statement: Development of the neuroendocrine system driving photoperiodic 34 responses in gonadal and somatic growth differ between the common and the tundra vole, 35 indicating that they use a different breeding strategy. 36 37 List of abbreviations: 38 ARC -arcuate nucleus 39 Dio2 -iodothyronine-deiodinase 2 40 Dio3 -iodothyronine-deiodinase 3 41 Dnmt1 -DNA methyltransferase 1 42 Dnmt3a -DNA methyltransferase 3a 43 GH -growth hormone 44 GnRH -gonadotropin-releasing hormone 45 Kiss1 -Kisspeptin 46 KNDy -kisspeptin/neurokininB/Dynorphin 47 PNESphotoperiodic neuroendocrine system 50 PTpars tuberalis 51 SCN -suprachiasmatic nucleus 52 SPshort photoperiod 53 Tsh -thyroid-stimulating-hormone- subunit 54 55 56 57 58 59 60 61 62 63 64 65 66 Abstract 67To optimally time reproduction, seasonal mammals use a photoperiodic neuroendocrine 68 system (PNES) that measures photoperiod and subsequently drives reproduction. To adapt to 69 late spring arrival at northern latitudes, a lower photoperiodic sensitivity and therefore a 70 higher critical photoperiod for reproductive onset is necessary in northern species to arrest 71 reproductive development until spring onset. Temperature-photoperiod relationships, and 72 hence food availability-photoperiod relationships, are highly latitude dependent. Therefore, 73we predict PNES sensitivity characteristics to be latitude-dependent. Here, we investigated 74 photoperiodic responses at different times during development in northern-(tundra/root vole, 75Microtus oeconomus) and southern vole species (common vole, Microtus arvalis) exposed to 76 constant short (SP) or long photoperiod (LP). 77 M. oeconomus grows faster under LP, whereas no photoperiodic effect on somatic 78 growth is observed in M. arvalis. Contrastingly, gonadal growth is more sensitive to 79 photoperiod in M. arvalis, suggesting that photoperiodic responses in somatic and gonadal 80 growth can be plastic, and might be regulated through different mechanisms. In both species, 81 thyroid-stimulating-hormone- subunit (Tsh) and iodothyronine-deiodinase 2 (Dio2) 82 expression is highly increased under LP, whereas Tshr and Dio3 decreases under LP. High 83 Tshr levels in voles raised under SP may lead to increased sensitivity to increasing 84 photoperiods later in life. The higher photoperiodic induced Tshr response in M. oeconomus 85 suggests that the northern vole species might be more sensitive to TSH when raised under SP. 86 Species differences in developmental programming of the PNES, which is dependent 87 on photoperiod early in development, may form part divergent breeding strategies evolving 88 as part of latitudinal adaptation. 89 90
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