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Parasitism in early life: environmental conditions shape within-brood variation in responses to infection.

Granroth-Wilding HM, Burthe SJ, Lewis S, Reed TE, Herborn KA, Newell MA, Takahashi EA, Daunt F, Cunningham EJ - Ecol Evol (2014)

Bottom Line: In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses.Whole-brood growth rate was not affected by treatment, indicating that within-brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning.We show that gastrointestinal parasites can be a key component of offspring's developmental environment.

View Article: PubMed Central - PubMed

Affiliation: Centre for Immunity, Infection and Evolution, Institute of Evolutionary Biology, School of Biology, University of Edinburgh, Ashworth Laboratories King's Buildings, West Mains Rd, Edinburgh, EH9 3JT, U.K.

ABSTRACT
Parasites play key ecological and evolutionary roles through the costs they impose on their host. In wild populations, the effect of parasitism is likely to vary considerably with environmental conditions, which may affect the availability of resources to hosts for defense. However, the interaction between parasitism and prevailing conditions is rarely quantified. In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses. Offspring hierarchies, established by parents in response to uncertain rearing conditions, may be an important source of variation between individuals. Here, we use experimental antiparasite treatment across 5 years of variable conditions to test how annual population productivity (a proxy for environmental conditions) and parasitism interact to affect growth and survival of different brood members in juvenile European shags (Phalacrocorax aristotelis). In control broods, last-hatched chicks had more plastic growth rates, growing faster in more productive years. Older siblings grew at a similar rate in all years. Treatment removed the effect of environment on last-hatched chicks, such that all siblings in treated broods grew at a similar rate across environmental conditions. There were no differences in nematode burden between years or siblings, suggesting that variation in responses arose from intrinsic differences between chicks. Whole-brood growth rate was not affected by treatment, indicating that within-brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning. We show that gastrointestinal parasites can be a key component of offspring's developmental environment. Our results also demonstrate the value of considering prevailing conditions for our understanding of parasite effects on host life-history traits. Establishing how environmental conditions shape responses to parasitism is important as environmental variability is predicted to increase.

No MeSH data available.


Related in: MedlinePlus

A brood of asynchronously hatched European shags (Phalacrocorax aristotelis), aged c. 25 days, with an attending parent.
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fig01: A brood of asynchronously hatched European shags (Phalacrocorax aristotelis), aged c. 25 days, with an attending parent.

Mentions: In this study, we examine the effect of annual population productivity (a proxy of prevailing environmental conditions) on the consequences of parasitism in juvenile European shags, Phalacrocorax aristotelis (Fig.1). Individuals of this species are infected with gastrointestinal nematodes from the fish they eat (Anderson 2000; Hoberg 2005; Fagerholm and Overstreet 2008), and there is a high prevalence of infection among adults and juveniles (Reed et al. 2012; Burthe et al. 2013; Granroth-Wilding 2013). Shag chicks hatch asynchronously, and chick survival varies considerably among years. Last-hatched chicks show lower survival on average (Amundsen and Stokland 1988) and therefore potentially more variable responses to environmental conditions. Here, we experimentally manipulate parasite loads over 5 years of variable conditions to investigate the effect of gastrointestinal nematode infection on individual chick growth rate and survival in a system where we can disentangle the confounding effects of parasite distributions between related individuals. We also investigate whether these differences arise as a result of changes in parental resource provisioning to the whole brood or to changes in how resources are allocated to different members of a brood.


Parasitism in early life: environmental conditions shape within-brood variation in responses to infection.

Granroth-Wilding HM, Burthe SJ, Lewis S, Reed TE, Herborn KA, Newell MA, Takahashi EA, Daunt F, Cunningham EJ - Ecol Evol (2014)

A brood of asynchronously hatched European shags (Phalacrocorax aristotelis), aged c. 25 days, with an attending parent.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4228615&req=5

fig01: A brood of asynchronously hatched European shags (Phalacrocorax aristotelis), aged c. 25 days, with an attending parent.
Mentions: In this study, we examine the effect of annual population productivity (a proxy of prevailing environmental conditions) on the consequences of parasitism in juvenile European shags, Phalacrocorax aristotelis (Fig.1). Individuals of this species are infected with gastrointestinal nematodes from the fish they eat (Anderson 2000; Hoberg 2005; Fagerholm and Overstreet 2008), and there is a high prevalence of infection among adults and juveniles (Reed et al. 2012; Burthe et al. 2013; Granroth-Wilding 2013). Shag chicks hatch asynchronously, and chick survival varies considerably among years. Last-hatched chicks show lower survival on average (Amundsen and Stokland 1988) and therefore potentially more variable responses to environmental conditions. Here, we experimentally manipulate parasite loads over 5 years of variable conditions to investigate the effect of gastrointestinal nematode infection on individual chick growth rate and survival in a system where we can disentangle the confounding effects of parasite distributions between related individuals. We also investigate whether these differences arise as a result of changes in parental resource provisioning to the whole brood or to changes in how resources are allocated to different members of a brood.

Bottom Line: In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses.Whole-brood growth rate was not affected by treatment, indicating that within-brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning.We show that gastrointestinal parasites can be a key component of offspring's developmental environment.

View Article: PubMed Central - PubMed

Affiliation: Centre for Immunity, Infection and Evolution, Institute of Evolutionary Biology, School of Biology, University of Edinburgh, Ashworth Laboratories King's Buildings, West Mains Rd, Edinburgh, EH9 3JT, U.K.

ABSTRACT
Parasites play key ecological and evolutionary roles through the costs they impose on their host. In wild populations, the effect of parasitism is likely to vary considerably with environmental conditions, which may affect the availability of resources to hosts for defense. However, the interaction between parasitism and prevailing conditions is rarely quantified. In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses. Offspring hierarchies, established by parents in response to uncertain rearing conditions, may be an important source of variation between individuals. Here, we use experimental antiparasite treatment across 5 years of variable conditions to test how annual population productivity (a proxy for environmental conditions) and parasitism interact to affect growth and survival of different brood members in juvenile European shags (Phalacrocorax aristotelis). In control broods, last-hatched chicks had more plastic growth rates, growing faster in more productive years. Older siblings grew at a similar rate in all years. Treatment removed the effect of environment on last-hatched chicks, such that all siblings in treated broods grew at a similar rate across environmental conditions. There were no differences in nematode burden between years or siblings, suggesting that variation in responses arose from intrinsic differences between chicks. Whole-brood growth rate was not affected by treatment, indicating that within-brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning. We show that gastrointestinal parasites can be a key component of offspring's developmental environment. Our results also demonstrate the value of considering prevailing conditions for our understanding of parasite effects on host life-history traits. Establishing how environmental conditions shape responses to parasitism is important as environmental variability is predicted to increase.

No MeSH data available.


Related in: MedlinePlus