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

Abstract

Sexual selection favours the expression of traits in one sex that attract members of the opposite sex for mating. The nature of sexually selected traits such as vocalization, colour and ornamentation, their fitness benefits as well as their costs have received ample attention in field and laboratory studies. However, sexually selected traits may not always be expressed: coloration and ornaments often follow a seasonal pattern and behaviours may be displayed only at specific times of the day. Despite the widely recognized differences in the daily and seasonal timing of traits and their consequences for reproductive success, the actions of sexual selection on the temporal organization of traits has received only scant attention. Drawing on selected examples from bird and mammal studies, here we summarize the current evidence for the daily and seasonal timing of traits. We highlight that molecular advances in chronobiology have opened exciting new opportunities for identifying the genetic targets that sexual selection may act on to shape the timing of trait expression. Furthermore, known genetic links between daily and seasonal timing mechanisms lead to the hypothesis that selection on one timescale may simultaneously also affect the other. We emphasize that studies on the timing of sexual displays of both males and females from wild populations will be invaluable for understanding the nature of sexual selection and its potential to act on differences within and between the sexes in timing. Molecular approaches will be important for pinpointing genetic components of biological rhythms that are targeted by sexual selection, and to clarify whether these represent core or peripheral components of endogenous clocks. Finally, we call for a renewed integration of the fields of evolution, behavioural ecology and chronobiology to tackle the exciting question of how sexual selection contributes to the evolution of biological clocks.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Keywords: circadian rhythm; circannual rhythm; display behaviour; sexual selection; timing of reproduction.

Figure 1.

Hypothetical surface profile representation of the timing of a trait and its interaction with the quality of its expression (e.g. size, colour and complexity). Examples for specific traits could be bird song, or ornaments in birds and mammals. Sexual selection would favour an early expression of this trait, while fecundity/viability selection may act against an early display. Likewise, sexual selection would promote a high quality of trait expression, while fecundity/viability selection would act against the expression of the highest quality traits. Consequently, only individuals of the highest quality would be able to sustain the costs of displaying this trait early and at high quality, but would gain maximal reproductive success. Specifics of surface profile depend on parametrization of the model, and this representation serves mainly illustrative and not quantitative purposes. For additional explanations, see text. (Online version in colour.)

Figure 2.

Daily and annual timing share neurobiological and molecular pathways. In birds and mammals, the annual timing mechanism uses input from the circadian (daily) timing mechanism at the neurobiological and at the molecular level. In birds (a), light regulates the circadian system through photoreceptors in the pineal gland and various opsin-expressing brain areas, with the eyes playing a species-specific role in circadian organization. The avian pineal gland produces melatonin and contains a self-sustained circadian oscillator which, together with the suprachiasmatic nucleus (SCN), regulates daily timing in physiology and behaviour. In mammals (b), light input from the retina stimulates the SCN, which regulates daily timing in behaviour, physiology and melatonin production in the pineal gland. Melatonin receptors in the pars tuberalis (PT) of the pituitary regulate annual timing by thyroid-stimulating hormone (TSH) signalling to the tanycytes in the third ventricle (3V) wall, which in turn regulate thyroid hormone and gonadotropin-releasing hormone signalling, regulating gonadotropin secretion by the PT and subsequent annual timing of reproduction. Contrastingly, in birds (a), melanopsin-positive cerebrospinal fluid-contacting neurons in the 3V wall can directly signal photoperiodic information to the PT-tanycyte pathway, regulating annual timing of reproduction. At the molecular level, the core vertebrate circadian oscillator (c) consists of the BMAL1::CLOCK transcription factor inducing Per and Cry genes which, after dimerization, repress their own promotor activation by the BMAL1::CLOCK dimer. This oscillatory feedback mechanism causes rhythmical induction of BMAL1 which, after dimerizing with CLOCK, produces circadian regulation of output genes like Tef, Hlf and other clock-controlled genes regulating daily rhythms in cellular physiology and metabolism. Synaptic light input signalling to the SCN causes Per induction ((c) lightning symbol) and entrainment to the external light–dark cycle. In mammals, a similar circadian feedback network resides in the PT (d), but here melatonin induces Cry ((d) top lightning symbol), while BMAL1::CLOCK induces Tef and Hlf enhances BMAL1::CLOCK induction of Eya3. Under long winter nights, the induction of Eya3 is fully blocked by melatonin still present in the morning. When morning melatonin is absent during long summer days, EYA3 will cause TSH release, leading to tanycyte thyroid hormone production and, in long-day breeders ((d) bottom lightning symbol), to subsequent gonadotropin production by the pituitary, leading to seasonal gonadal development. ccg, clock-controlled gene. See www.genecards.org for full names of abbreviated genes. (Online version in colour.)

Figure 3.

Onset of daily activity influences reproductive success. (a) Treatment of wild great tit males with a melatonin implant delayed their activity onset (data represent individual averages from 2 to 19 days of recording), and (b) melatonin-treated males also suffered a greater cuckoldry risk (higher proportion of extra-pair (EP) young in their nest). Data points represent mean values for individuals, and vertical lines indicate the mean ± s.e.m. for each treatment group. Adapted from [78].

Figure 4.

Timing of daily activity onset (x-axis) in adult European ground squirrels at different seasonal stages (y-axis). Males: filled symbols and solid lines, females: open symbols and broken line. During the pre-mating and mating phases, males are active at earlier times than females, while the opposite pattern occurs during lactation and pre-hibernation. CET, Central European Time. Redrawn after data from Everts et al. [173].