A comparative study of an innate immune response in Lamprologine cichlid fishes

Abstract

Social interactions facilitate pathogen transmission and increase virulence. Therefore, species that live in social groups are predicted to suffer a higher pathogen burden, to invest more heavily in immune defence against pathogens, or both. However, there are few empirical tests of whether social species indeed invest more heavily in immune defence than non-social species. In the current study, we conducted a phylogenetically controlled comparison of innate immune response in Lamprologine cichlid fishes. We focused on three species of highly social cichlids that live in permanent groups and exhibit cooperative breeding (Julidochromis ornatus, Neolamprologus pulcher and Neolamprologus savoryi) and three species of non-social cichlids that exhibit neither grouping nor cooperative behaviour (Telmatochromis temporalis, Neolamprologus tetracanthus and Neolamprologus modestus). We quantified the innate immune response by injecting wild fishes with phytohaemagglutinin (PHA), a lectin that causes a cell-mediated immune response. We predicted that the three highly social species would show a greater immune reaction to the PHA treatment, indicating higher investment in immune defence against parasites relative to the three non-social species. We found significant species-level variation in immune response, but contrary to our prediction, this variation did not correspond to social system. However, we found that immune response was correlated with territory size across the six species. Our results indicate that the common assumption of a positive relationship between social system and investment in immune function may be overly simplistic. We suggest that factors such as rates of both in-group and out-group social interactions are likely to be important mediators of the relationship between sociality and immune function.

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

“…On the contrary, at the cellular level, the local immune response (i.e., skin swelling) increased significantly in all injected fish, whatever the antigen concentration. This result is consistent with the effects of both LPS and PHA on local immune response (Ardia & Clotfelter, 2006; O'Connor et al, 2014; Otálora‐Ardila et al, 2016; Tella et al, 2008), which is due to the local infiltration of neutrophils, macrophages, and lymphocytes and more broadly local inflammation (Ardia & Clotfelter, 2006). The type of PHA used in our study may explain the long‐lasting effect (i.e., until 16 days) of the antigens mixture on swelling measurement because PHA‐P may elicit higher cells agglutination and tissue damage at the injection point than other types of PHA (Tylan & Langkilde, 2017).…”

“…We assessed the local immune response by measuring the local skin swelling (i.e., thickness measurement) of the caudal peduncle after immune challenge or control injection following previous studies in fish (Ardia & Clotfelter, 2006; O'Connor et al, 2014). The local immune response reflects the intensity of the local inflammation and the proliferation of T cells (Ardia & Clotfelter, 2006; O'Connor et al, 2014; Tella et al, 2008).…”

“…We assessed the local immune response by measuring the local skin swelling (i.e., thickness measurement) of the caudal peduncle after immune challenge or control injection following previous studies in fish (Ardia & Clotfelter, 2006; O'Connor et al, 2014). The local immune response reflects the intensity of the local inflammation and the proliferation of T cells (Ardia & Clotfelter, 2006; O'Connor et al, 2014; Tella et al, 2008). The thickness of the caudal peduncle was measured three times by the same operator and averaged before and after the injection of the antigen mixture or PBS using a thickness gauge (Elcometer ® 124) to calculate the intensity of the local immune response as the difference of peduncle thickness before and after injection divided by the thickness before injection × 100.…”

Thermal sensitivity of juvenile rabbitfishes Siganus doliatus and S. lineatus (Siganidae): a key role for habitat?

“…In order to examine the sensitivity of the immune system of S. doliatus and S. lineatus to thermal stress, we carried out an immune challenge on all individuals. After 11 weeks of exposure to their respective treatments, we measured the immune response of each individual (S. doliatus n = 36; S. lineatus n = 45) using a phytohaemagglutinin (PHA) injection assay to elicit body inflammation as a proxy for a cell-mediated immune response (O'Connor et al 2014). Since this was the first time that this method has been used to quantify immunity in the two study species, we also conducted separate control injections of phosphate buffer saline solution (PBS) in order to validate the PHA assay methodology for S. doliatus and S. lineatus.…”

Critical review of the phytohemagglutinin assay for assessing amphibian immunity

“…Studies in birds have associated PHA responses with a range of other measures, including contaminant levels, noise pollution and coloration ( Grasman et al , 1996 ; Smits and Williams, 1999 ; Møller and Cassey, 2004 ; Møller and Saino, 2004 ; Moreno et al , 2005 ; Grasman, 2010 ; Sivaraman and Kumar, 2013 ; Lopez-Antia et al , 2015 ; Kerimov et al , 2018 ; Pusch and Navara, 2018 ; Arct et al , 2019 ; Minias et al , 2019 ; Obomsawin et al , 2021 ), and have assessed the impact of immunocompetence on health outcomes ( Mougeot et al , 2004 ; Moreno et al , 2005 ; Sivaraman and Kumar, 2013 ; Martínez et al , 2018 ). While the PHA assay is still often used for avian studies ( O’Connor et al , 2014 ; LaMonica et al , 2021 ), it has also grown increasingly popular among other taxa, including mammals, reptiles and fish ( Finger et al , 2015 ; Hernández-Arciga et al , 2018 ; Merlo et al , 2018 ; Plasman et al , 2019 ; Nasri et al , 2020 ; LaMonica et al , 2021 ; Stienbarger et al , 2021 ; Miyazawa et al , 2022 ).…”