Photoperiodic regulation of behavior: Peromyscus as a model system

Abstract

Winter and summer present vastly different challenges to animals living outside of the tropics. To survive and reproduce, individuals must anticipate seasonal environmental changes and adjust physiology and behavior accordingly. Photoperiod (day length) offers a relatively ‘noise free’ environmental signal that non-tropical animals use to tell the time of year, and whether winter is approaching or receding. In some cases, photoperiodic signals may be fine-tuned by other proximate cues such as food availability or temperature. The pineal hormone, melatonin, is a primary physiological transducer of the photoperiodic signal. It tracks night length and provokes changes in physiology and behavior at appropriate times of the year. Because of their wide latitudinal distribution, Peromyscus has been well studied in the context of photoperiodic regulation of physiology and behavior. Here, we discuss how photoperiodic signals are transduced by pineal melatonin, how melatonin acts on target tissues, and subsequent consequences for behavior. Using a life-history paradigm involving trade-offs between the immune and reproductive systems, specific emphasis is placed on aggression, metabolism, and cognition. We discuss future directions including examining the effects of light pollution on photoperiodism, genetic manipulations to test the role of specific genes in the photoperiodic response, and using Peromyscus to test evolutionary theories of aging.

Introduction

Deer mice (genus Peromyscus) comprise 56 distinct species and are the most widespread and abundant mammals in North America [1]. They inhabit a wide array of climes, including urban environments, and develop specific physiological and behavioral adaptations relevant to survival and reproductive success such as coat color variation, metabolic and immune specializations, and burrowing behavior (reviewed in [2]). Several species of Peromyscus inhabit areas that undergo substantial seasonal changes in temperature, snow cover, and population density, as well as food and mate availability. These fluctuations in ecologically salient variables provide selective pressures for mice to predict seasonal changes in order to develop season-specific adaptations and improve the odds of survival and reproduction. Environmental conditions themselves (e.g., temperature, barometric pressure, and rainfall) have little predictive value as they can vary widely over short time spans. Peromyscus and other non-tropical small rodents use a relatively neutral geophysical cue, day length (i.e., photoperiod), to organize seasonal physiology and behavior (see [3]). By using two bits of photoperiodic information, viz., the absolute day length and whether day lengths are increasing or decreasing, mice can ascertain the time of year and whether winter or summer is approaching.

In response to short photoperiods, Peromyscus mice reorganize key components of their immune and reproductive systems, as well as behavior, to increase survival and reproductive success. Sustainable energy utilization requires seasonal adjustments of physiological priorities (Fig. 1). Reproductive function and behavior are restricted to long days in most non-tropical small rodents, as they signal a time when resources are abundant and conditions are optimal for offspring success [4]. However, in response to the onset of short days prior to winter, when the odds of offspring survival are low, individuals of many species invest heavily in immune function putatively to increase the odds of survival until the next breeding season [5]. Winter investment into immune function may buffer individuals from immunosuppression induced by an energetic bottleneck formed when demands for increased thermoregulation and reduced food availability coincide [6]. This reallocation of energy is accompanied by changes in behavior, including breeding, aggression, and learning and memory. Because day length is an environmentally discrete signal (i.e., it is relatively ‘noise free’), studies that experimentally manipulate photoperiod are ideal for investigations into the mechanisms behind ‘gene by environment’ interactions. Indeed, day length can alter the behavioral effect of estradiol administration by influencing which estradiol receptor is expressed and subsequently activated [7]. Additionally, day length can affect the proliferation and integration of newly formed neurons migrating to the olfactory bulb and influence olfactory behavior [8]. Most research on photoperiod-dependent changes in physiology and behavior within Peromyscus has been conducted on white-footed mice (P. leucopus) and the closely related species of North American deer mice Peromyscus maniculatus. In this review, we discuss how day length is transduced into biochemical signals via the neuroendocrine system and how these signals alter physiology and behaviors important for biological fitness. In contrast to Peromyscus, common laboratory house mice (Mus musculus) no longer display photoperiodic responses. Mus are, however, able to process the photoperiodic signal, although it remains uncoupled from reproduction [9]. Many of the studies discussed below could not be conducted with house mice as they do not show standard responses to photoperiod. Therefore, the use of Peromyscus offers a unique opportunity to investigate how an easily tunable environmental variable (photoperiod) can influence a wide array of functions.