Early to rise, early to breed: a role for daily rhythms in seasonal reproduction

Abstract

Vertebrates use environmental cues to time reproduction to optimal breeding conditions. Numerous laboratory studies have revealed that light experienced during a critical window of the circadian (daily) rhythm can influence reproductive physiology. However, whether these relationships observed in captivity hold true under natural conditions and how they relate to observed variation in timing of reproductive output remains largely unexplored. Here we test the hypothesis that individual variation in daily timing recorded in nature (i.e. chronotype) is linked with variation in timing of breeding. To address this hypothesis and its generality across species, we recorded incubation behavior data to identify individual patterns in daily onset of activity for 2 temperate-breeding songbird species, the dark-eyed junco (Junco hyemalis aikeni) and the great tit (Parus major). We found that females who first departed from their nest earlier in the morning (earlier chronotype) also initiated nests earlier in the year. Date of data collection and ambient temperature had no effect, but stage of incubation influenced daily onset of activity in great tits. Our findings suggest a role for daily rhythms as one mechanism underlying the observed variation in seasonal timing of breeding.

Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

“…Studies of repeated journeys of individuals in some species have revealed between-individual variation in combination with high individual consistency [16,[93][94][95][96]. Similar findings have been reported for daily behaviours of animals, where chronotype has become an increasingly popular measure [55,[97][98][99][100][101].…”

“…remaining relatively early or late members of the population). In practice, environmental effects can often be accounted for, for example, by identifying work days for the exemplary human chronotype discussed above (table 1d; [13]), or by accounting for year of study when analysing reproductive phenology [143] or avian activity and sleep timing [101,142]. Moreover, whenever possible, chronotype should reflect an individual's characteristic phase, rather than singular timing events.…”

“…Such fitness differences could arise from timing-dependent selection pressures identified above, for example via energy requirements, foraging and mating opportunities, or predation risks ( figure 3). Consequently, ecologists are keen to quantify chronotype and its repeatability for individuals [93,100,101,[139][140][141][142]. Under strong directional environmental pressure, entire local populations can modify chronotype, as for example observed in marine midges exposed to different tidal regimes [50].…”

Timing as a sexually selected trait: the right mate at the right moment

“…Indeed, a few phenotypic connections between circadian and annual timing systems have recently been discovered. For example, a phenotypic link between daily (first morning departure from the nest) and seasonal chronotypes (nest initiation dates) has recently been documented in females of two songbird species [70]. Additional specific examples will be discussed below.…”

Variation in chronotype is associated with migratory timing in a songbird

“…absence of zeitgebers) contributes to differences in seasonal timing of events stimulated by increasing daylengths (hereafter, 'spring' events) [12,13]. Although chronotype has been used previously as an indicator of intrinsic period, chronotype itself, as an expression of an organism's entrained circadian clock under natural conditions, may be of greater biological relevance [29].…”