Endocrinological studies have contributed considerably to the development of theory concerning the proximate aspects of the timing of reproduction. In non-domesticated, avian species, the relative importance of the photoperiodic and non-photoperiodic factors influencing later stages of the breeding cycle, such as the onset of egg laying, remains unclear because egg laying is difficult to obtain with captive populations and laboratory experiments of breeding are rarely carried out in the framework of long-term field studies. We set up a special experimental design such that captive Mediterranean blue tits (Parus caeruleus) can breed with success in large outdoor aviaries at similar latitudes and altitudes to their wild counterparts. Here we demonstrate experimentally that the non-photoperiodic factors responsible for large and consistent differences in the expression of natural breeding responses between three captive outdoor blue tit populations are ignored during long-day treatment. Based on these findings, an evolutionary explanation is provided for why the relative importance of the non-photoperiodic factors decreases with the progress of the season. The hypothesis can explain observed maladapted breeding dates in free-living populations and could possibly be used to increase the success of breeding programmes with some endangered, captive, non-domesticated, photoperiodic species.