Offspring size and performance in invertebrates often decrease with maternal age or as a response to seasonal environment. In viviparous ectoparasites maternal provision may wholly determine offspring performance outside the host. The viviparous deer ked (Lipoptena cervi), an ectoparasite of cervids, breeds from autumn to spring. We reared deer ked pupae through the reproductive period to investigate whether offspring size and performance vary according to maternal age and offspring environment. We expected that, in autumn, young females would produce the largest offspring to ensure that early-born pupae would survive a long period of winter diapause, and that offspring size would decrease with maternal age and decreasing diapause length. Diapause was associated with a significant weight loss, which reduced survival through post-diapause development. It was thus surprising that the early-born offspring were the smallest, and that size and survival (eventually) increased towards the spring. The variability among offspring in the length of off-host period seems to be an important component of life-history evolution in this ectoparasite, and should be studied further. Unexpected seasonal variation in the offspring size of this blood-feeding ectoparasite may result from changes in female resources due to weakening host condition as the winter progresses.

Off-host stages of temperate parasites must cope with low temperatures. Cold tolerance is often highest in winter, as a result of diapause and cold acclimation, and low during the active summer stages. In some blood-feeding ectoparasites, offspring provisioning determines cold tolerance through all the non-feeding, off-host stages. Large size increases survival in the cold, but so far seasonal variation in within-female offspring size has not been associated with offspring cold tolerance. The deer ked (Lipoptena cervi) reproduces on cervids from autumn to spring. Newborn pupae drop off the host, facing frosts without any acclimation. We examined cold tolerance through 4 seasons and from birth to adulthood by means of short- and long-term frost exposure. We expected females to produce more tolerant offspring in winter than in spring. Large spring pupae survived prolonged frosts better than did small winter pupae. Thus more tolerant offspring were not produced when the temperature outside the host is at its lowest. Unexpectedly, the freezing points were −20°C or below all year round. We showed that high cold tolerance is possible without acclimation regardless of life stage, which presumably correlates with other survival characteristics, such as the starvation resistance of free-living ectoparasites.