Polymorphism of winter phenotype in Siberian hamster: consecutive litters do not differ in photoresponsiveness but prolonged acclimation to long photoperiod inhibits winter molt

Abstract

Background The theory of delayed life history effects assumes that phenotype of adult individual results from environmental conditions experienced at birth and as juvenile. In seasonal environments, being born late in the reproductive season affects timing of puberty, body condition, longevity, and fitness. We hypothesized that late-born individuals are more prone to respond to short photoperiod (SP) than early born ones. We used Siberian hamsters Phodopus sungorus, a model species characterized by high polymorphism of winter phenotype. We experimentally distinguished the effect of litter order (first or third) from the effect of exposure to long photoperiod (LP) before winter (3 months or 5 months) by manipulating the duration of LP acclimation in both litters. We predicted that, irrespective of the litter order, individuals exposed to long photoperiod for a short time have less time to gather energy resources and consequently are more prone to developing energy-conserving phenotypes. To assess effect of litter order, duration of acclimation to long days, and phenotype on basal cost of living we measured basal metabolic rate (BMR) of hamsters. Results Individuals born in third litters had faster growth rates and were bigger than individuals from first litters, but these differences vanished before transfer to SP. Litter order or duration of LP acclimation had no effects on torpor use or seasonal body mass changes, but prolonged acclimation to LP inhibited winter molting both in first and third litters. Moreover, individuals that did not molt had significantly higher BMR in SP than those which molted to white fur. Although one phenotype usually predominated within a litter, littermates were often heterogeneous. We also found that over 10% of individuals presented late response to short photoperiod. Conclusions Our data indicate that duration of postnatal exposure to LP may define propensity to photoresponsiveness, regardless of the litter in which animal was born. Existence of littermates presenting different phenotypes suggests a prudent reproductive strategy of investing into offspring of varied phenotypes, that might be favored depending on environmental conditions. This strategy could have evolved in response to living in stochastic environment.

Housing conditions modify seasonal changes in basal metabolism and body mass of the Siberian hamster, Phodopus sungorus

“…Although BMR is typically negatively related to mean T a in the environment and positively correlated with m b (Lovegrove 2003 ; Rezende et al 2004 ; Raichlen et al 2010 ; White and Kearney 2013 ; Naya et al 2018 ), there is also a considerable intraspecific variation in BMR (Genoud et al 2018 ). In Siberian hamsters seasonal changes in BMR may depend on the litter in which hamsters were born or on the degree of seasonal changes in the phenotype ( m b , fur properties, reproductive status, daily torpor; Przybylska-Piech et al 2021 ; but see Przybylska et al 2019a ). Variability of seasonal changes in BMR observed in hamsters originating from the same breeding colony (Boratyński et al 2016 ; Przybylska et al 2019a , 2021 ) but housed under different conditions, highlights the importance of considering and controlling for the cage enrichment and housing conditions during comparative analyses.…”

“…In Siberian hamsters seasonal changes in BMR may depend on the litter in which hamsters were born or on the degree of seasonal changes in the phenotype ( m b , fur properties, reproductive status, daily torpor; Przybylska-Piech et al 2021 ; but see Przybylska et al 2019a ). Variability of seasonal changes in BMR observed in hamsters originating from the same breeding colony (Boratyński et al 2016 ; Przybylska et al 2019a , 2021 ) but housed under different conditions, highlights the importance of considering and controlling for the cage enrichment and housing conditions during comparative analyses.…”

“…The hamsters respond to short photoperiod by adjusting several traits that constitute its winter phenotype. Namely, they decrease m b , molt to a white fur, regress gonads and use daily torpor (Figala et al 1973 ; Hoffmann 1973 ; Heldmaier and Steinlechner 1981a , b ; Lynch and Puchalski 1986 ; Ruf and Heldmaier 1992 ; Ruf et al 1993 ; Przybylska-Piech et al 2021 ). Boratyński et al ( 2016 ) also found that Siberian hamsters acclimated to winter-like conditions had lower whole animal BMR than summer-acclimated ones.…”