Abstract
Identifying how developmental temperature affects the immune system is critical for understanding how ectothermic animals defend against pathogens and their fitness in the changing world. However, reptiles have received little attention regarding this issue. We incubated eggs at three ecologically relevant temperatures to determine how incubation temperature affects the immune function of hatchling soft-shelled turtles, Pelodiscus sinensis. When exposed to bacterial infections, hatchlings from 24 °C had lower cumulative mortalities (55%, therefore, higher immunocompetence) than those from 28 °C (85%) or 32 °C (100%). Consistent with higher immunocompetence, hatchlings from low incubation temperature had higher IgM, IgD, and CD3γ expressions than their counterparts from the other two higher incubation temperatures. Conversely, the activity of immunity-related enzymes did not match the among-temperature difference in immune function. Specifically, enzyme activity was higher at intermediate temperatures (alkaline phosphatase) or was not affected by incubation temperature (acid phosphatase, lysozyme). Our study is the first to provide unequivocal evidence (at the molecular and organismal level) about the significant effect of incubation temperature on offspring immunity in reptiles. Our results also indicate that the reduced immunity induced by high developmental temperatures might increase the vulnerability of reptiles to the outbreak of diseases under global warming scenarios.
Highlights
After being challenged with a concentration gradient of the pathogen Aeromonas hydrophilia TL1 from 5 × 103 to 5 × 107 Colony-Forming Units (CFU), all hatchlings from all three incubation temperatures died at the concentration of 5 × 107 CFU, and had similar cumulative mortalities at the concentration of 5 × 104 CFU (G = 3.68, df = 2, P > 0 .05)
Our results indicate that incubation temperature significantly affects immune function, in addition to associated biochemical and molecular processes, including the activity of immunity-related enzymes and the expression of immune genes
While several studies have found that incubation temperature may affect immune function of avian offspring[5,6], similar studies are rare in reptiles
Summary
37 °C)[5,6]. just one study has investigated how temperature affects offspring immunity in reptiles; namely, the map turtles (Graptemys ouachitensis and Graptemys pseudogeographica)[9]. Exploring the effect of temperature on the expression of these immunity-related enzymes and genes would enhance our understanding about the proximate mechanisms by which developmental temperature affects offspring immunity in animals. We aim to determine the effect of incubation temperature on the immune function of hatchling soft-shelled turtles, Pelodiscus sinensis. We incubated P. sinensis eggs at three temperatures that span the range of temperatures experienced by the eggs in natural nests The hatchlings from these thermal treatments were exposed to bacterial infections and mortality was determined over a 1-week period. To identify the underlying mechanism of temperature effects on offspring immunity, we determined the activity of specific immunity-related enzymes (such as lysozyme, acid phosphatase, and alkaline phosphatase) and the regulation of specific immune genes (including IgM, IgD, CD3γ , and CD9). We tested the hypothesis that the activity of these enzymes would increase and that the expression of these immune genes would become upregulated in hatchlings that had high immune function
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