Maternal effects and population regulation: maternal density‐induced reproduction suppression impairs offspring capacity in response to immediate environment in root voles Microtus oeconomus

Abstract

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.

Maternal density stress and coccidian parasitism: Synergistic effects on overwinter survival in root voles

“…FCM is primarily derived from plasma‐free CORT in rodents (Palme, Rettenbacher, Touma, El‐Bahr, & Möstl, ). Our previous study validated that measurement of the FCM level is a reliable method to assess the physiological state and stress level of root voles (Bian et al., ; He et al., ).…”

“…Specifically, we have found that high population density is associated with a significantly elevated stress response in both parents and offspring (Bian et al., ; Du et al., ). Density stress during the maternal phase significantly suppresses offspring reproduction function and decreases offspring body size at sexual maturity and the physiological condition in offspring under maternal stress (Bian et al., ). Similar to those characteristics that can be observed in other species (Nelson, Asfaw, DeVries, & Demas, ; Sinclair & Lochmiller, ), density stress in root voles is associated with an immune suppression and a prevalence of parasitic infection.…”

“…Our recent studies indicate that population density plays an important role in the regulation of the physiological conditions of root voles and their population dynamics (Bian et al., , ; Du, Cao, Nie, Wu, & Bian, ). Specifically, we have found that high population density is associated with a significantly elevated stress response in both parents and offspring (Bian et al., ; Du et al., ). Density stress during the maternal phase significantly suppresses offspring reproduction function and decreases offspring body size at sexual maturity and the physiological condition in offspring under maternal stress (Bian et al., ).…”

Error management theory and the adaptive significance of transgenerational maternal‐stress effects on offspring phenotype

“…The consequences of maternal stress have long been considered to be maladaptive in biomedical fields because offspring phenotypes that can occur in response to maternal stress (e.g., smaller size, slower growth, lower energetic demand, higher anxiety‐like behavior) are assumed to confer reduced fitness (Sheriff & Love, 2013). However, researchers have recently proposed that maternal stress can play adaptive roles across a wide variety of animal taxa if stress‐induced phenotypes better prepare offspring for a stressful postnatal environment in mammals (Bian et al., 2015; Dantzer et al., 2013; Sheriff, 2015; Sheriff, Krebs, & Boonstra, 2010), birds (Chin et al., 2009; Coslovsky & Richner, 2011; Love, Chin, Wynne‐Edwards, & Williams, 2005; Love & Williams, 2008), reptiles (Bestion, Clobert, & Cote, 2015; de Fraipont, Clobert, John‐Adler, & Meylan, 2000; Meylan & Clobert, 2005), and fish (Giesing, Suski, Warner, & Bell, 2011). Despite this recent progress, a unified framework that both explains the selective mechanisms and allows field‐testing of the adaptive role of maternal stress has yet to be proposed.…”

Prenatal predatory stress in a wild species of subterranean rodent: Do ecological stressors always have a negative effect on the offspring?

“…While these effects of prenatal stress in offspring have been extensively investigated in laboratory rats using usually conventional laboratory stressors (e.g., physical restraint, Maccari et al, ; electric foot shock, Estanislau & Morato, ; psychological stress, Abe et al, ; and psychosocial stress, Götz & Stefanki, ), comparatively fewer studies have involve wild species and ecologically relevant stressors (Sheriff et al, ). Examples of this last situation in rodents were carried out by Bian and colleagues (), who studied the effects of maternal population density on offspring physiology, reproduction and population dynamics in root voles ( M. oeconomus ), and Dantzer et al () who found that density‐induced maternal stress in red squirrels ( Tamiasciurus hudsonicus ) results in faster growing offspring through an adaptive hormone‐mediated maternal effect. Natural stressors, like the presence of a predator or cues indicative of its presence, which certainly represent an ecologically more relevant stimulus, are comparatively less used as stressors in experimental laboratory conditions.…”