Photoperiodic induction without light-mediated circadian entrainment in a high arctic resident bird

Abstract

Organisms use changes in photoperiod to anticipate and exploit favourable conditions in a seasonal environment. While species living at temperate latitudes receive day length information as a year-round input, species living in the Arctic may spend as much as two-thirds of the year without experiencing dawn or dusk. This suggests that specialised mechanisms may be required to maintain seasonal synchrony in polar regions. Svalbard ptarmigan (Lagopus muta hyperborea) are resident at 74–81°N latitude. They spend winter in constant darkness (DD) and summer in constant light (LL); extreme photoperiodic conditions under which they do not display overt circadian rhythms. Here, we explored how Arctic adaptation in circadian biology affects photoperiodic time measurement in captive Svalbard ptarmigan. For this purpose, DD-adapted birds, showing no circadian behaviour, either remained in prolonged DD, were transferred into a simulated natural photoperiod (SNP) or were transferred directly into LL. Birds transferred from DD to LL exhibited a strong photoperiodic response in terms of activation of the hypothalamic thyrotropin-mediated photoperiodic response pathway. This was assayed through expression of the Eya3, Tshβ and deiodinase genes, as well as gonadal development. While transfer to SNP established synchronous diurnal activity patterns, activity in birds transferred from DD to LL showed no evidence of circadian rhythmicity. These data show that the Svalbard ptarmigan does not require circadian entrainment to develop a photoperiodic response involving conserved molecular elements found in temperate species. Further studies are required to define how exactly Arctic adaptation modifies seasonal timer mechanisms.

Evidence for circadian-based photoperiodic timekeeping in Svalbard ptarmigan, the northernmost resident bird

“…Both sexes were used for the experiments as we have not seen any sex differences in hypothalamic gene expression in our previous study. 3 Similarly, the seasonal rhythm in body mass, activity and food intake is similar between the sexes. 6,27 A full table with all birds with their respective experimental group and their respective data is available online at DataverseNO (https://doi.org/10.18710/LUAHFK).…”

“…All in situ hybridization probes (Tshb, Dio2, Dio3, Per2 and Cry1) are based on RNA extracted from Svalbard ptarmigan brain tissue and were designed using a Icelandic ptarmigan genome. 48 Brain cryo-sectioning, probe synthesis and in situ hybridization were performed as reported previously 3,49 and are described in short as follows.…”

Mechanisms of temperature modulation in mammalian seasonal timing

“…A detailed description of the in situ hybridization protocol can be found elsewhere 47,48 . In short, 20 µm coronal brain sections were cut on a cryostat in caudal to rostral direction, starting from the mammillary bodies to the optic chiasm, to cover the area of the hypothalamus and third ventricle.…”

“…A detailed description of the in situ hybridization protocol can be found elsewhere. 47,48 In short, 20 µm coronal brain sections were cut on a cryostat in caudal to rostral direction, starting from the mammillary bodies to the optic chiasm, to cover the area of the hypothalamus and third ventricle. Sections were mounted onto precoated Superfrost Plus slides (Thermo scientific: ref J1800AMNZ) with 6-10 sections per slide and 10 slides per individual.…”

A Chromosome-Level Genome Assembly for the Rock Ptarmigan (Lagopus muta)

“…Future studies into Rock Ptarmigan genomics will benefit from decades of studies into these birds in captivity (Stokkan et al, 1988). Recently, Rock Ptarmigan hatched and raised in captivity have been used for gene expression studies to understand circadian rhythms and investigate the cecal microbiome representing valuable opportunities going forward (Appenroth et al, 2021; Appenroth et al, 2020; Salgado-Flores et al, 2019).…”