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Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host.

Benesh DP, Hafer N - Parasit Vectors (2012)

Bottom Line: However, a handful of studies with parasites, and numerous studies with free-living, complex-life-cycle animals, have found that larval size correlates poorly with fitness under particular conditions, implying that other traits, such as physiological or ontogenetic variation, may predict fitness more reliably.Infection probability in fish increased with larval size chiefly in young worms, when size and ontogeny are positively correlated, but not in older worms that had essentially completed their larval development in copepods.Transmission to sticklebacks as a small, not-yet-fully developed larva has clear costs for S. solidus, but it remains unclear what prevents the evolution of faster growth and development in this species.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany. benesh@evolbio.mpg.de

ABSTRACT

Background: For parasites with complex life cycles, size at transmission can impact performance in the next host, thereby coupling parasite phenotypes in the two consecutive hosts. However, a handful of studies with parasites, and numerous studies with free-living, complex-life-cycle animals, have found that larval size correlates poorly with fitness under particular conditions, implying that other traits, such as physiological or ontogenetic variation, may predict fitness more reliably. Using the tapeworm Schistocephalus solidus, we evaluated how parasite size, age, and ontogeny in the copepod first host interact to determine performance in the stickleback second host.

Methods: We raised infected copepods under two feeding treatments (to manipulate parasite growth), and then exposed fish to worms of two different ages (to manipulate parasite ontogeny). We assessed how growth and ontogeny in copepods affected three measures of fitness in fish: infection probability, growth rate, and energy storage.

Results: Our main, novel finding is that the increase in fitness (infection probability and growth in fish) with larval size and age observed in previous studies on S. solidus seems to be largely mediated by ontogenetic variation. Worms that developed rapidly (had a cercomer after 9 days in copepods) were able to infect fish at an earlier age, and they grew to larger sizes with larger energy reserves in fish. Infection probability in fish increased with larval size chiefly in young worms, when size and ontogeny are positively correlated, but not in older worms that had essentially completed their larval development in copepods.

Conclusions: Transmission to sticklebacks as a small, not-yet-fully developed larva has clear costs for S. solidus, but it remains unclear what prevents the evolution of faster growth and development in this species.

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Infection rate of procercoids in the high and low feeding treatments after 11 and 17 days in copepods. Error bars represent the 95% CI and numbers within columns are sample sizes.
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Figure 3: Infection rate of procercoids in the high and low feeding treatments after 11 and 17 days in copepods. Error bars represent the 95% CI and numbers within columns are sample sizes.

Mentions: At 11 DPE, only 9.5% (11/116) of procercoids successfully infected fish, whereas 82% (82/100) were successful at 17 DPE. Given the low variation in infection success within the two age groups, there was relatively low power to detect interactions between AGE and the other predictors, so non-significant effects need to be interpreted cautiously. There was, however, a significant AGE x DEVO interaction (Wald χ12 = 5.92, P = 0.015). Fast developers had a higher infection probability 11 DPE, but not 17 DPE, and the results of Benesh et al. suggest an intermediate effect 14 DPE (Figure 1). Surprisingly, neither PROC nor its interaction with AGE was significant (Wald χ12 = 0.054, P = 0.82 and Wald χ12 = 0.026, P = 0.87, respectively), even though bigger worms seemed more successful at day 11 (and day 14) (Figure 2). Similarly, FEED seems important when considered in isolation, with procercoids from the low food treatment having lower infection rates (Figure 3), but the effect was not significant in the full model (Wald χ12 = 2.23, P = 0.135). The PROC and FEED main effects remained non-significant when their interactions with AGE were removed from the model (P = 0.84 and P = 0.09, respectively). The absence of significant PROC or FEED effects could reflect collinearity, i.e. the variation in infection attributable to these variables is better captured by AGE or DEVO.


Growth and ontogeny of the tapeworm Schistocephalus solidus in its copepod first host affects performance in its stickleback second intermediate host.

Benesh DP, Hafer N - Parasit Vectors (2012)

Infection rate of procercoids in the high and low feeding treatments after 11 and 17 days in copepods. Error bars represent the 95% CI and numbers within columns are sample sizes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3403952&req=5

Figure 3: Infection rate of procercoids in the high and low feeding treatments after 11 and 17 days in copepods. Error bars represent the 95% CI and numbers within columns are sample sizes.
Mentions: At 11 DPE, only 9.5% (11/116) of procercoids successfully infected fish, whereas 82% (82/100) were successful at 17 DPE. Given the low variation in infection success within the two age groups, there was relatively low power to detect interactions between AGE and the other predictors, so non-significant effects need to be interpreted cautiously. There was, however, a significant AGE x DEVO interaction (Wald χ12 = 5.92, P = 0.015). Fast developers had a higher infection probability 11 DPE, but not 17 DPE, and the results of Benesh et al. suggest an intermediate effect 14 DPE (Figure 1). Surprisingly, neither PROC nor its interaction with AGE was significant (Wald χ12 = 0.054, P = 0.82 and Wald χ12 = 0.026, P = 0.87, respectively), even though bigger worms seemed more successful at day 11 (and day 14) (Figure 2). Similarly, FEED seems important when considered in isolation, with procercoids from the low food treatment having lower infection rates (Figure 3), but the effect was not significant in the full model (Wald χ12 = 2.23, P = 0.135). The PROC and FEED main effects remained non-significant when their interactions with AGE were removed from the model (P = 0.84 and P = 0.09, respectively). The absence of significant PROC or FEED effects could reflect collinearity, i.e. the variation in infection attributable to these variables is better captured by AGE or DEVO.

Bottom Line: However, a handful of studies with parasites, and numerous studies with free-living, complex-life-cycle animals, have found that larval size correlates poorly with fitness under particular conditions, implying that other traits, such as physiological or ontogenetic variation, may predict fitness more reliably.Infection probability in fish increased with larval size chiefly in young worms, when size and ontogeny are positively correlated, but not in older worms that had essentially completed their larval development in copepods.Transmission to sticklebacks as a small, not-yet-fully developed larva has clear costs for S. solidus, but it remains unclear what prevents the evolution of faster growth and development in this species.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany. benesh@evolbio.mpg.de

ABSTRACT

Background: For parasites with complex life cycles, size at transmission can impact performance in the next host, thereby coupling parasite phenotypes in the two consecutive hosts. However, a handful of studies with parasites, and numerous studies with free-living, complex-life-cycle animals, have found that larval size correlates poorly with fitness under particular conditions, implying that other traits, such as physiological or ontogenetic variation, may predict fitness more reliably. Using the tapeworm Schistocephalus solidus, we evaluated how parasite size, age, and ontogeny in the copepod first host interact to determine performance in the stickleback second host.

Methods: We raised infected copepods under two feeding treatments (to manipulate parasite growth), and then exposed fish to worms of two different ages (to manipulate parasite ontogeny). We assessed how growth and ontogeny in copepods affected three measures of fitness in fish: infection probability, growth rate, and energy storage.

Results: Our main, novel finding is that the increase in fitness (infection probability and growth in fish) with larval size and age observed in previous studies on S. solidus seems to be largely mediated by ontogenetic variation. Worms that developed rapidly (had a cercomer after 9 days in copepods) were able to infect fish at an earlier age, and they grew to larger sizes with larger energy reserves in fish. Infection probability in fish increased with larval size chiefly in young worms, when size and ontogeny are positively correlated, but not in older worms that had essentially completed their larval development in copepods.

Conclusions: Transmission to sticklebacks as a small, not-yet-fully developed larva has clear costs for S. solidus, but it remains unclear what prevents the evolution of faster growth and development in this species.

Show MeSH
Related in: MedlinePlus