The reproductive response of collared lemmings (Dicrostonyx groenlandicus) to photoperiod is unique for rodents. Whereas most reproductively photoresponsive rodents show maximal gonadal growth when exposed to long photoperiod (long day), collared lemmings show delayed maturation when born and maintained under this condition. However, transfer of lemmings from short photoperiod (short day) to long day results in maximal gonadal growth, indicating that the response to long day depends upon photoperiod history. We hypothesized that the slowing of maturation observed in animals born and maintained on long day reflects an inability to respond fully to long day, resulting from the absence of previous exposure to short day. To determine whether young lemmings born in long day are capable of being stimulated by long day, we exposed them at weaning (19 days of age) to 1, 6 or 10 weeks of short day, and then challenged them with a second exposure to long day. Relative to animals transferred permanently to short day at weaning, lemmings exposed to 6 weeks of short day showed accelerated gonadal growth after both 5 and 10 weeks of subsequent exposure to long day, and those exposed to 10 weeks of short day had larger testes after 6 weeks of long day. Thus, during transient exposure to short day, the animals acquired sensitivity to the stimulatory effects of long day. The responses of body mass, bifid claw width and pelage colour to the photoperiod manipulations did not parallel that of the gonads, indicating independent regulation of somatic and reproductive parameters. The unique way in which the reproductive system of collared lemmings responds to photoperiod may reflect evolution in an environment where the production of offspring during periods of unchanging long day (for example, the Arctic summer) is not selectively advantageous.