Seasonal Changes in Immune Function

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Abstract

Winter is energetically demanding. Physiological and behavioral adaptations have evolved among nontropical animals to cope with winter because thermoregulatory demands increase when food availability decreases. Seasonal breeding is central within the suite of winter adaptations among small animals. Presumably, reproductive inhibition during winter conserves energy at a time when the adds of producing viable young are low. In addition to the well-studied seasonal cycles of mating and birth, there are also significant seasonal cycles of illness and death among many populations of mammals and birds in the field. Challenging winter conditions, such as low ambient temperatures and decreased food availability, can directly induce death via hypothermia, starvation or shock. In some cases, survival in demanding winter conditions puts individuals under great physiological stress, defined here as an adaptive process that results in elevated blood levels of glucocorticoids. The stress of coping with energetically demanding conditions can also indirectly cause illness and death by compromising immune function. Presumably, the increased blood concentrations of adrenocortical steroids in response to winter stressors compromise immune function and accelerate catabolic mechanisms in the field, although the physiological effects of elevated glucocorticoids induced by artificial stressors have been investigated primarily in the laboratory. However, recurrent environmental stressors could reduce survival if they evoke persistent glucocorticoid secretion. The working hypothesis of this article is that mechanisms have evolved in some animals to combat seasonal stress-induced immunocompromise as a temporal adaptation to promote survival. Furthermore, we hypothesize that mechanisms have evolved that allow individuals to anticipate periods of immunologically challenging conditions, and to cope with these seasonal health-threatening conditions. The primary environmental cue that permits physiological anticipation of season is the daily photoperiod; however, other environmental factors may interact with photoperiod to affect immune function and disease processes. The evidence for seasonal fluctuations in lymphatic organ size, structure, immune function, and disease processes, and their possible interactions with recurrent environmental stressors, is reviewed. Seasonal peaks of lymphatic organ size and structure generally occur in late autumn or early winter and seasonal minima are observed prior to the onset of breeding. Although many of the field data suggest that immune function and disease processes are also enhanced during the winter, the opposite seasonal pattern is also observed in some studies. We propose that compromised immune function may be observed in some populations during particularly harsh winters when stressors override the enhancement of immune function evoked by short day lengths. Because so many factors covary in field studies, assessment of our proposal that photoperiod mediates seasonal changes in immune function requires laboratory studies in which only photoperiod is varied. A review of the effects of photoperiod on immune function in laboratory studies reveals that exposure to short day lengths enhances immune function in every species examined. Short day exposure in small mammals causes reproductive inhibition and concomitant reduction in plasma levels of prolactin and steroid hormones, as well as alterations in the temporal pattern of pineal melatonin secretion. These hormones affect immune function, and influence the development of opportunistic diseases, including cancer: however, it appears that either prolactin or melatonin secretion is responsible for mediating the effects of photoperiod on immune function. Taken together, day length appears to affect immune function in many species, including animals that typically do not exhibit reproductive responsiveness to day length.

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