Costs of immune defense: an enigma wrapped in an environmental cloak?

Sandland, Gregory J.; Minchella, Dennis J.

doi:10.1016/j.pt.2003.10.006

Cited by 125 publications

(127 citation statements)

References 33 publications

Supporting

Mentioning

116

Contrasting

Order By: Relevance

“…We attempted to reduce the environmental variation by maintaining the hosts in controlled conditions in the laboratory. However, we cannot exclude a seasonality effect in the physiology of hosts and the level of immune defence of hosts (Sandland & Minchella 2003) nor parasite 'qualities' that could explain the higher infectivity and faster development found in winter. Nevertheless, higher prevalence in autumn and winter has been reported in the field for P. laevis infection in Gammarus balcanicus (Dudinak & Spakulova 2003).…”

Section: Discussionmentioning

confidence: 93%

Variation and covariation in infectivity, virulence and immunodepression in the host–parasite associationGammarus pulex–Pomphorhynchus laevis

et al. 2009

View full text Add to dashboard Cite

Parasites often manipulate host immunity for their own benefit, either by exacerbating or suppressing the immune response and this may directly affect the expression of parasite virulence. However, genetic variation in immunodepression, which is a prerequisite to its evolution, and the relationship between immunodepression and virulence, have rarely been studied. Here, we investigated the variation among sibships of the acanthocephalan parasite, Pomphorhynchus laevis, in infecting and in immunodepressing its amphipod host, Gammarus pulex. We also assessed the covariation between infectivity, parasite-induced immune depression and host mortality (parasite virulence). We found that infectivity, the intensity of immunodepression and virulence were variable among parasite sibships. Infectivity and the level of immunodepression were not correlated across parasite sibships. Whereas infectivity was unrelated to host mortality, we found that gammarids that were exposed to the parasite sibships that immunodepressed their hosts the most survived better. This positive covariation between host survival and immunodepression suggests that gammarids exposed to the less immunodepressive parasites could suffer from damage imposed by a higher activity of the phenoloxidase.

show abstract

Section: Discussionmentioning

confidence: 93%

Variation and covariation in infectivity, virulence and immunodepression in the host–parasite associationGammarus pulex–Pomphorhynchus laevis

et al. 2009

View full text Add to dashboard Cite

show abstract

“…Varying environmental conditions, such as temperature and resource availability, have been shown to generate a change in the direction and/or magnitude of correlations between life-history traits not involving resistance (Service and Rose, 1985;Gebhardt and Stearns, 1988;Reznick et al, 2000;Rigby et al, 2002;Messina and Fry, 2003;Sgrò and Hoffmann, 2004). Environmental stressors in also modify the expression and magnitude of costs of resistance among plantpathogen associations (see Bazzaz et al, 1987;Bergelson and Purrington, 1996;Sandland and Minchella, 2003). Similar environment-dependent expression of costs have been detected in animal-parasite systems as well (Kraaijeveld and Godfray, 1997;Fellowes et al, 1998;Lochmiller and Deerenberg, 2000;Moret and Schmid-Hempel, 2000;Hoang, 2001).…”

Section: Introductionmentioning

confidence: 87%

“…In addition to environmental variation, different stages of host ontogeny can influence the expression of costs (Kraaijeveld et al, 2002;Sandland and Minchella, 2003). Previously, we demonstrated that resistance-selected lines experience a significant reduction in female fecundity, and that this effect is temperature-dependent (Luong and Polak, 2007).…”

Section: Introductionmentioning

confidence: 90%

“…Yet, genetic polymorphisms for resistance exist in most natural host populations (Parker, 1991;Henter and Via, 1995;Kraaijeveld et al, 1998). The cost of resistance hypothesis provides a potential mechanism for the maintenance of this variation (Sheldon and Verhulst, 1996;Gemmill and Read, 1998;Rigby et al, 2002;Brown, 2003;Sandland and Minchella, 2003). This hypothesis is based on a fundamental assumption underlying life-history theory, that the evolution of fitness traits is constrained by universal trade-offs among them (Reznick et al, 2000;Roff, 2002;Sgrò and Hoffmann, 2004).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila–Macrocheles system

Luong

Polák

2007

Heredity

View full text Add to dashboard Cite

Costs of resistance are expected to contribute to the maintenance of genetic variation for resistance in natural host populations. In the present study, we experimentally test for genetic trade-offs between parasite resistance and larval competitive ability expressed under varying levels of crowding and temperature. Artificial selection for increased behavioral resistance was applied against an ectoparasitic mite (Macrocheles subbadius) in replicate lines of the fruit fly Drosophila nigrospiracula. We then measured correlated responses to selection in larval competitive ability by contrasting replicate selected and control (unselected) lines in the absence of parasitism. Experiments were conducted under variable environmental conditions: two temperatures and three levels of larval density. Our results reveal a negative genetic correlation between resistance and larval-adult survival under conditions of moderate and severe intra-specific competition. At both low and high temperature, percent emergence was significantly higher among control lines than selected lines. This divergence in larval competitive ability was magnified under high levels of competition, but only at low temperature. Hence, the interaction between selection treatment and larval density was modified by temperature. As predicted, larvae experiencing medium and high levels of competition exhibited an overall reduction in female body size compared to larvae at low levels of competition. Female flies emerging from selected lines were significantly smaller than those females from control lines, but this effect was only significant under conditions of moderate to severe competition. These results provide evidence of environment-dependent trade-offs between ectoparasite resistance and larval competitive ability, a potential mechanism maintaining genetic polymorphism for resistance.

show abstract

“…It is well known that resistance against parasites is often energetically expensive and a number of studies have investigated the potential trade-offs between resistance and other energetically demanding processes (Sheldon and Verhulst, 1996;Lochmiller and Deerenberg, 2000;Rigby et al, 2002;Sandland and Minchella, 2003; but see Klasing, 1998;Hasselquist and Nilsson, 2012 trade-off may be particularly noticeable in energy-limited organisms, or young animals facing elevated energetic demands associated with growth (Ricklefs and Wikelski, 2002;. While the exact cost of resistance remains difficult to quantify, it is increasingly clear that from a life-history perspective, maintenance and upregulation of immune function may suffer in the face of a limited energy supply (Lochmiller and Deerenberg, 2000;Pilorz et al, 2005;French et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Age at weaning, immunocompetence and ectoparasite performance in a precocial desert rodent

Dlugosz

Bellocq

Khokhlova

et al. 2014

Journal of Experimental Biology

View full text Add to dashboard Cite

We studied the effects of early weaning on immunocompetence and parasite resistance in a precocial rodent Acomys cahirinus. We hypothesized that if parasite resistance is energetically expensive and nutritional and immunological support from mothers are necessary for the long-term health of offspring, then early weaned animals would be immunologically weaker and less able to defend themselves against parasites than later weaned animals. We weaned pups at 14, 21 or 28 days after birth and assessed their immunocompetence and resistance against fleas Parapulex chephrenis when they attained adulthood. Immunocompetence was assessed using leukocyte concentration (LC) and a phytohaemagglutinin injection assay (PHA test). To estimate resistance against fleas, we measured performance of fleas via the number of produced eggs and duration of development and resistance to starvation of the flea offspring. We found a significant positive effect of weaning age on the PHA response but not on LC. The effect of age at weaning on flea egg production was manifested in male but not female hosts, with egg production being higher if a host was weaned at 14 than at 28 days. Weaning age of the host did not affect either duration of development or resistance to starvation of fleas produced by mothers fed on these hosts. We conclude that even in relatively precocial mammals, weaning age is an important indicator of future immunological responses and the ability of an animal to resist parasite infestations. Hosts weaned at an earlier age make easier, less-resistant targets for parasite infestations than hosts weaned later in life. KEY WORDS: Fleas, PHA response, Weaning, Spiny mouse INTRODUCTIONIt is well known that resistance against parasites is often energetically expensive and a number of studies have investigated the potential trade-offs between resistance and other energetically demanding processes (Sheldon and Verhulst, 1996;Lochmiller and Deerenberg, 2000;Rigby et al., 2002;Sandland and Minchella, 2003; but see Klasing, 1998;Hasselquist and Nilsson, 2012 trade-off may be particularly noticeable in energy-limited organisms, or young animals facing elevated energetic demands associated with growth (Ricklefs and Wikelski, 2002;. While the exact cost of resistance remains difficult to quantify, it is increasingly clear that from a life-history perspective, maintenance and upregulation of immune function may suffer in the face of a limited energy supply (Lochmiller and Deerenberg, 2000;Pilorz et al., 2005;French et al., 2009).Reproductive choices concerning weaning time in mammals are likely to have a great effect on a number of life-history parameters. Evolutionarily, mammalian mothers face a conflict: lactation is wellknown to be energetically demanding and it delays future reproductive events; however, early weaning may place nursing offspring at greater risk for restricted growth or increased susceptibility to pathogens or parasites (Grindstaff et al., 2003;Grindstaff, 2008). Mothers absorb some of the energetic costs plac...

show abstract

Costs of immune defense: an enigma wrapped in an environmental cloak?

Cited by 125 publications

References 33 publications

Variation and covariation in infectivity, virulence and immunodepression in the host–parasite associationGammarus pulex–Pomphorhynchus laevis

Variation and covariation in infectivity, virulence and immunodepression in the host–parasite associationGammarus pulex–Pomphorhynchus laevis

Environment-dependent trade-offs between ectoparasite resistance and larval competitive ability in the Drosophila–Macrocheles system

Age at weaning, immunocompetence and ectoparasite performance in a precocial desert rodent

Contact Info

Product

Resources

About