Seasonality of host immunity in a tropical disease system

Abstract

Infectious disease systems frequently exhibit strong seasonal patterns, yet the mechanisms that underpin intra‐annual cycles are unclear, particularly in tropical regions. We hypothesized that host immune function fluctuates seasonally, contributing to oscillations in infection patterns in a tropical disease system. To test this hypothesis, we investigated a key host defense of amphibians against a lethal fungal pathogen, Batrachochytrium dendrobatidis (Bd). We integrated two field experiments in which we perturbed amphibian skin secretions, a critical host immune mechanism, in Panamanian rocket frogs (Colostethus panamansis). We found that this immunosuppressive technique of reducing skin secretions in wild frog populations increased Bd prevalence and infection intensity, indicating that this immune defense contributes to resistance to Bd in wild frog populations. We also found that the chemical composition and anti‐Bd effectiveness of frog skin secretions varied across seasons, with greater pathogen inhibition during the dry season relative to the wet season. These results suggest that the effectiveness of this host defense mechanism shifts across seasons, likely contributing to seasonal infection patterns in a lethal disease system. More broadly, our findings indicate that host immune defenses can fluctuate across seasons, even in tropical regions where temperatures are relatively stable, which advances our understanding of intra‐annual cycles of infectious disease dynamics.

The complement system and its involvement in inhibition of Batrachochytriym dendrobatidis, a lethal fungal pathogen of amphibians

“…help determine how, and to what extent, temperature could be involved in complement system functioning, which may help resolve seasonal immune fluctuations that have been observed for chytridiomycosis (Le Sage et al, 2021;Rosa et al, 2022). Third, we can build on this preliminary work to understand if complement system activation underpins interspecific differences in susceptibility to chytridiomycosis (Grogan et al, 2018b) and if so, we can further refine the mechanisms of complement protein effectiveness within the epidermis.…”

“…Investigators have made considerable advances in the pursuit of understanding amphibian immune responses in recent decades (Raffel et al, 2006;Rollins-Smith et al, 2011;Le Sage et al, 2021;Assis et al, 2022;2017;Rosa et al, 2022;Ruiz and Robert, 2023). However, there is still much to learn about how amphibian defenses operate in response to infection with Batrachochytrium dendrobatidis and the development of chytridiomycosis (reviewed in Grogan et al, 2018b;Rodriguez & Voyles, 2020).…”

“…First, although many components of the amphibian immune system are highly conserved among vertebrates, the diversity of immunological responses among amphibian host species provides insights into susceptibility to disease and the generation of resistance mechanisms (Assis et al, 2022;Ruiz & Robert, 2023). Second, as ectotherms, environmental conditions (e.g., temperature, relative humidity, and rainfall) that affect amphibian physiology also mediate immunity and the manifestation of disease (Raffel et al, 2006;Rollins-Smith et al, 2011;Rollins-Smith, 2017;Le Sage et al, 2021;Rosa et al, 2022). Third, infectious diseases have been implicated in severe global declines in amphibian populations and species in recent decades (Wake and Vredenburg, 2008;Scheele et al, 2019), making the study of amphibian immunity an important focus of recent research.…”

Drivers of Batrachochytrium dendrobatidis infection load, with evidence of infection tolerance in adult male toads (Bufo spinosus)

“…Many factors related to the host (Fernández-Beaskoetxea et al 2016 ), the pathogen (Farrer et al 2011 ; Rothstein et al 2021 ), and the environment (Rosa et al 2022 ) may interact to affect the intensity of infection and therefore the outcome of infection and disease. However, the importance of these is likely to vary both between and within species, and in particular between temperate and tropical communities.…”