scholarly journals Recent evolution of extreme cestode growth suppression by a vertebrate host

2016 ◽  
Author(s):  
Jesse N. Weber ◽  
Natalie C. Steinel ◽  
Kum Chuan Shim ◽  
Daniel I. Bolnick
Keyword(s):  
Natural Selection ◽  
Gasterosteus Aculeatus ◽  
Growth Suppression ◽  
Threespine Stickleback ◽  
Vertebrate Host ◽  
Population Divergence ◽  
Infection Prevalence ◽  
Heritable Variation ◽  
F1 Hybrid ◽  
Schistocephalus Solidus

AbstractParasites can be a major cause of natural selection on hosts, which consequently evolve a variety of strategies to avoid, eliminate, or tolerate infection. When ecologically similar host populations present disparate infection loads, this natural variation can reveal immunological strategies underlying adaptation to infection and population divergence. For instance, the tapeworm Schistocephalus solidus persistently infects between 0% to 80% of threespine stickleback (Gasterosteus aculeatus) in lakes on Vancouver Island. To test whether these heterogeneous infection rates are due to evolved differences in immunity, we experimentally exposed lab-reared fish from high-and low-infection populations, which are not known to differ in natural exposure risk, to controlled doses of Schistocephalus. We observed heritable between-population differences in several immune traits: fish from the naturally uninfected population initiated a stronger granulocyte response to Schistocephalus infection, and their granulocytes constitutively generated threefold more reactive oxygen species (ROS). Despite these immunological differences, Schistocephalus was equally successful at establishing initial infections in both host populations. However, the low-infection fish dramatically suppressed tapeworm growth relative to high-infection fish, and parasite size was intermediate in F1 hybrid hosts. Our results show that stickleback recently evolved heritable variation in their capacity to suppress helminth growth. Comparative data from many from natural populations indicate that growth suppression is widespread but not universal and, when present, is associated with reduced infection prevalence. Host suppression of helminth somatic growth may be an important immune strategy that aids in parasite clearance, or in mitigating the fitness costs of persistent infection.SignificanceLarge parasites remain a persistent source of morbidity and mortality in humans, domesticated animals, and wildlife. Hosts are subject to strong natural selection to eliminate or tolerate these parasite infections. Here, we document the recent evolution of a striking form of resistance by a vertebrate host (threespine stickleback) against its cestode parasite (Schistocephalus solidus). After Pleistocene glacial retreat, marine stickleback colonized freshwater lakes, encountered Schistocephalus, and evolved varying levels of resistance to it. We show that a heavily-and a rarely-infected population of stickleback have similar resistance to Schistocephalus colonization, but rarely-infected fish suppress parasite growth by orders of magnitude. These populations represent ends of a natural continuum of cestode growth suppression, which is associated with reduced infection prevalence.

scholarly journals Recent evolution of extreme cestode growth suppression by a vertebrate host

2017 ◽  
Vol 114 (25) ◽  
pp. 6575-6580 ◽  
Author(s):  
Jesse N. Weber ◽  
Natalie C. Steinel ◽  
Kum Chuan Shim ◽  
Daniel I. Bolnick
Keyword(s):  
Gasterosteus Aculeatus ◽  
Natural Populations ◽  
Somatic Growth ◽  
Parasite Clearance ◽  
Growth Suppression ◽  
Population Divergence ◽  
Infection Prevalence ◽  
Heritable Variation ◽  
F1 Hybrid ◽  
High Infection

Parasites can be a major cause of natural selection on hosts, which consequently evolve a variety of strategies to avoid, eliminate, or tolerate infection. When ecologically similar host populations present disparate infection loads, this natural variation can reveal immunological strategies underlying adaptation to infection and population divergence. For instance, the tapeworm Schistocephalus solidus persistently infects 0–80% of threespine stickleback (Gasterosteus aculeatus) in lakes on Vancouver Island. To test whether these heterogeneous infection rates result from evolved differences in immunity, we experimentally exposed laboratory-reared fish from ecologically similar high-infection and no-infection populations to controlled doses of Schistocephalus. We observed heritable between-population differences in several immune traits: Fish from the naturally uninfected population initiated a stronger granulocyte response to Schistocephalus infection, and their granulocytes constitutively generate threefold more reactive oxygen species in cell culture. Despite these immunological differences, Schistocephalus was equally successful at establishing initial infections in both host populations. However, the no-infection fish dramatically suppressed tapeworm growth relative to high-infection fish, and parasite size was intermediate in F1 hybrid hosts. Our results show that stickleback recently evolved heritable variation in their capacity to suppress helminth growth by two orders of magnitude. Data from many natural populations indicate that growth suppression is widespread but not universal and, when present, is associated with reduced infection prevalence. Host suppression of helminth somatic growth may be an important immune strategy that aids in parasite clearance or in mitigating the fitness costs of persistent infection.

Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus

Parasitology ◽  
2010 ◽  
Vol 137 (11) ◽  
pp. 1681-1686 ◽  
Author(s):  
D. C. HEINS ◽  
E. L. BIRDEN ◽  
J. A. BAKER
Keyword(s):  
Gasterosteus Aculeatus ◽  
Infected Fish ◽  
Threespine Stickleback ◽  
Intensity Of Infection ◽  
Host Fish ◽  
Schistocephalus Solidus ◽  
Second Intermediate Host ◽  
Host Mortality ◽  
Abiotic And Biotic Factors ◽  
Host Behaviour

SUMMARYAn analysis of the metrics of Schistocephalus solidus infection of the threespine stickleback, Gasterosteus aculeatus, in Walby Lake, Alaska, showed that an epizootic ended between 1996 and 1998 and another occurred between 1998 and 2003. The end of the first epizootic was associated with a crash in population size of the stickleback, which serves as the second intermediate host. The likely cause of the end of that epizootic is mass mortality of host fish over winter in 1996–1997. The deleterious impact of the parasite on host reproduction and increased host predation associated with parasitic manipulation of host behaviour and morphology to facilitate transmission might also have played a role, along with unknown environmental factors acting on heavily infected fish or fish in poor condition. The second epizootic was linked to relatively high levels of prevalence and mean intensity of infection, but parasite:host mass ratios were quite low at the peak and there were no apparent mass deaths of the host. A number of abiotic and biotic factors are likely to interact to contribute to the occurrence of epizootics in S. solidus, which appear to be unstable and variable. Epizootics appear to depend on particular and, at times, rare sets of circumstances.

scholarly journals Using seasonal genomic changes to understand historical adaptation: parallel selection on stickleback in highly-variable estuaries

2020 ◽  
Author(s):  
Alan Garcia-Elfring ◽  
Antoine Paccard ◽  
Timothy J. Thurman ◽  
Ben A. Wasserman ◽  
Eric P. Palkovacs ◽  
...  
Keyword(s):  
Natural Selection ◽  
Allele Frequency ◽  
Calcium Binding ◽  
Gasterosteus Aculeatus ◽  
Environmental Changes ◽  
Threespine Stickleback ◽  
Functional Enrichment ◽  
Genomic Changes ◽  
Parallel Selection ◽  
Frequency Changes

AbstractParallel evolution is considered strong evidence for natural selection. However, few studies have investigated the process of parallel selection as it plays out in real time. The common approach is to study historical signatures of selection in populations already well adapted to different environments. Here, to document selection in action under natural conditions, we study six populations of threespine stickleback (Gasterosteus aculeatus) inhabiting bar-built estuaries that undergo seasonal cycles of environmental changes. Estuaries are periodically isolated from the ocean due to sandbar formation during dry summer months, with concurrent environmental shifts that resemble the long-term changes associated with postglacial colonization of freshwater habitats by marine populations. We used pooled whole-genome sequencing (Pool-WGS) to track seasonal allele frequency changes in these populations and search for signatures of natural selection. We found consistent changes in allele frequency across estuaries, suggesting a potential role for parallel selection. Functional enrichment among candidate genes included transmembrane ion transport and calcium binding, which are important for osmoregulation and ion balance. The genomic changes that occur in threespine stickleback from bar-built estuaries could provide a glimpse into the early stages of adaptation that have occurred in many historical marine to freshwater transitions.

Virulence of the cestode Schistocephalus solidus and reproduction in infected threespine stickleback, Gasterosteus aculeatus

1999 ◽  
Vol 77 (12) ◽  
pp. 1967-1974 ◽  
Author(s):  
David C Heins ◽  
Scarlet S Singer ◽  
John A Baker
Keyword(s):  
Gasterosteus Aculeatus ◽  
Parasitic Infection ◽  
Population Level ◽  
Reproductive Period ◽  
Threespine Stickleback ◽  
South Central ◽  
Schistocephalus Solidus ◽  
Chi Squared ◽  
Parasite Relationship ◽  
Host Parasite

We investigated the relationship between reproduction in the threespine stickleback (Gasterosteus aculeatus) and parasitism by plerocercoids of the cestode Schistocephalus solidus in Walby Lake, Alaska, by quantifying stickleback reproduction and parasite infection using 1655 fish from four samples collected in 1990-1996. Stickleback in Walby Lake largely spawned during May and June as 2-year-olds in the second spring-summer after hatching, as was the case with other stickleback populations we studied in south-central Alaska. Contrary to an earlier hypothesis that S. solidus has been selected to delay its deleterious effects on threespine stickleback, i.e., limit its infection levels, until after the stickleback have reproduced, substantial levels of parasitic infection co-occurred with the stickleback reproductive period. Chi-squared analyses of individual samples suggested that in May, infected females were as capable of producing clutches of eggs as uninfected females but in June, S. solidus inhibited clutch production. An overall analysis, however, failed to support the hypothesis that the effect of S. solidus on clutch production differed between early and late periods of the spawning season. We concluded that S. solidus inhibits the ability of female stickleback in Walby Lake to produce a clutch, and that there was no differential effect on clutch production with season. Nonetheless, 77% of all infected females produced clutches. These results contrast with those of one study in which it was found only 9% of infected females became gravid (ripe) and another report that 23% of infected females were able to mature. We offer hypotheses for the co-occurrence of stickleback reproduction and substantial parasitism at the population level and for the ability of a large proportion of infected females to produce clutches. Our results suggest that the host-parasite relationship is more complex than was previously realized.

Some effects of the cestode (Schistocephalus solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus): evolutionary aspects of a host–parasite interaction

1983 ◽  
Vol 61 (4) ◽  
pp. 901-908 ◽  
Author(s):  
J. D. McPhail ◽  
S. D. Peacock
Keyword(s):  
Adverse Effects ◽  
Breeding Season ◽  
Gasterosteus Aculeatus ◽  
Threespine Stickleback ◽  
Schistocephalus Solidus ◽  
Egg Number ◽  
Gravid Females ◽  
Host Parasite ◽  
Evolutionary Aspects ◽  
Sexually Mature

Monthly samples of threespine stickleback (Gasterosteus aculeatus) were collected from May through September 1975 from Fuller Lake, Vancouver Island. A total of 2175 adult sticklebacks were collected from 10 trap sites located at depths ranging from 0.25 to 5 m. These samples were assayed for length, weight, sex, state of maturity, and egg number (when applicable). In addition, we recorded the number and weight of the plerocercoids of a cestode tapeworm (Schistocephalus solidus) often found in the abdominal cavities of sticklebacks. The purpose of the study was to document the effects of Schistocephalus on reproduction in Gasterosteus. Stickleback spawning reached a peak in June and declined sharply through July and August. Over the entire breeding season, less than 5% of the gravid females were infected with Schistocephalus, whereas over 40% of the sexually mature but nongravid females were infected. There was no difference between breeding and nonbreeding males in the prevalence of Schistocephalus. In both sexes, the prevalence and severity of Schistocephalus infection were low in May, June, and July but increased sharply through August and September. Since the majority of Fuller Lake sticklebacks live for 1 year, the major adverse effects of Schistocephalus were confined to postreproductive adults. We hypothesize that Schistocephalus plerocercoids have been selected to delay adverse effects on their host until after the host has reproduced.

Influence of the pseudophyllidean cestode Schistocephalus solidus on oocyte development in the threespine stickleback Gasterosteus aculeatus

Parasitology ◽  
2010 ◽  
Vol 137 (7) ◽  
pp. 1151-1158 ◽  
Author(s):  
D. C. HEINS ◽  
N. J. BROWN-PETERSON
Keyword(s):  
Gasterosteus Aculeatus ◽  
Secondary Growth ◽  
Infected Fish ◽  
Threespine Stickleback ◽  
Spawning Season ◽  
Oocyte Development ◽  
Schistocephalus Solidus ◽  
Primary Growth ◽  
The Difference ◽  
Ovulatory Follicles

SUMMARYThe objective of this study was to investigate the means by which Schistocephalus solidus might reduce annual fecundity in female threespine stickleback fish (Gasterosteus aculeatus) through processes of oocyte development. Histological examinations of specimens from one lake in Alaska in 2000 and 2001 were used to analyse the effects of S. solidus on recruitment of primary growth oocytes into vitellogenesis, atresia of vitellogenic oocytes, and the interspawning interval. The ratio of primary growth to late secondary growth (late vitellogenic) oocytes was significantly greater (P<0·01) among infected fish than uninfected ones in early-season samples from 2000 and 2001, revealing a decrease in recruitment of oocytes from primary growth into vitellogenic oocytes among infected females. The difference was marginally non-significant (P=0·087) in a mid-season sample from 2001 due to reductions in the entire pool of vitellogenic (early and late secondary growth) oocytes recruited prior to the spawning season in this determinate-fecundity species. Atresia among all vitellogenic oocytes was low and did not differ between infected and uninfected females. Histological estimations of the interspawning interval using post-ovulatory follicles showed no significant differences between infected and uninfected fish, suggesting that the number of spawnings in stickleback females each spawning season is unaffected by S. solidus infection. Thus, annual fecundity appears to be reduced only through recruitment of oocytes into vitellogenesis.

scholarly journals Dimensionality and modularity of adaptive variation: Divergence in threespine stickleback from diverse environments

2021 ◽  
Author(s):  
Grant E. Haines ◽  
Louis Moisan ◽  
Alison M. Derry ◽  
Andrew P. Hendry
Keyword(s):  
Gasterosteus Aculeatus ◽  
Threespine Stickleback ◽  
The Other ◽  
Cook Inlet ◽  
Heritable Variation ◽  
Phenotypic Divergence ◽  
Multiple Phenotype ◽  
Effective Dimensionality ◽  
Plastic Responses ◽  
Trait Covariance

In nature, populations are subjected to a wide variety of environmental conditions that affect fitness and induce adaptive or plastic responses in traits, resulting in phenotypic divergence between populations. The dimensionality of that divergence, however, remains contentious. At the extremes, some contend that populations diverge along a single axis of trait covariance with greatest availability of heritable variation, even if this does not lead a population directly to its fitness optimum. Those at the other extreme argue that selection can push populations towards their fitness optima along multiple phenotype axes simultaneously, resulting in divergence in numerous dimensions. Here, we address this debate using populations of threespine stickleback (Gasterosteus aculeatus) in the Cook Inlet region of southern Alaska from lakes with contrasting ecological conditions. We calculated effective dimensionality of divergence in several trait suites (defensive, swimming, and trophic) thought to be under correlated selection pressures, as well as across all traits. We also tested for integration among the trait suites and between each trait suite and the environment. We found that populations in the Cook Inlet radiation exhibit dimensionality of phenotype high enough to preclude a single axis of divergence.

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