psilotrema simillimum and Sphaeridiotrema pseudoglobulus, were sequenced and analyzed. High-quality transcriptomes were generated, and the reference sets of protein-coding genes were used for differential expression analysis in order to identify stage-specific genes. Comparative analysis of gene sets, their expression dynamics and Gene Ontology enrichment analysis were performed for three life stages within each species and between the two species. Results Reference transcriptomes for P. simillimum and S. pseudoglobulus include 21,433 and 46,424 sequences, respectively. Among 14,051 orthologous groups (OGs), 1354 are common and specific for two analyzed psilostomatid species, whereas 13 and 43 OGs were unique for P. simillimum and S. pseudoglobulus, respectively. In contrast to P. simillimum, where more than 60% of analyzed genes were active in the redia, cercaria and adult worm stages, in S. pseudoglobulus less than 40% of genes had such a ubiquitous expression pattern. In general, 7805 (36.41%) and 30,622 (65.96%) of genes were preferentially expressed in one of the analyzed stages of P. simillimum and S. pseudoglobulus, respectively. In both species 12 clusters of co-expressed genes were identified, and more than a half of the genes belonging to the reference sets were included into these clusters. Functional specialization of the life cycle stages was clearly supported by Gene Ontology enrichment analysis. Conclusions During the life cycles of the two species studied, most of the genes change their expression levels considerably, consequently the molecular signature of a stage is not only a unique set of expressed genes, but also the specific levels of their expression. Our results indicate unexpectedly high level of plasticity in gene regulation between closely related species. Transcriptomes of P. simillimum and S. pseudoglobulus provide high quality reference resource for future evolutionary studies and comparative analyses.

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Section: Discussionsupporting

confidence: 76%

“…Benesh [75] previously reviewed the relationships between different stages in parasitic life cycles and proposed that there is evidence for both autonomy as well as integration. Our results agree with this observation.…”

Section: Discussionmentioning

confidence: 99%

Molecular signatures of the rediae, cercariae and adult stages in the complex life cycles of parasitic flatworms (Digenea: Psilostomatidae)

et al. 2020

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“…In complex life cycles of parasites, if a parasites performance is enhanced in one host, this may benefit the performance of the next stage (i.e. a larger growing parasite may produce more nutrient rich eggs) (Benesh ).…”

Section: Discussionmentioning

confidence: 99%

Consequences of divergent temperature optima in a host–parasite system

Franke

Raifarth

Kurtz

et al. 2019

Oikos

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It was suggested that parasite infections become more severe with rising temperature, as expected during global warming. In ectothermic systems, the growth of a parasite and therefore its reproductive capacity is expected to increase with temperature. However, the outcome of the interaction depends on the temperature optima of both host and parasite. Here we used experimental infections of three‐spined stickleback fish Gasterosteus aculeatus with its specific tapeworm parasite Schistocephalus solidus to investigate in detail the temperature optima for both host and parasite. We analyzed the fitness consequences thereof, focusing on growth and immunity of the host, and growth and offspring production of the parasite as fitness correlates. We checked for potential differences among populations, using the offspring of hosts and parasites derived from four study sites in Iceland, Germany and Spain that differ in average annual temperature ranging between 4.8°C and 18.4°C. We found differences in temperature optima of host and parasites that were quite consistent across the populations: while sticklebacks grew faster and had higher immune activity at low temperatures, the parasites did not even grow fast enough to reach sexual maturity in these conditions. By contrast, with increasing temperatures, parasite growth, egg production and offspring hatching increased strongly while host immunity and growth were impaired. Our results show that divergent temperature optima of hosts and parasites can have drastic fitness consequences and support the expectation that some parasites will benefit from global warming.

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“…Annual mean temperature, besides imposing pressure on species thermal tolerance, is often an indicator of resource availability in the environment (e.g. primary productivity), which could affect parasite growth and persistence both directly and indirectly through driving host abundance and diversity (Benesh, ; Brown, ). Although differences in size measures (i.e.…”

Section: Discussionmentioning

confidence: 99%

Contrasting latitudinal gradients of body size in helminth parasites and their hosts

Dallas

Gehman

Aguirre

et al. 2019

Global Ecol Biogeogr

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Aim We examined body size scaling relationships for two developmental life stages of parasitic helminths (egg and adult) separately in relationship to latitude (i.e. Bergmann's rule), temperature and temperature seasonality. Given that helminth eggs experience environmental conditions more directly, whereas adults live inside infected host individuals, we predict stronger environmentally driven gradients of body size for eggs than for adults. Location Global. Time period Present day. Major taxa studied Parasitic helminths. Methods We compiled egg size and adult body size data (both minimum and maximum) for 265 parasitic helminth species from the literature, along with species latitudinal distribution information using an extensive global helminth occurrence database. We then examined how the average helminth egg and adult body size of all helminth species present (minimum and maximum separately) scaled with latitude, temperature and temperature variability, using generalized linear models. Results Both the egg size and the adult body size of helminths tended to decrease towards higher latitudes, although we found the opposite body size scaling pattern for their host species. Helminth sizes were also positively correlated with temperature and negatively, but more weakly, with temperature seasonality. Main conclusions Instead of following the body size patterns of their hosts, helminth parasites are more similar to other ectotherms in that they follow the converse Bergmann's rule. This pattern did not differ between helminth developmental stages, suggesting that mean annual temperature and seasonality are unlikely to be related mechanistically to body size variation in this case.

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Autonomy and integration in complex parasite life cycles

Cited by 24 publications

References 338 publications

Molecular signatures of the rediae, cercariae and adult stages in the complex life cycles of parasitic flatworms (Digenea: Psilostomatidae)

Molecular signatures of the rediae, cercariae and adult stages in the complex life cycles of parasitic flatworms (Digenea: Psilostomatidae)

Consequences of divergent temperature optima in a host–parasite system

Contrasting latitudinal gradients of body size in helminth parasites and their hosts

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