The hypothesis that maternal effects act as an adaptive bridge in translating maternal environments into offspring phenotypes, and thereby affecting population dynamics has not been studied in the well-controlled fields. In this study, the effects of maternal population density on offspring stress axis, reproduction and population dynamics were studied in root voles (Microtus oeconomus). Parental enclosures for breeding offspring were established by introducing six adults per sex into each of 4 (low density) and 30 adults per sex into each of another 4 (high density) enclosures. Live-trapping started 2 weeks after. Offspring captured at age of 20-30 days were removed to the laboratory, housed under laboratory conditions until puberty, and subsequently used to establish offspring populations in these same enclosures, after parental populations had been removed. [Correction added on 8 January 2015 after first online publication: '10-20 days' has been changed to '20-30 days.'] Offspring from each of the two parental sources were assigned into four enclosures with two for each of the two density treatments used in establishing parental populations (referred to as LL and LH for maternally unstressed offspring, assigned in low and high density, and HL and HH for maternally stressed offspring, assigned in low and high density). Faecal corticosterone metabolites (FCM) levels, offspring reproduction traits and population dynamics were tested following repeated live-trapping over two seasons. Differential fluctuations in population size were observed between maternally density-stressed and density-unstressed offspring. Populations in LL and LH groups changed significantly in responding to initial density and reached the similar levels at beginning of the second trapping season. Populations in HL and HH groups, however, were remained relatively steady, and in HL group, the low population size was sustained until end of experiment. Maternal density stress was associated with FCM elevations, reproduction suppression and body mass decrease at sexual maturity in offspring. The FCM elevations and reproduction suppression were independent of offspring population density and correlated with decreased offspring quality. These findings indicate that intrinsic state alterations induced by maternal stress impair offspring capacity in response to immediate environment, and these alterations are likely mediated by maternal stress system. The maladaptive reproduction suppression seen in HL group suggests intrinsic population density as one of ecological factors generating delayed density-dependent effects.

Individuals in poor physiological condition are known to be more susceptible to infection that, once it occurs, further deteriorates the individuals' conditions, making them even more susceptible to infection and leading to death. This vicious synergy between the host condition and infection has recently been proposed to be among the key factors determining the oscillation characteristics in natural populations. Field studies that directly test such a hypothesis, however, are currently scarce, and the physiological traits involved remain largely unclear. In this field study, we systematically examined the synergistic effects of maternal stress and coccidian parasitic interaction on the physiological conditions and overwinter survival of offspring in the root vole (Microtus oeconomus) via repeated live trapping and measurements of faecal corticosterone metabolite (FCM) levels and immunocompetence in captured animals. We found that maternal density stress significantly increased FCM levels and both the prevalence and intensity of coccidian infection in offspring, significantly suppressed offspring immunocompetence and reduced offspring overwinter survival. Coccidian infection significantly potentiated increases in FCM levels and exacerbated the immune suppression induced by maternal density stress. Coccidian infection also significantly accelerated a decrease in overwinter survival and a population decline in maternal‐density‐stressed populations. Our findings indicate that both stress and immune systems are involved in the synergistic process through which stressors and parasites interact with the host to influence the fitness of individuals and cause a population decline in the natural environment. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13129/suppinfo is available for this article.