Dose‐ and time‐dependent effects of an immune challenge on fish across biological levels

Abstract

Due to global changes, fish are increasingly exposed to immune challenges associated with disease outbreaks in aquatic ecosystems. Adjustments in physiology and behavior are generally critical to maintaining homeostasis after an immune challenge, but there is limited knowledge on the specific thresholds and dynamics of responses across levels of biological organization in fish. In this study, we tested how different concentrations of an antigens mixture (phytohemagglutinin and lipopolysaccharide) affected innate immunity with potential consequences on oxidative stress, energy reserves, body condition, and behavior across time, using the common gudgeon (Gobio sp.) as model species. The immune challenge induced a transitory increase in lytic enzyme activity (i.e., lysozyme) and local immune response (i.e., skin swelling) 2 days after the antigen injection. The available energy stored in muscle was also reduced 4 days after injection, without inducing oxidative stress at the cellular level. Overall, the immune challenge induced limited costs at the molecular and cellular levels but had strong effects at the whole organism level, especially on behavior. Indeed, fish swimming activity and sociability were affected in a dose‐ and time‐dependent manner. These results suggest that immune challenges have dose‐dependent effects across levels of biological organization and that behavior is a key response trait to cope with pathogen‐induced immune costs in the wild, although fitness consequences remain to be tested.

Sickness and the Social Brain: How the Immune System Regulates Behavior across Species

“…For example, researchers have shown that red colobus monkeys infected with ringworm are lethargic, groom less, and copulate less [Ghai et al, 2015], and that deworming vervet monkeys of gastrointestinal parasites significantly increases their propensity for social interaction [Chapman et al, 2016]. In zebrafish, infection with LPS decreases swimming and drastically reduces social preference [Kirsten et al, 2018;Petitjean et al, 2021]. Finally, in a series of studies by Schall and colleagues, it was demonstrated that malaria infection in western fence lizards decreases aggression, social displays, and social dominance [Schall and Dearing, 1987;Schall and Houle, 1992;Dunlap and Schall, 1995].…”

Energetic costs of mounting an immune response in a coral reef damselfish (Pomacentrus amboinensis)

“…These factors may explain the lack of clear differences observed in SSI between our groups vs. those found in Binning et al (2018). Spleen enlargement alone may not be an accurate measure to characterize the occurrence of an immune response given the large amongindividual variation that exists among treatments (Petitjean et al 2021) We found altered immune gene expression in fish injected with the two highest doses of LPS (50mg kg -1 and 100mg kg -1 ) and with the lowest one (3mg kg -1 ). Responses to immune stimulants are dose and time dependent.…”

Carotenoids modulate stress tolerance and immune responses in aquatic animals

“…23,24 The overproduction of ROS could conceivably entail host immunosuppression and severe oxidative damages since the immune response is a costly physiological activity when initiated against foreign microorganisms (non-self entities) or pathogenic processes. 25,26 From this perspective, supplementation of carotenoids for a well-integrated antioxidant system is imperative for enhanced stress tolerance and immunity in cultured animals.…”

“…Furthermore, as potent singlet oxygen quenchers, carotenoids can potentially halt the toxic effects of reactive oxygen species (ROS) generated during mounting host defence activities without raising the associated costs of immunity 23,24 . The overproduction of ROS could conceivably entail host immunosuppression and severe oxidative damages since the immune response is a costly physiological activity when initiated against foreign microorganisms (non‐self entities) or pathogenic processes 25,26 . From this perspective, supplementation of carotenoids for a well‐integrated antioxidant system is imperative for enhanced stress tolerance and immunity in cultured animals.…”