Photoperiod is involved in the regulation of seasonal breeding in male water voles (Arvicola terrestris)

Mammals living at temperate latitudes typically display annual cyclicity in their reproductive activity: births are synchronized when environmental conditions are most favorable. In a majority of these species, daylength is the main proximate factor used to anticipate seasonal changes and to adapt physiology. The brain integrates this photoperiodic signal through key hypothalamic structures, which regulate the reproductive axis. In this context, our study aims to characterize regulations that occur along the hypothalamo-pituitary-gonadal (HPG) axis in male fossorial water voles (Arvicola terrestris, also known as Arvicola amphibius) throughout the year and to further probe the implication of photoperiod in these seasonal regulations. Our monthly field monitoring shows dramatic seasonal changes in the morphology and activity of reproductive organs, as well as in the androgen-dependent lateral scent glands. Moreover, our data uncover seasonal variations at the hypothalamic level. During the breeding season, Kisspeptin expression in the arcuate nucleus (ARC) decreases, while RFRP3 expression in the dorsomedial hypothalamic nucleus (DMH) increases. Our follow-up laboratory study reveals activation of the reproductive axis and confirms a decrease in Kisspeptin expression in males exposed to a long photoperiod (summer condition) compared to those maintained under a short photoperiod (winter condition) that retain all features reminiscent of sexual inhibition. Altogether, our study characterizes neuroendocrine and anatomical markers of seasonal reproductive rhythmicity in male water voles and further suggests that these seasonal changes are chiefly driven by photoperiod.

Mirror replication of sexual facial expressions increases the success of sexual contacts in bonobos

Rapid Facial Mimicry (RFM), one of the possible predictors of emotional contagion, is defined as the rapid, involuntary and automatic replication of a facial expression. Up to now, RFM has been demonstrated in nonhuman animals exclusively during play. Since in bonobos, as in humans, socio-sexuality is a powerful tool for assessing/strengthening inter-individual relationships, we investigated RFM in this domain. Bonobos displayed silent bared-teeth (sbt, the most common facial expression during sexual contacts) more frequently after the detection of an sbt emitted by the trigger than in the no-detection condition. This is the first demonstration of the presence of RFM during sex. The occurrence of RFM was positively affected by the sex of the partners with female homo-sexual contacts being punctuated by a higher presence of RFM. At an immediate level, RFM increased the duration of homo- and hetero-sexual contacts. This finding suggests that RFM can increase individuals’ potential fitness benefits. By prolonging their sexual contacts, females can strengthen their social relationships thus increasing the probability to obtain priority over resources (RFM indirect fitness benefits). Via longer copulations, males can increase the probability to make females pregnant (RFM direct fitness benefits). In conclusion, in bonobos the access to the partner’s face during sexual contacts (face-to-face, proximate factor) and the role of socio-sexuality in increasing the individual direct and indirect fitness (ultimate factor) could have favoured the evolution of specific sexual facial expressions and their rapid mirror replication. Our findings on bonobos expand the role of RFM well beyond the animal play domain thus opening new scenarios for future comparative studies exploring the evolution of socio-sexuality in humans.

Circadian versus circannual rhythm in the photoperiodic programming of seasonal responses in Eurasian tree sparrow (Passer montanus)

Experiments were done on the subtropical tree sparrow to examine whether day length, as a proximate factor, involves circadian rhythm in timing seasonal responses or these events are programmed by the mediation of endogenous circannual rhythm.

Delayed mite hatching in response to mechanical stimuli simulating egg predation attempts

Delayed or induced hatching in response to predation risk has been reported mainly in aquatic systems, where waterborne cues from predators and injured neighbouring eggs are available. Newly emerged larvae of the terrestrial predatory mite Neoseiulus womersleyi are vulnerable to predation by con- and heterospecific predatory mites, whereas their eggs are not. We examined whether N. womersleyi embryos delay hatching in response to artificial mechanical stimuli that simulates egg predation attempts. When embryos near the hatching stage were artificially stimulated every 5 min for 60 min, most stopped hatching for the duration of the 60-min period, whereas unstimulated embryos did not. Stimulated embryos resumed hatching when the treatment was stopped, and the proportion of hatched stimulated embryos caught up with that of unstimulated embryos within 120 min after stimuli stopped. Since hatching did not stop in response to changes in gravity direction, the effect of direct mechanical stimuli on the eggs was considered a proximate factor in delayed hatching. These results suggest that N. womersleyi embryos recognise immediate predation risk via mechanical stimuli, and delay hatching until the predation risk is reduced.

Annual and lunar breeding rhythmicity in females of the terrestrial hermit crab Coenobita rugosus H. Milne Edwards, 1837 (Decapoda: Anomura: Coenobitidae) in Okinawa, Japan

We investigated the reproductive characteristics of a terrestrial hermit crab (Coenobita rugosus H. Milne Edwards, 1837) inhabiting Okinawa-Jima. Monthly changes in the gonadosomatic index and ovarian histology revealed that this species had fully developed oocytes from May to October. Data showing that females with (ovigerous females) and without (non-ovigerous females) embryos on their pleopods appeared simultaneously on the shore from June to September 2014 demonstrates that this species undergoes larval release several times for four months. When non-ovigerous females were reared under a combination of two day lengths and two temperatures, oocyte development was induced in the high-temperature group, suggesting that temperature is a proximate factor in ovarian development. The weekly collection of females during the spawning season revealed that the proportion of fully developed oocytes in an ovary increased toward the time of the new moon and decreased around the first-quarter moon, suggesting that this species is a lunar-spawner with a new-moon preference. Some females releasing larvae around the new or full moon were recaptured at approximately 30 d intervals, suggesting at least two major groups with lunar-synchronized larval release. The ovarian development and larval release of C. rugosus are likely entrained to external factors, which change periodically in their habitats.

Timing of Breeding

This chapter argues that the timing of the initiation of a single breeding event, or the initiation of the first of multiple breeding events within the same breeding season, is completely dependent on the female-specific reproductive process of timing of egg production and egg-laying. It discusses how early-season events are critical in determining timing of breeding; fitness consequences of timing decisions; selection on timing of breeding; sex-specific response mechanisms for timing of breeding; physiological mechanisms associated with photoperiod (day length) as a proximate factor; physiological mechanisms associated with temperature as a proximate factor; and physiological mechanisms associated with food availability as a “proximate” factor.