Photoperiodic regulation of behavioral responses to bacterial and viral mimetics: a test of the winter immunoenhancement hypothesis

Abstract

Siberian hamsters (Phodopus sungorus) exhibit changes in immune function following adaptation to short photoperiods, including a marked attenuation of energetically expensive thermoregulatory and behavioral responses to gram-negative bacterial infections. Whether this seasonal attenuation of the immune response is idiosyncratic to gram-negative infections or is representative of innate immune responses in general is not known. If seasonal attenuation of responsiveness to infection is indeed driven primarily by anticipation of energetic constraints, then one would predict that responsiveness to all pathogens would be diminished during short days. If, on the other hand, seasonal changes in responsiveness to infection reflect anticipation of specific pathogens that are common at different phases of the annual cycle, then one would expect short photoperiods to attenuate responsiveness to some pathogens and long photoperiods to attenuate responsiveness to others. To resolve this issue, we exposed male Siberian hamsters to either long or short photoperiods for 11 weeks, then examined their behavioral sickness responses to compounds that represent the minimally immunogenic components of gram-negative bacterial (lipopolysaccharide), gram-positive bacterial (muramyl dipeptide), and viral (polyinosinepolycytidylic acid) organisms. Hamsters exhibited anorexic, anhedonic, ponderal, and/or thermoregulatory sickness behaviors to all 3 pathogen mimetics, but in all cases in which sickness responses were evident, they were attenuated in short days. Energetically costly behavioral responses to several distinct classes of infectious organisms are attenuated in anticipation of winter. The data are not consistent with a pathogen-specific seasonal modulation of innate immune responses.