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

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). M. oeconomus grows faster under LP, whereas no photoperiodic effect on somatic growth is observed in M. arvalis. Contrastingly, gonadal growth is more sensitive to photoperiod in M. arvalis, 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-{beta} subunit (Tsh{beta}) 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 M. oeconomus suggests that the northern vole species might be more sensitive to TSH when raised under SP. Species differences in developmental programming of the PNES, which is dependent on photoperiod early in development, may form part divergent breeding strategies evolving as part of latitudinal adaptation. Summary statementDevelopment of the neuroendocrine system driving photoperiodic responses in gonadal and somatic growth differ between the common and the tundra vole, indicating that they use a different breeding strategy.