• Energy Research

Timekeeping is important at two levels: to time changes in physiology and behavior within each day and within each year. For the former, birds have a system of at least three independent circadian clocks present in the retina of the eyes, the pineal gland, and the hypothalamus. This differs from the situation in mammals in which the input, pacemaker, and output are localized in different structures. Each bird clock interacts with at least one other clock, and together, they appear to form a centralized clock system that keeps daily time. These clocks have a powerful endogenous component, and the daily light-dark cycle entrains them to 24 h. The timing and duration of life history stages that make up annual cycle of an individual must also be controlled by some form of timekeeping. However, evidence for the existence of an equivalent endogenous circannual clock is less clear. Environmental cues, particularly photoperiod, appear to have a more direct role than simply entraining the clock to calendar time. For example, the timing of migration is probably greatly influenced by photoperiod, but its manifestation each day, as Zugunruhe, appears to be under circadian control. Migration involves marked changes in physiology to cope with the energetic demands. There is still much that we do not know about how organisms' timekeeping systems respond to their natural environment, particularly how salient signals from the environment are perceived and then transduced into appropriately timed biological functions. However, given that changes in environmental input affects the clock, increasing human disturbance of the environment is likely to adversely affect these systems.

Many bird species have advanced their seasonal timing in response to global warming, but we still know little about the causal effect of temperature. We carried out experiments in climate-controlled aviaries to investigate how temperature affects luteinizing hormone, prolactin, gonadal development, timing of egg laying and onset of moult in male and female great tits. We used both natural and artificial temperature patterns to identify the temperature characteristics that matter for birds. Our results show that temperature has a direct, causal effect on onset of egg-laying, and in particular, that it is the pattern of increase rather than the absolute temperature that birds use. Surprisingly, the pre-breeding increases in plasma LH, prolactin and in gonadal size are not affected by increasing temperature, nor do they correlate with the onset of laying. This suggests that the decision to start breeding and its regulatory mechanisms are fine-tuned by different factors. We also found similarities between siblings in the timing of both the onset of reproduction and associated changes in plasma LH, prolactin and gonadal development. In conclusion, while temperature affects the timing of egg laying, the neuroendocrine system does not seem to be regulated by moderate temperature changes. This lack of responsiveness may restrain the advance in the timing of breeding in response to climate change. But as there is heritable genetic variation on which natural selection can act, microevolution can take place, and may represent the only way to adapt to a warming world.

AbstractMany organisms advance their seasonal reproduction in response to global warming. In birds, which regress their gonads to a nonfunctional state each winter, these shifts are ultimately constrained by the time required for gonadal development in spring. Gonadal development is photoperiodically controlled and shows limited phenotypic plasticity in relation to environmental factors, such as temperature. Heritable variation in the time required for full gonadal maturation to be completed, based on both onset and speed of development and resulting in seasonally different gonad sizes among individuals, is thus a crucial prerequisite for an adaptive advancement of seasonal reproduction in response to changing temperatures. We measured seasonal gonadal development in climate‐controlled aviaries for 144 great tit (Parus major) pairs, which consisted of siblings obtained as whole broods from the wild. We show that the extent of ovarian follicle development (follicle size) in early spring is highly heritable (h2 = 0.73) in females, but found no heritability of the extent of testis development in males. However, heritability in females decreased as spring advanced, caused by an increase in environmental variance and a decrease in additive genetic variation. This low heritability of the variation in a physiological mechanism underlying reproductive timing at the time of selection may hamper genetic adaptation to climate change, a key insight as this great tit population is currently under directional selection for advanced egg‐laying.

1.Annual variation in the timing of avian reproduction is associated with predictive cues related to ambient temperature. Understanding how these cues affect timing, and estimating the genetic variation in sensitivity to these cues, is essential to predict the micro-evolutionary changes in timing which are needed to adapt to climate change. 2.We carried out a 2-year experiment with great tits Parus major of known genetic background, which were kept in pairs in climate-controlled aviaries with simulated natural photoperiod and exposed to a seasonal change in temperature, where the two treatments differed by 4 °C. We recorded the dates of laying the first and last eggs and timing of moult, as well as physiological proxies associated with reproduction: plasma luteinizing hormone (LH), prolactin, and gonadal size at four-weekly intervals. 3.The temperature treatments did not affect first-egg dates, nor gonadal growth or plasma LH and prolactin concentrations. However, birds terminated egg laying, regressed their testes and started their moult earlier at higher temperatures. 4.There were marked family differences in both the start of egg laying, with sisters from early laying maternal families laying early, and in the termination of laying, indicating that there is heritable variation in sensitivity to cues involved in timing. 5.Our experiment, the first to use genetically related individuals in an experimental design with a natural change in photoperiod and biologically realistic temperature differences, thus shows that genetic adaptation in cue sensitivity is possible, essential for species to be able to adapt to a warming world.

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.