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

Abstract

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.

Population density does not affect seasonal regulation of reproductive physiology in male water voles

“…A seasonal rhythm in male reproductive function was observed over the 3 years of monitoring. The greater mass of testes in voles trapped in spring compared to autumn is consistent with the findings of previous studies [19,22,24]. This result suggests greater testicular activity in the spring than in the autumn.…”

“…In April and May, plasma testosterone levels would therefore not have peaked, and consequently, LSGs would not have reached full development in water voles at the time of capture. This result is consistent with previous data that did not show significant differences between spring and autumn; only finerscale annual monitoring would allow seasonal variations to be observed [19,22]. Mammals living in temperate latitudes use yearly variation in day length ( photoperiod) as the most predictive environmental cue to adapt their physiology to seasonal changes in the environment, notably for synchronizing their reproductive activity [33,34].…”

“…To minimize the effects of seasonal body mass variations in analyses, an organ-to-body mass ratio was used to study the relative mass of testes and seminal vesicles. Similarly, the lateral scent gland (LSG) surface was divided by body size to provide a relative surface index as previously described [22]. The body condition index (BCI) is the ratio of body mass to body length.…”

GnRHand the photoperiodic control of seasonal reproduction: Delegating the task to kisspeptin andRFRP‐3

“…Thereafter, a number of studies reported a very similar photoperiodic pattern of RFRP-3 mRNA/protein expression in many seasonal mammals. This is true not only for long-day breeders such as male and female Syrian and Siberian hamsters, 195,230,239,251,260 female Turkish hamsters, 206 male European hamsters, 114 male and female Jerboas, 197 female Brandt's voles, 200 male water voles 261 and male wild-derived mice, 202 but also for short-day breeders such as ewes, 231,232 female brushtail possums, 262 female goats, 263 and male and female dromedary camels. 201 Additionally, the number of RFRP-3 fibers contacting GnRH neurons in the Siberian hamster and ewe 232,239 and NpffR2 expression in the Syrian hamster 238 are lower in short-compared to long-day conditions.…”

Drought disrupts year-round breeding readiness in a tropical songbird

“…Determining how organisms respond to drier conditions has thus emerged as a key goal for both conservationists and ecologists (Rees et al 2009, Albright et al 2010, Brodie et al 2012. Unlike most temperate zone inhabitants that rely on seasonal changes in photoperiod as a key phenological cue (Dawson et al 2001, Wingfield 2005, Poissenot et al 2021, for many tropical species variation in precipitation is used to time breeding (Moreau 1950, Boag and Grant 1984, Shine and Brown 2008, Skagen et al 2018, Aranzamendi et al 2019, Halali et al 2021. Precipitation can serve as a reliable predictive cue of food availability, especially in insectivorous bird species (Poulin et al 1992, McKinnon et al 2015, Aranzamendi et al 2019).…”