Developmental plasticity of immune defence in two life-history ecotypes of the garter snake, Thamnophis elegans - a common-environment experiment

Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA 50010, USA.
Journal of Animal Ecology (Impact Factor: 4.5). 03/2011; 80(2):431-7. DOI: 10.1111/j.1365-2656.2010.01785.x
Source: PubMed


1. Ecoimmunological theory predicts a link between life-history and immune-defence strategies such that fast-living organisms should rely more on constitutive innate defences compared to slow-living organisms. An untested assumption of this hypothesis is that the variation in immune defence associated with variation in life history has a genetic basis.
2. Replicate populations of two life-history ecotypes of the garter snake Thamnophis elegans provide an ideal system in which to test this assumption. Free-ranging snakes of the fast-living ecotype, which reside in lakeshore habitats, show higher levels of three measures of constitutive innate immunity than those of the slow-living ecotype, which inhabit meadows around the lake. Although this pattern is consistent with the ecoimmunological pace-of-life hypothesis, environmental differences between the lakeshore and meadow habitats could also explain the observed differences in immune defence.
3. We performed a common-environment experiment to distinguish between these alternatives. Snakes born and raised in common-environment conditions reflected the immune phenotype of their native habitats when sampled at 4 months of age (i.e. fast-living lakeshore snakes showed higher levels of natural antibodies, complement activity and bactericidal competence than slow-living meadow snakes), but no longer showed differences when 19 months old.
4. This suggests that the differences in innate immunity observed between the two ecotypes have an important – and likely age-specific – environmental influence, with these immune components showing developmental plasticity. A genetic effect in early life may also be present, but further research is needed to confirm this possibility and therefore provide a more definitive test of the ecoimmunological pace-of-life hypothesis in this system.

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Available from: Maria G. Palacios, Oct 05, 2015
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    • "This divergence in life-history strategies, despite significant gene flow between populations (Manier and Arnold 2005, 2006), is putatively driven by differing thermal regimes (Bronikowski 2000), resource availability (Bronikowski and Arnold 1999; Miller et al. 2011), and predation rates (Sparkman et al. 2013). Studies in this system have demonstrated ecotypic differences in immune investment (Sparkman and Palacios 2009; Palacios et al. 2011), endocrine function (Sparkman et al. 2009; Palacios et al. 2012), cellular repair efficiency (Robert and Bronikowski 2010), and stress response pathways (Schwartz and Bronikowski 2012). Adult L-fast snakes have higher resting metabolic rates than M-slow snakes across 157–327C (Bronikowski and Vleck 2010), but this ecotypic difference was not present in month-old snakes reared under common laboratory conditions (Robert and Bronikowski 2010), *Corresponding author; e-mail: "
    Physiological and Biochemical Zoology 06/2015; DOI:10.1086/682239 · 2.40 Impact Factor
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    • "Conversely, short-lived vertebrates (fast pace of life) should invest more in innate immune mechanisms in contrast to investing in adaptive immune functions (Lee 2006). This hypothesis has led to a number of studies, testing this hypothesis both at the level of species and individuals in birds and mammals—with variable amounts of support (e.g., Martin et al. 2006, 2007; Cutrera et al. 2010; Buehler et al. 2012; Horrocks et al. 2012; Previtali et al. 2012, but see Palacios et al. 2011; Lucas and French 2012). Here, we approach this topic from a herpetological perspective, and we argue that a strong adaptive immune response is not necessary for the survival of slow pace-of-life vertebrates. "
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    ABSTRACT: We propose a new heuristic model that incorporates metabolic rate and pace of life to predict a vertebrate species' investment in adaptive immune function. Using reptiles as an example, we hypothesize that animals with low metabolic rates will invest more in innate immunity compared with adaptive immunity. High metabolic rates and body temperatures should logically optimize the efficacy of the adaptive immune system-through rapid replication of T and B cells, prolific production of induced antibodies, and kinetics of antibody-antigen interactions. In current theory, the precise mechanisms of vertebrate immune function oft are inadequately considered as diverse selective pressures on the evolution of pathogens. We propose that the strength of adaptive immune function and pace of life together determine many of the important dynamics of host-pathogen evolution, namely, that hosts with a short lifespan and innate immunity or with a long lifespan and strong adaptive immunity are expected to drive the rapid evolution of their populations of pathogens. Long-lived hosts that rely primarily on innate immune functions are more likely to use defense mechanisms of tolerance (instead of resistance), which are not expected to act as a selection pressure for the rapid evolution of pathogens' virulence.
    Integrative and Comparative Biology 04/2014; 54(3). DOI:10.1093/icb/icu021 · 2.93 Impact Factor
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    • "The total leukocyte count was estimated by the indirect Phloxin B method (Campbell and Ellis 2007) using 0.1% phloxin stain (Vetlab Supply, Palmetto Bay, FL) and a hemocytometer, whereas the proportion of lymphocytes was derived from a differential leukocyte count on blood smears stained with Wright's stain and scanned under #1,000 oil immersion using a compound microscope as described in Palacios et al. (2009). Bactericidal Competence of Plasma We assessed bactericidal competence of plasma following the method of Matson et al. (2006), with a few modifications for use in garter snakes (Sparkman and Palacios 2009; Palacios et al. 2011). A pellet of lyophilized E. coli (ATCC8739; Microbiologics , St. Cloud, MN) was reconstituted using 40 mL #1 phosphate-buffered saline (PBS), and a fraction was further diluted 1 : 64 with PBS to produce a working solution containing approximately 150 colony-forming bacteria per 10 mL. "
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    ABSTRACT: Abstract The immunocompetence "pace-of-life" hypothesis proposes that fast-living organisms should invest more in innate immune defenses and less in adaptive defenses compared to slow-living ones. We found some support for this hypothesis in two life-history ecotypes of the snake Thamnophis elegans; fast-living individuals show higher levels of innate immunity compared to slow-living ones. Here, we optimized a lymphocyte proliferation assay to assess the complementary prediction that slow-living snakes should in turn show stronger adaptive defenses. We also assessed the "environmental" hypothesis that predicts that slow-living snakes should show lower levels of immune defenses (both innate and adaptive) given the harsher environment they live in. Proliferation of B- and T-lymphocytes of free-living individuals was on average higher in fast-living than slow-living snakes, opposing the pace-of-life hypothesis and supporting the environmental hypothesis. Bactericidal capacity of plasma, an index of innate immunity, did not differ between fast-living and slow-living snakes in this study, contrasting the previously documented pattern and highlighting the importance of annual environmental conditions as determinants of immune profiles of free-living animals. Our results do not negate a link between life history and immunity, as indicated by ecotype-specific relationships between lymphocyte proliferation and body condition, but suggest more subtle nuances than those currently proposed.
    Physiological and Biochemical Zoology 09/2013; 86(5):547-558. DOI:10.1086/672371 · 2.40 Impact Factor
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