Phenology refers to the periodic appearance of life-cycle events and currently receives abundant attention as the effects of global change on phenology are so apparent. Phenology as a discipline observes these events and relates their annual variation to variation in climate. But phenology is also studied in other disciplines, each with their own perspective. Evolutionary ecologists study variation in seasonal timing and its fitness consequences, whereas chronobiologists emphasize the periodic nature of life-cycle stages and their underlying timing programmes (e.g. circannual rhythms). The (neuro-) endocrine processes underlying these life-cycle events are studied by physiologists and need to be linked to genes that are explored by molecular geneticists. In order to fully understand variation in phenology, we need to integrate these different perspectives, in particular by combining evolutionary and mechanistic approaches. We use avian research to characterize different perspectives and to highlight integration that has already been achieved. Building on this work, we outline a route towards uniting the different disciplines in a single framework, which may be used to better understand and, more importantly, to forecast climate change impacts on phenology.

Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. We tested the direct effect of temperature on laying dates in great tits (Parus major) using climatized aviaries in a 6-year experiment. We mimicked the temperature patterns from two specific years in which our wild population laid either early ('warm' treatment) or late ('cold' treatment). Laying dates were affected by temperature directly. As the relevant temperature period started three weeks prior to the mean laying date, with a range of just 48C between the warm and the cold treatments, and as the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. We furthermore show a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. Our results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.

Timing of reproduction in temperate-zone birds is strongly correlated with spring temperature, with an earlier onset of breeding in warmer years. Females adjust their timing of egg laying between years to be synchronized with local food sources and thereby optimize reproductive output. However, climate change currently disrupts the link between predictive environmental cues and spring phenology. To investigate direct effects of temperature on the decision to lay and its genetic basis, we used pairs of great tits (Parus major) with known ancestry and exposed them to simulated spring scenarios in climate-controlled aviaries. In each of three years, we exposed birds to different patterns of changing temperature. We varied the timing of a temperature change, the daily temperature amplitude, and the onset and speed of a seasonal temperature rise. We show that females fine-tune their laying in response to a seasonal increase in temperature, whereas mean temperature and daily temperature variation alone do not affect laying dates. Luteinizing hormone concentrations and gonadal growth in early spring were not influenced by temperature or temperature rise, possibly posing a constraint to an advancement of breeding. Similarities between sisters in their laying dates indicate genetic variation in cue sensitivity. These results refine our understanding of how changes in spring climate might affect the mismatch in avian timing and thereby population viability.

Summary 1.Breeding at the right time of the year is crucial for many temperate zone organisms, as any mismatch with their optimal breeding period leads to a reduction in fitness. The roles of the breeding partners in these adaptive decisions have, however, only rarely been studied. 2. In blue tits ( Cyanistes caeruleus ) that breed in heterogenous Mediterranean habitats, nearby populations show up to 1-month differences in breeding time. This difference is adaptive as the optimal time for breeding varies by the same amount due to habitat characteristics. But which sex is determining this large difference in timing? 3. We show here that the seasonal development of female reproductive activity (yolk precursor production) closely matches the local optimal breeding time in these two highly contrasted landscapes, while previous studies have demonstrated that male gonadal development does not. In accordance with this, quantitative genetic analyses reveal that timing for breeding is determined by the female only, with no evidence for an additive genetic male effect on laying date. 4. Our results strongly suggest that the adaptive inter-population difference in the laying periods has been driven by females. The central role of females in the determination of breeding period needs to be included when studying how micro-evolutionary processes are affected by global climate change.

How temperature affects the timing of life cycles in warm-blooded organisms remains a mystery but must be addressed in order to predict the future consequences of global warming.