Significance This work examined whether epigenetic mechanisms participate in the regulation of seasonal reproduction. In long-day (summer) breeding hamsters, exposure to inhibitory winter photoperiods, or winter-like patterns of melatonin, altered DNA methyltransferase expression; decreased DNA methylation in the proximal promoter region of deiodinase type III ( dio3 ) in the hypothalamus; and, in turn, increased hypothalamic dio3 expression. Pharmacological blockade of photoperiod-driven demethylation attenuated reproductive responses to winter photoperiods. Winter demethylation was reversed in anticipation of spring: spontaneous reproductive development was accompanied by remethylation of the dio3 promoter and decreases in dio3 mRNA. Methylation dynamics in the adult brain are reversible and may constitute an important component of the mechanism by which seasonal time is represented in the nervous system.

The rhythm of life on earth is shaped by seasonal changes in the environment. Plants and animals show profound annual cycles in physiology, health, morphology, behaviour and demography in response to environmental cues. Seasonal biology impacts ecosystems and agriculture, with consequences for humans and biodiversity. Human populations show robust annual rhythms in health and well-being, and the birth month can have lasting effects that persist throughout life. This review emphasizes the need for a better understanding of seasonal biology against the backdrop of its rapidly progressing disruption through climate change, human lifestyles and other anthropogenic impact. Climate change is modifying annual rhythms to which numerous organisms have adapted, with potential consequences for industries relating to health, ecosystems and food security. Disconcertingly, human lifestyles under artificial conditions of eternal summer provide the most extreme example for disconnect from natural seasons, making humans vulnerable to increased morbidity and mortality. In this review, we introduce scenarios of seasonal disruption, highlight key aspects of seasonal biology and summarize from biomedical, anthropological, veterinary, agricultural and environmental perspectives the recent evidence for seasonal desynchronization between environmental factors and internal rhythms. Because annual rhythms are pervasive across biological systems, they provide a common framework for trans-disciplinary research.

Public health surveillance systems are important for tracking disease dynamics. In recent years, social and real-time digital data sources have provided new means of studying disease transmission. Such affordable and accessible data have the potential to offer new insights into disease epidemiology at national and international scales. We used the extensive information repository Google Trends to examine the digital epidemiology of a common childhood disease, chicken pox, caused by varicella zoster virus (VZV), over an 11-y period. We (i) report robust seasonal information-seeking behavior for chicken pox using Google data from 36 countries, (ii) validate Google data using clinical chicken pox cases, (iii) demonstrate that Google data can be used to identify recurrent seasonal outbreaks and forecast their magnitude and seasonal timing, and (iv) reveal that VZV immunization significantly dampened seasonal cycles in informationseeking behavior. Our findings provide strong evidence that VZV transmission is seasonal and that seasonal peaks show remarkable latitudinal variation. We attribute the dampened seasonal cycles in chicken pox information-seeking behavior to VZV vaccine-induced reduction of seasonal transmission. These data and the methodological approaches provide a way to track the global burden of childhood disease and illustrate population-level effects of immunization. The global latitudinal patterns in outbreak seasonality could direct future studies of environmental and physiological drivers of disease transmission.

Epigenetics represents a widely accepted set of mechanisms for how organisms respond to the environment by regulating phenotypic plasticity and life history transitions. Understanding the effects of environmental control on phenotypes and fitness, via epigenetic mechanisms, is essential for understanding the ability of organisms to rapidly adapt to environmental change. This review highlights the significance of environmental temperature on epigenetic control of phenotypic variation, with the aim of furthering our understanding of how epigenetics might help or hinder species’ adaptation to climate change. It outlines how epigenetic modifications, including DNA methylation and histone/chromatin modification, i) respond to temperature and regulate thermal stress responses in different kingdoms of life, ii) regulate temperature-dependent expression of key developmental processes and seasonal phenotypes, iii) facilitate transgenerational epigenetic inheritance of thermal adaptation, iv) adapt populations to local and global climate gradients and finally v) facilitate in biological invasions. Although the evidence points towards a conserved role of epigenetics in responding to temperature change, there appears to be an element of temperature- and species-specificity in the specific effects of temperature change on epigenetic modifications and resulting phenotypic responses. The review identifies areas of future research in epigenetic responses to environmental temperature change.

Seasonal variations in immunity are common in nature, and changes in day length are sufficient to trigger enhancement and suppression of immune function in many vertebrates. Drawing primarily on data from Siberian hamsters, this review describes formal and physiological aspects of the neuroendocrine regulation of seasonal changes in mammalian immunity. Photoperiod regulates immunity in a trait-specific manner, and seasonal changes in gonadal hormone secretion and thyroid hormone signaling all participate in seasonal immunomodulation. Photoperiod-driven changes in the hamster reproductive and immune systems are associated with changes in iodothyronine deiodinase-mediated thyroid hormone signaling, but photoperiod exerts opposite effects on the epigenetic regulation of reproductive neuroendocrine and lymphoid tissues. Photoperiodic changes in immunocompetence may explain a proportion of the annual variance in disease incidence and severity in nature, and provide a useful framework to help understand brain-immune interactions.