Gonads or body? Differences in gonadal and somatic photoperiodic growth response in two vole species

Abstract

To optimally time reproduction, seasonal mammals use a photoperiodic neuroendocrine system (PNES) that measures photoperiod and subsequently drives reproduction. To adapt to late spring arrival at northern latitudes, a lower photoperiodic sensitivity and therefore a higher critical photoperiod for reproductive onset is necessary in northern species to arrest reproductive development until spring onset. Temperature-photoperiod relationships, and hence food availability-photoperiod relationships, are highly latitude dependent. Therefore, we predict PNES sensitivity characteristics to be latitude-dependent. Here, we investigated photoperiodic responses at different times during development in northern (tundra/root vole, Microtus oeconomus) and southern vole species (common vole, Microtus arvalis) exposed to constant short (SP) or long photoperiod (LP). Although, the tundra vole grows faster under LP, no photoperiodic effect on somatic growth is observed in the common vole. Contrastingly, gonadal growth is more sensitive to photoperiod in the common vole, suggesting that photoperiodic responses in somatic and gonadal growth can be plastic, and might be regulated through different mechanisms. In both species, thyroid-stimulating-hormone-β subunit (Tshβ) and iodothyronine- deiodinase 2 (Dio2) expression is highly increased under LP, whereas Tshr and Dio3 decreases under LP. High Tshr levels in voles raised under SP may lead to increased sensitivity to increasing photoperiods later in life. The higher photoperiodic induced Tshr response in tundra voles suggests that the northern vole species might be more sensitive to TSH when raised under SP. In conclusion, species differences in developmental programming of the PNES, which is dependent on photoperiod early in development, may form different breeding strategies evolving as part of latitudinal adaptation.

Mechanisms of temperature modulation in mammalian seasonal timing

“…52,53 Gene expression patterns in the pars tuberalis (ie, Tshβ) and tanycytes (Dio2, Dio3) also follow a positive relationship to photoperiod (Figure 3), which supports previous findings confirming photoperiodic responsiveness of those genes in common voles. 44,45 Here we show that photoperiodic relationships can be described by dose-response curves, from which critical photoperiods can be derived as inflexion points, ED50. Whether photoperiod can be seen as a dose is debatable, since it has been shown that it is not the photoperiodic length per se, but rather the circadian phase at which light is perceived that determines melatonin suppression leading to photoperiodic responses.…”

“…Our data describe full dose-response curves, and show that indeed the sensitivity to photoperiod has increased in animals born under SP, which explained increased responses to intermediate photoperiods. Increased Tshr expression in the tanycytes early in development of vole and hamsters raised under constant SP, 11,45 may lead to increased TSH sensitivity, which may therefore provide an explanation for elevated Dio2, and reduced Dio3 levels in spring animals compared to autumn animals (Figure 3).…”

“…Postweaning photoperiods were (hours light: hours dark): 18L:6D, 16L:8D, 14L:10D, 12L:12D, 10L:14D, 8L:16D, and 6L:18D. Physiological data from 8L:16D was published elsewhere, 45 and was only applied in the winter-born group. While all postweaning photoperiods were applied at 21°C, the extreme photoperiods were omitted at 10°C for experimental efficiency (Figure 1).…”

“…The neuroanatomy, genes, and promotor elements that are crucial in this response pathway, have been identified in several mammalian and bird species, 30,[36][37][38][39][40][41][42][43] including the common vole, Microtus arvalis. 44,45 Recently, Sáenz de Miera and colleagues demonstrated that the Tsh-Dio2/Dio3 system is subjected to photoperiodic regulation in utero, before the fetal pineal gland starts to produce a rhythmic melatonin signal, indicating that early life maternal photoperiodic programming operates through this pathway. 11 To explore the levels at which photoperiodic history and thermal cues are integrated in the photoperiodic neuroendocrine system (PNES), we manipulated photoperiodic history, postweaning photoperiod and ambient temperature in captive reared common voles (M. arvalis, Pallas 1778), a species in which flexible timing of reproduction is extensively documented, and assessed gonadal and somatic development alongside hormone levels and hypothalamic gene expression.…”

Gut microbiota is associated with the effect of photoperiod on seasonal breeding in male Brandt’s voles (Lasiopodomys brandtii)

“…We hypothesize that photoperiod may affect seasonal breeding by adjusting the composition of gut microbiota. We expect that (1) as compared to long-day (LD) photoperiod, short-day (SD) photoperiod reduces reproduction performance as characterized by a decrease in weight of reproductive organs (testis and epididymis), levels of serum hormones (FSH, LH, and T), hypothalamic genes ( Dio2 , Rfrp-3 , and Kiss-1 ), and testicular genes ( Dio2 , Kiss-1 , and GPR54 ), but increase in levels of serum hormone (MT) and testicular genes ( Dio3 and Stra8 ), and aggressive behavior, as demonstrated in various species [ 14 , 42 , 43 ]; (2) there is a significant difference in the composition of gut microbiota between SD and LD voles, which is associated with reproduction performance; and (3) implantation of specific gut microbiota into recipient voles can trigger similar photoperiod-induced changes in the performance of reproduction and behavior compared with those in SD and LD donor voles.…”