Abstract
Vertebrate cellular immunity displays substantial variation among taxa and environments. Hematological parameters such as white blood-cell counts have emerged as a valuable tool to understand this variation by assessing the immunological status of individuals. These tools have long revealed that vertebrate cellular immune systems are highly plastic and respond to injury and infection. However, cellular immune systems may also be able to anticipate a high risk of injury from environmental cues (e.g., predation-related cues) and respond plastically ahead of time. We studied white blood-cell (leukocyte) profiles in African cichlids Pelvicachromis taeniatus that were raised for 4 years under different levels of perceived predation risk. In a split-clutch design, we raised fish from hatching onwards under chronic exposure to either conspecific alarm cues (communicating high predation risk) or a distilled water control treatment. Differential blood analysis revealed that alarm cue-exposed fish had twice as many lymphocytes in peripheral blood as did controls, a condition called lymphocytosis. The presence of a higher number of lymphocytes makes the cellular immune response more potent, which accelerates the removal of invading foreign antigens from the bloodstream, and, therefore, may be putatively beneficial in the face of injury. This observed lymphocytosis after long-term exposure to conspecific alarm cues constitutes first evidence for an anticipatory and adaptive plastic response of the cellular immune system to future immunological challenges.
Highlights
Male and female leukocyte profiles did not differ in their response to the treatment (“interaction sex × treatment”, likelihood ratio tests (LRT): leukocytes, χ2 = 0.117, p = 0.732; lymphocytes, χ2 = 0.321, p = 0.571; neutrophils, χ2 = 0.006, p = 0.939; monocytes, χ2 = 2.585, p = 0.108; proportion neutrophils:lymphocytes, χ2 = 0.152, p = 0.697)
Fish from the alarm cue exposure treatment had approximately 30% more leukocytes (LRT, χ2 = 5.693, p = 0.017), which was caused by a doubling of lymphocyte counts in alarm cue-exposed individuals (LRT, χ2 = 9.512, p = 0.002, Fig. 2)
Our results revealed that alarm cue-exposed fish had a significantly higher absolute number of leukocytes which was caused by a significantly greater number of lymphocytes in alarm cue-exposed P. taeniatus relative to the water control
Summary
In the face of possible future injury, a cue-induced proliferation of cellular immune system components has the potential to fight off pathogens early and thereby may vastly reduce disease-related fitness costs. This may constitute another case of how adaptive phenotypic plasticity allows individuals to adapt to changing environments (West-Eberhard 2003; Scheiner et al 2020), similar to how prey animals respond plastically to the key ecological factor predation (Lima and Dill 1990; Nosil and Crespi 2006). While there is a lot of evidence for behavioral (Ferrari et al 2015; Kim 2016; Meuthen et al 2019d, 2019c) and life-history antipredator phenotypic plasticity (Reznick and Endler 1982; Belk 1998; Johnson and Belk 2001; Dzikowski et al 2004) across fish taxa, no single study has considered that the fish cellular immune system may likewise respond with adaptive plasticity to perceived predation risk
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