The oviduct is the site of fertilization, and factors present in the oviductal fluid appear to be crucial to the future success of conceptus development. The spatial and temporal localization of mRNA encoding components of the insulin-like growth factor (IGF) system (IGF-I, IGF-II, the type 1 IGF receptor, and IGF-binding proteins -2, -3 and -4) in the ovine oviduct were examined in tissue samples taken during the early and late stages of follicular development, and the early, mid-, and late luteal phases using in situ hybridization. Expression of mRNA encoding IGF-I showed a cyclical pattern, increasing sharply in the mucosa and muscularis during the late follicular phase (P < or = 0.001), then declining. In the muscularis, mRNA encoding IGF-II exhibited no temporal changes, but concentrations in the mucosa increased from the late follicular stage to the early luteal phase. mRNA encoding the type 1 IGF receptor was present throughout the oviduct. Concentrations increased during the follicular phase to peak in the early luteal phase in both the mucosa and muscularis (P < 0.001). IGFBP-2 gene transcripts were undetectable at all time points examined. mRNAs encoding IGFBP-3 and IGFBP-4 were localized primarily in the stromal region. IGFBP-3 expression peaked in the late follicular stage of the cycle P < or = 0.001). The concentration of mRNA encoding IGFBP-4 increased in the follicular phase and was maintained at a significantly higher concentration during the early and mid-luteal stages (P < 0.001). The co-ordinate maximum expression of mRNA for both IGF-I and IGF-II, the type 1 IGF receptor and IGFBP-3 during the period when the gametes and embryo are in transit suggests a role for IGF-I and possibly IGF-II peptides in providing an oviductal environment propitious to conception and early embryonic growth and metabolism.