Anticipatory plastic response of the cellular immune system in the face of future injury: chronic high perceived predati

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PHYSIOLOGICAL ECOLOGY – ORIGINAL RESEARCH

Anticipatory plastic response of the cellular immune system in the face of future injury: chronic high perceived predation risk induces lymphocytosis in a cichlid fish Denis Meuthen1,2   · Ingo Meuthen3 · Theo C. M. Bakker2   · Timo Thünken2  Received: 24 April 2020 / Accepted: 8 October 2020 © The Author(s) 2020

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. Keywords  Pelvicachromis taeniatus · Hematology · Lymphocytes · Phenotypic plasticity · Alarm cues

Introduction To protect themselves against pathogens, the vertebrate immune system has evolved highly effective cellular immunity, of which white blood cells, also called leukocytes, are Communicated by Donovan P German. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0044​2-020-04781​-y) contains supplementary material, which is available to authorized users. * Denis Meuthen denis.meuthen@uni‑bielefeld.de 1



Evolutionary Biology, Bielefeld University, Konsequenz 45, 33615 Bielefeld, Germany

2



Institute for Evolutionary Biology and Ecology, University of Bonn, An der Immenburg 1, 53121 Bonn, Germany

3

Practice of Internal Medicine, Hematology and Oncology, Hauptstraße 39‑41, 50996 Cologne, Germany



an important component. There are different types of leukocytes, ranging from cells with phagocytotic activity (neutrophils) to those that produce proteins such as antibodies (specialized lymphocytes called B cells). Hence, both the absolute amount and the relat