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This article has been accepted for publication and undergone full peer review but has not been 
through the copyediting, typesetting, pagination and proofreading process, which may lead to 
differences between this version and the Version of Record. Please cite this article as doi: 
10.1111/1365-2656.13039 
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Journal of Animal Ecology 
 
 JOANNES  VAN CANN (Orcid ID : 0000-0002-1394-804X) 
 
Article type      : Research Article 
 
Handling Editor: Celine Teplitsky 
 
ToC Category: Evolutionary Ecology 
 
TITLE: Intergenerational fitness effects of the early life environment in a wild rodent 
 
AUTHORS: Joannes Van Cann1*, Esa Koskela1, Tapio Mappes1, Angela Sims1, Phillip C. Watts1,2 
 
Authors after the first author are listed in alphabetical order 
 
1 Department of Biological and Environmental Science, University of Jyväskylä, FI-40014 Jyväskylä, 
Finland 
2 Ecology and Genetics, University of Oulu, FI-90014, Oulu, Finland 
*email: joannes.j.vancann@jyu.fi 
JOURNAL: Journal of Animal Ecology 
 
 
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Summary 
1. The early life environment can have profound, long-lasting effects on an individual’s fitness. For 
example, early life quality might (1) positively associate with fitness (a silver spoon effect), (2) 
stimulate a predictive adaptive response (by adjusting the phenotype to the quality of the 
environment to maximize fitness) or (3) be obscured by subsequent plasticity. Potentially, the 
effects of the early life environment can persist beyond one generation, though the 
intergenerational plasticity on fitness traits of a subsequent generation is unclear. 
2. To study both intra- and inter-generational effects of the early life environment, we exposed a 
first generation of bank voles to two early life stimuli (variation in food and social environment) in 
a controlled environment. To assess possible intra-generational effects, the reproductive success 
of female individuals was investigated by placing them in large outdoor enclosures in two 
different, ecologically relevant environments (population densities). 
3. Resulting offspring were raised in the same population densities where they were conceived 
and their growth was recorded. When adult, half of the offspring were transferred to opposite 
population densities to evaluate their winter survival, a crucial fitness trait for bank voles. 
4. Our setup allowed us to assess: (1) do early life population density cues elicit an intra-
generational adaptive response i.e. a higher reproductive success when the density matches the 
early life cues and (2) can early life stimuli of one generation elicit an intergenerational adaptive 
response in their offspring i.e. a higher growth and winter survival when the density matches the 
early life cues of their mother. 
5. Our results show that the early life environment directly affects the phenotype and 
reproductive success of the focal generation, but adaptive responses are only evident in the 
offspring. Growth of the offspring is maintained only when the environment matches their 
mother’s early life environment. Furthermore, winter survival of offspring also tended to be 
higher in high population densities if their mothers experienced an competitive early life. These 
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results show that the early life environment can contribute to maintain high fitness in challenging 
environments, but not necessarily in the generation experiencing the early life cues. 
 
KEYWORDS: early life, intergenerational plasticity, maternal effect, population density, predictive 
adaptive response, protein restriction, silver spoon, social environment 
 
INTRODUCTION 
Many organisms adjust their phenotype in response to environmental stimuli (Burton & Metcalfe, 
2014; Nettle, Frankenhuis, & Rickard, 2013; Paaby & Testa, 2018). The early life environment is of 
particular importance as it can have a profound, and often irreversible, impact upon the phenotype 
(Burton & Metcalfe, 2014). A high quality early life environment can elicit high adult fitness – the so 
called ‘silver spoon effect’ (Grafen, 1988; Monaghan, 2008) or ‘condition transfer’ (Bonduriansky & 
Crean, 2018) which appears to be a common phenomenon in animals (Cartwright, Nicoll, Jones, 
Tatayah, & Norris, 2014; Lindström, 1999; Wong & Kölliker, 2014). Alternatively, either a high or a 
low quality early life environment might stimulate a certain phenotypic trajectory that maximizes 
the fitness in a matching (i.e. high or low quality) environment – a ‘predictive adaptive response’ 
(Duckworth, Belloni, & Anderson, 2015; Galloway & Etterson, 2007; Gluckman, Hanson, & Spencer, 
2005). For example, in the marine polychaete Ophryotrocha labronica, maternal temperature during 
oogenesis can lead to increased temperature tolerance when the offspring are reared in a similar 
(‘matching’) environment (i.e. an environment with thermal variation; Massamba-N’Siala, Prevedelli, 
& Simonini, 2014). The evolutionary benefits of a predictive adaptive response are unclear when the 
future environment is not predictable, as the early life environment can stimulate a phenotype that 
performs poorly in later conditions (Bateson, Gluckman, & Hanson, 2014; Vickers et al., 2000).  
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Traditionally the focus of early life effects has been on within-generational plastic responses  
because considering the length of time between the environmental cue and the expressed 
phenotype, the effects might be expected to be more apparent within (F1 early environment 
affecting F1 fitness) than between generations (F1 early environment affecting F2 fitness) (Burton & 
Metcalfe, 2014). Indeed, laboratory studies on rodents (Bateson et al., 2014; Vickers et al., 2000) and 
insects (Raveh, Vogt, & Kölliker, 2016; Vijendravarma, Narasimha, & Kawecki, 2010) show how the 
similarity in nutritional environment during early (development) and late (mature) life (i.e. occurring 
within one generation) determines the fitness of phenotype. With this in mind, it is intriguing that 
the phenotypic consequences of an F1 individual’s early life environment can persist to the next 
generation (F2) (Burton & Metcalfe, 2014; Donelson, Salinas, Munday, & Shama, 2018; Donohue, 
1999), as depending on environmental autocorrelation, intergenerational effects can either limit or 
enhance the ability of an individual to express the optimal phenotype (Guillaume, Monro, & 
Marshall, 2016; Heckwolf, Meyer, Döring, Eizaguirre, & Reusch, 2018). Of course, the F2 adult 
phenotype might be plastic (Ergon, Lambin, & Stenseth, 2001; Piersma & Drent, 2003) (i.e. able to 
reversibly change the phenotype based on immediate environmental cues) and capable of mitigating 
the consequences of the early life environment (Beaman, White, & Seebacher, 2016). The processes 
that impact phenotype have obvious eco-evolutionary relevance and yet it has proved difficult to 
quantify their relative impact in natural populations (Monaghan, 2008). The challenge in identifying 
the eco-evolutionary relevance of the early life environment (Mousseau & Fox, 1998) on subsequent 
generations lies in assessing the fitness consequences, which in turn depend on the degree of 
environmental variation.  
Numerous examples exist of F1 early life exposure resulting in intergenerational F2 responses. For 
example, F1 early life ambient temperature for certain fish species (Acanthochromis polyacanthus 
Donelson, Munday, McCormick, & Pitcher, 2012; Gasterosteus aculeatus Shama & Wegner, 2014; 
Shama et al., 2016) and lizards (Lacerta vivipara Marquis, Massot, & Le Galliard, 2008) can lead to 
changes in offspring body size. Evidence in mammals for intergenerational phenotypic effects of F1 
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early life environment on F2 is derived largely from biomedical studies of humans (Gluckman et al., 
2005) and laboratory rodents (Bateson et al., 2014), whereby conditions experienced during 
pregnancy can impact the birth characteristics and health of both the focal generation (F1) and the 
next generation (F2) (Lumey & Stein, 1997; Painter et al., 2008; Rickard et al., 2012). 
Intergenerational effects may occur through several different pathways, such as differential parental 
investment into F2 offspring and/or by direct environmental influence on the F2 through epigenetic 
processes that occur during prenatal or early life (Burton & Metcalfe, 2014). Despite unambiguous 
evidence of intergenerational early life effects in humans and laboratory animal models, it is unclear 
whether intergenerational effects have fitness consequences in natural settings (Sheriff & Love, 
2013) and the extent to which any (mal)adaptive effects are mediated in different ecological 
circumstances. For example, intergenerational phenotypic effects could allow populations to cope 
with climate change (Donelson et al., 2018) by facilitating individuals to rapid changes in 
temperature and precipitation (e.g. Marquis et al., 2008; Shama & Wegner, 2014). 
The bank vole Myodes glareolus has several life-history traits that make it an ideal species to study 
the within- and between-generation consequences of the early life environment through the 
maternal line: females are promiscuous, males do not display paternal care, and females are 
territorial during the breeding season (Gromov & Osadchuk, 2013). The maternal environment is 
therefore presumed to be the main contributor to the early life environment of the next generation 
(but see Vaiserman, Koliada, & Jirtle, 2017; Weyrich et al., 2016 for potential environmental paternal 
effects in other study systems). Furthermore, varying (early life) environments are relevant to bank 
voles as natural populations typically undergo cyclic fluctuations in density (Kallio et al., 2009; 
Korpela et al., 2013; Korpimaki et al., 2005; Prévot-Julliard, Henttonen, Yoccoz, & Stenseth, 1999). As 
a consequence, density-related factors, such as nutritional quality (Helle, Koskela, & Mappes, 2012) 
and population density itself (Prévot-Julliard et al., 1999) impact several life-history traits including 
maturation, reproductive success and susceptibility to the costs of reproduction (Koskela, Jonsson, 
Hartikainen, & Mappes, 1998; Mappes et al., 2008; S. C. Mills et al., 2007; Prévot-Julliard et al., 
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1999). Some life-history traits follow a delayed density pattern and a predictive adaptive response 
has previously been hypothesized to be partly responsible (Oksanen, Koivula, Koskela, Mappes, & 
Soulsbury, 2012). An important aspect of the bank vole’s life cycle is the overwintering survival 
where populations can easily decrease by 50% during winter (Kallio et al., 2009). For voles born 
during the summer the first mating opportunity is after the winter, making winter survival a key 
fitness trait. Intra-generationally, it has been shown that bank voles born in a certain density have a 
higher winter survival if the adult winter density matches that early life density (Oksanen et al., 
2012). So far, no efforts have been made to investigate potential intergenerational effects of the 
early life density. In theory, intergenerational effects that ‘prepare’ offspring for an increasing 
population density could be beneficial for bank voles due to the cyclicity of the population 
fluctuations.  
Our aim was to quantify the role of the early life environment in mediating fitness traits in natural 
conditions both within and between generations and in different environments. We predict that (1) 
if early life environmental cues have a silver spoon effect (Grafen, 1988; Monaghan, 2008), then a 
low quality early life reduces adult fitness independent of the adult environmental quality; (2) if 
early life cues elicit a predictive adaptive response (Gluckman et al., 2005), then a low quality early 
life leads to a lower adult fitness only if the adult environmental quality does not match the early life 
quality and (3) if the phenotype is plastic and can compensate for any effects of the early life 
environment, then our treatments will have little to no effect on adult fitness. To test these 
predictions, we varied the early life environment, which is the intra-uterine development and 
nursing period of female bank voles (termed F1), by exposing them to two population density-
related cues in a factorial setup in the laboratory (Fig. 1a). The chosen early life cues were (1) social 
confrontation, relevant to bank voles as gravid female bank voles fiercely defend their territories 
(Gromov & Osadchuk, 2013; Koskela, Juutistenaho, Mappes, & Oksanen, 2000; Koskela, Mappes, & 
Ylönen, 1997), and (2) variation in dietary protein, as the nutritional environment is related to 
population density (Brook & Bradshaw, 2006; Forbes et al., 2014; Tanner, 1966) and protein is an 
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important component of the bank vole diet (Hansson, 1971). To test the effects of the early life in 
either a matching or a non-matching adult environment, the F1 animals were released into 
experimental field-enclosures at two different population densities, where they freely competed and 
reproduced (Fig. 1b). Reproduction of F1 in the field produced a second generation (F2) whose 
growth and overwintering survival was quantified at different population densities, allowing us to 
test whether there was an intergenerational response (Fig. 1c). We quantified the phenotypes (i.e. 
fitness-related traits - growth, reproductive characteristics and survival) of the focal (F1) and second 
(F2) generations at both low and high population densities under a full factorial design (Fig. 1).  
METHODS 
Starting colony 
Three hundred and eighty two bank voles females (F0) (Table S1) were bred in spring of 2014 (first 
replicate) and 2015 (second replicate) from a random mix of first or second generation wild-caught 
animals that had been trapped in Central Finland (62°8379 N; 26°8209 E). All bank voles were kept in 
polyethylene cages (43x26x15 cm) and maintained on a 16L:8D photoperiod at 20±2°C, with wood 
shavings and hay provided as bedding. Water was provided ad libitum and prior to the experiment 
standard food (Labfor 36; Lactamin AB, Stockholm, Sweden) was provided ad libitum. Animals were 
chipped with electronic Trovan tags (EID Aalten BV, Aalten, Holland) for identification. 
Early life environment– laboratory manipulation 
All F0 females were randomly assigned to four groups in a two by two factorial design (Fig. 1; Table 
S1): (1) a control group (PR-SC-; Fig. 1), (2) a protein restricted group (PR+SC-), (3) a social 
confrontation group (PR-SC+) and (4) a group which received both protein restriction and social 
confrontation (PR+SC+). There were no significant differences in average body mass (one way 
ANOVA; F3,477=0.359; p=0.783) between groups. Mature males (from the laboratory stock, non-kin 
with the females) were randomly grouped with F0 females. 
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At the start of the breeding, F0 females receiving the PR- treatment received a control diet (18% 
protein; 3.1 kCal/g; Envigo, WI, USA) that has a similar protein content as found in the wild (Droždž, 
1968) while females from the PR+ treatment were given a restricted protein diet (9% protein; 3.2 
kCal/g; Envigo, WI, USA). After seven days, males were removed and females receiving the SC+ 
treatment started receiving social confrontation. Social confrontation consisted of confronting each 
female in a new, empty cage with another SC+ female every second day (Marchlewska-Koj, Kruczek, 
Kapusta, & Pochroń, 2003) for 10 minutes. New combinations of females were used every day to 
avoid habituation. A more detailed explanation of the social confrontation treatment can be found 
in the supplementary information. All treatments were carried out throughout the pregnancy and 
continued until the pups (F1) had weaned (20 days post-partum). Upon weaning, F1 individuals were 
transferred to separate cages per litter where they received water and standard food ad libitum 
(Labfor 36; Lactamin AB, Stockholm, Sweden). At the age of 30 days, litters were separated per sex 
until they were released to the field enclosures. 
Population density treatments – field experiments 
At the age of two months, i.e. the beginning of July 2014 or 2015 for individuals born in 2014 or 2015 
respectively, fitness of F1 females from all treatment groups was assessed by releasing them to field 
enclosures twice for approximately three weeks (Fig. 1b). F1 individuals mated and carried litters in 
the first three weeks and nursed their litters in the second three weeks. Twenty three enclosures 
(40m x 50m) were used, located in Central Finland (62°37'30"N 26°14'38"E and 62°39'23"N 
26°09'32"E; Fig. S2). Enclosures were fenced with 1.25m high galvanized sheet metal buried 0.5 m in 
the ground, which prevented immigration and emigration of bank voles but did not prevent 
predation by avian predators. Trapping was performed by placing 20 Ugglan live traps (Grahnab, 
Hillerstorp, Sweden) per enclosure, organized in a grid, baited with sunflower seeds and potato. 
Traps were not set and contained no food during any other period. Throughout the field 
experiments, individuals relied on natural resources for food and water.  
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Over two years, F1 females were released in enclosures in one of two population densities (termed 
‘population density 1’; PD1): (1) a low population density treatment, consisting of four female 
individuals (one from each early life treatment group), or (2) a high population density treatment, 
consisting of eight female individuals (two from each early life treatment group). Densities 
corresponded to the variation of natural bank vole populations over the multiannual density cycle 
(Rikalainen, Aspi, Galarza, Koskela, & Mappes, 2012; Yoccoz, Stenseth, Henttonen, & Prévot-Julliard, 
2001). In total, the two replicates consisted of nineteen low and twelve high density enclosures. 
After one day, experimentally naive males, previously caught from wild populations, were added to 
the enclosures to produce a 1:1 sex ratio, and all individuals were allowed to mate. Individuals were 
exhaustively trapped (individuals not caught were considered dead) and brought to the laboratory 
just before their parturitions, where they could give birth to the F2 generation (Fig. 1b).  
Intergenerational effect on F2 phenotype – field experiments 
After parturitions, F1 mothers and their new-born F2 litters were returned to the same densities as 
before. Releases were done by placing the cage in which the mother gave birth in the enclosure on 
its side, giving the mother opportunity to relocate her nest (after which the cages were removed). 
This method to trap late pregnant bank vole females to give birth in the lab and then promptly 
return them with their new-born pups back to the enclosures makes it possible to determine the 
phenotypes of new-born pups (Koskela, Juutistenaho, Mappes, & Oksanen, 2000; Oksanen, Koskela, 
& Mappes, 2002). New experimentally naïve males, not used for the experiment so far, were added 
after one day, in a 1:1 sex ratio. At weaning (ca. three weeks old), the F2 individuals were 
exhaustively trapped and brought to the laboratory where they were weighed and kept in standard 
cages until tested for winter survival. All F1 mothers and naïve males were also trapped and not 
used subsequently in the experiment.  
Intergenerational effects on F2 survival – winter survival 
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When F2 individuals were at least 50 days old their winter survival was assessed in outdoor 
enclosures in either low or high population densities (termed ‘population density 2’ (PD2); Fig. 1c). 
Half of the F2 individuals were designated to the density treatment by matching their early life 
density (PD1), and half were designated by not matching their early life density. This reciprocal 
transplant experiment meant that every F2 individual now had three factors for which their winter 
survival could be tested: (1) the intergenerational effects of the F1 early life (PR and/or SC), (2) the 
intra-generational effect of the density in which the F2 was conceived and raised (PD1) and (3) the 
direct effect of the density in which an individual resides during the winter (PD2). There were 10 low 
density populations consisting of 8 individuals (one female and one male F2 individual from each F1 
early life treatment group) and 5 high density populations with 16 individuals in each (two female 
and two male F2 individuals from each F1 early life treatment group). Enclosures never contained 
individuals from the same litter. The winter survival experiment began in October, when the 
temperature started dropping below zero (average temperature at day of release was 6°C), and 
long-term survival was determined by trapping all enclosures exhaustively in April, as the snow 
started melting and this means the onset of the next breeding season.  
 
Morphological measurements 
All body masses were measured using electronic scales. Body mass of F0 was measured at the start 
of the experiment, at the birth of F1 and at F1’s weaning age (20 days). F1 body mass was recorded 
at birth and as adults (30 days). F2 individuals’ body mass was recorded at the age of recapture (25 
days).  
 
 
Statistical analyses 
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Statistical analyses were performed using R v.3.4.2 (R Core Team, 2017). All analyses of body mass 
and the F2 winter survival (logit link) were performed using the package lme4 (Bates, Mächler, 
Bolker, & Walker, 2015), and p-values were calculated with the package lmerTest (Kuznetsova, 
Brockhoff, & Christensen, 2017) using Satterthwaite's method for approximating degrees of 
freedom. The litter size (number of offspring) that F1 produced in the field was analysed as a zero-
truncated Poisson generalized mixed model using glmmTMB (Brooks et al., 2017) (log link). Whether 
or not a F1 mother reproduced at all (“Reproduced”; binomial yes/no; logit link) was analysed using 
glmmTMB (Brooks et al., 2017). All model selections began with a full model that had stepwise 
reduction until the model with the lowest AIC was achieved, after which the model fit was 
examined. The F1 early life treatments, PR and SC, and their interaction term (PR x SC) were 
purposely retained during model selection. For the F1 enclosure experiments, density (PD1) was 
always included as a fixed factor in the model. For the analysis of F2 winter survival, the full model 
included the F2 winter density (PD2), as well as the F2 summer density (PD1), in which the F2 were 
conceived and raised, as fixed factors (in addition to PR, SC and PR x SC). For all analyses, sex 
(Koivula, Koskela, Mappes, & Oksanen, 2003; Koskela, Mappes, Niskanen, & Rutkowska, 2009; 
Schulte-Hostedde, 2007) and the litter size the individual was born in (Koivula et al., 2003; Mappes & 
Koskela, 2004; Oksanen et al., 2002; Schroderus et al., 2012) were included as covariates in the full 
model. As individuals were born in different years and weeks, all F1 analyses included the ‘batch 
number’ as a random factor. F2 individuals were released in two groups during the first year and this 
was included as a random factor for the summer F2 analyses. All analyses also included ‘litter 
number’ as a random factor, which groups siblings to account for litter effects (either for F1 or F2 
individuals). All field enclosure analyses included ‘enclosure number’ as a random factor, which 
accounts for local differences between the enclosures. Random factors were always included in the 
initial full model and retained during model selection. Standard deviations of all included random 
factors are reported in the supplementary tables (Tables S4, S5 and S6). 
RESULTS 
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Early Life Environment  
Both the social confrontation and protein restriction treatments affected the phenotype of F1 
individuals (Table 1). In total, 643 F1 individuals (Table S2) were born to 158 F0 mothers. A restricted 
protein diet significantly lowered both the F1 birthmass (mean±SD(g), PR-: 1.90±0.23; PR+: 
1.83±0.22) as well as the F1 adult body mass (mean±SD(g), PR-: 16.71±2.21; PR+: 16.11±2.48) 
compared with the control group (Fig. S1). F1 individuals receiving the SC treatment had a 
significantly lower adult body mass (mean±SD(g), SC-:16.57±2.51; SC+:16.21±2.21), while not having 
a significantly different body mass at birth (mean±SD(g), SC-:1.85±0.23; SC+:1.88±0.23), compared 
with the control group. The final model did not reveal a significant interaction of the PR and SC 
treatment indicating that their effects were independent of each other (Tables 1 and S3). 
 
F1 reproductive success  
Neither a restricted protein or social confrontation early environment had a significant influence on 
the reproductive success of F1 females in the field (Tables 1 and S4). Only PD1 density had a 
significant effect on the probability of breeding with high density populations significantly lowering 
the chance of reproduction. 88% of all F1 females originally released survived during the six weeks in 
the field enclosures (no difference in survival between treatments: one way ANOVA; F3,168=0.407; 
p=0.748), of which 105 (68%) were gravid. 
 
Intergenerational effects on F2 phenotype 
A high population density had a negative effect on the adult body mass of the F2 individuals if the 
mother did not receive the SC treatment (SC-; low density: mean±SD(g)=12.57±1.08; SC-; high 
density: mean±SD(g)=11.12±1.98; Tables 2 and S5; Fig. 2a), but if the mother did receive the SC 
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treatment, this negative effect associated with a high population density disappeared (SC+; low 
density: mean±SD(g)=12.41±1.33; SC+; high density: mean±SD(g)=12.06±1.53). Hence, if the mother 
received a high density related cue during her early life (i.e. social confrontation), her offspring were 
not affected by a high population density. Litter size in which the F2 individual was born had a 
significant negative correlation with the F2 body mass which is common in bank voles (Mappes & 
Koskela, 2004; Schroderus et al., 2012) (Table S5). 
 
Intergenerational effects on F2 survival 
F2 Individuals in high population densities had a lower winter survival, but this was somewhat 
countered if their mothers had received social confrontation during their early life. Of the 160 F2 
individuals that went to the enclosures in October, 37 survived (23%) until the start of the next 
breeding season in April (and no unknown immigrants were captured). The density in which the F2 
were conceived and raised (PD1) had no significant effect on winter survival (Tables 2 and S6). 
However, the early life treatment of their F1 mothers had a near statistically significant (p=0.0537) 
interaction effect with density on the winter survival (PD2) (Tables 2 and S6; Fig. 2b) indicating that 
effects of the maternal early life persisted to the F2 generation and provided a fitness benefit if the 
winter environment matched that of the maternal early life environment. Neither the restricted 
protein treatment, nor its interaction with SC, presented a statistically detectable effect upon F2 
winter survival. 
  
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Table 1: Phenotypic and reproductive characteristics of F1 individuals in relation to manipulation of 
early life environment and population density (PD1). Reduced table of body mass of F1 individuals at 
birth (n=643) and at 30 days old (n=565) in the laboratory and F1 reproductive success (littersize and 
reproduced (n=172)) in the field enclosures. PR= protein restriction; SC= social confrontation; PD1= 
population density in which F1 females reproduced; HD= high population density. Note that 
estimated values for reproduced represent the probability of not breeding. Bold p-values indicate p 
< 0.05. Est is estimated value; Std error is standard error; x indicates interaction between variables. 
Full results including random effects are provided in tables S3 and S4.   
 
  
Est Std error DF t value p 
F1 mass at birth PR (+) -0.1124 0.0394 144 -2.8540 0.0050 
 
SC (+) -0.0213 0.0404 143 -0.5280 0.5982 
 
PR x SC 0.0601 0.0551 145 1.0900 0.2774 
F1 mass at 30d PR (+) -1.0768 0.4024 137 -2.6760 0.0084 
 
SC (+) -0.8706 0.4157 136 -2.0940 0.0381 
 
PR x SC 0.6812 0.5623 138 1.2110 0.2278 
Reproduced PR (+) -0.6638 0.4752 
 
-1.3970 0.1624 
 
SC (+) -0.2307 0.4657 
 
-0.4950 0.6204 
 
PD1 (HD) 0.9005 0.3794 
 
2.3740 0.0176 
 
PR x SC -0.0093 0.6781 
 
-0.0140 0.9891 
Litter size PR (+) -0.1002 0.1195 
 
-0.8390 0.4016 
 
SC (+) -0.2177 0.1288 
 
-1.6910 0.0909 
 
PD1 (HD) -0.1013 0.0856 
 
-1.1830 0.2369 
 
PR x SC 0.2147 0.1716 
 
1.2510 0.2109 
  
Table 2: Adult body mass and winter survival of F2 individuals in relation to: early life treatments of 
their F1 mothers (PR and/or SC), their own early life (PD1) population density and their adult/winter 
(PD2) population density. Reduced results of 25 day body mass (n=414) and winter survival (n=160). 
PR= protein restriction; SC= social confrontation; PD1= population density in which the F2 individuals 
were raised; PD2= population density during winter survival; HD= high population density; Lsize= size 
of litter in which the F2 individual was born. Bold p-values indicate p < 0,05. Est is estimated value; 
Std error is standard error; x indicates interaction between variables. Full results including random 
effects are provided in tables S5 and S6. 
 
 
 
Est Std error DF t value p 
F2 Mass at 25 days PR (+) -0.2998 0.3459 75 -0.8670 0.3888 
 
SC (+) -0.9242 0.8082 75 -1.1440 0.2564 
 
PD1 (HD) -1.7794 0.4303 59 -4.1350 0.0001 
 
Lsize -0.4591 0.1139 94 -4.0310 0.0001 
 
PR x SC -0.1284 0.4970 77 -0.2580 0.7969 
 
PD1 x SC 1.0753 0.5085 77 2.1150 0.0377 
F2 Winter survival PR (+) 0.1178 0.6447 
 
0.183 0.8551 
 
SC (+) 0.3216 0.6691 
 
0.481 0.6307 
 
PR x SC -0.6692 0.8195 
 
-0.817 0.4141 
 
PD2 (HD) -1.3193 0.8055 
 
-1.638 0.1014 
 
SC x PD2 1.7024 0.8824 
 
1.929 0.0537 
 
  
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Fig. 1: Overview and summary of the experimental design to investigate the effects of population 
density related cues during the early life environment (ELE) of F1 on the morphology and 
reproductive success of F1, as well as the intergenerational effects on the phenotype and winter 
survival of F2. a) early life treatments (protein restriction (PR) and/or social confrontation (SC) in a 
factorial setup) are presented to the F1 individuals during the intra-uterine development and nursing 
period. b) The (adaptive) response is tested by placing the female F1 in natural outdoor enclosures in 
different population densities (low/high population density; blank square is population density that 
matches the ELE and shaded square is population density that does not match the ELE). c) Winter 
survival of F2 offspring is tested in a reciprocal transplant experiment where the population density 
(low/high population density; PD2) matches or does not match the population density in which the 
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F2 individual was born (blank square represents a PD2 that matches the PD1 and shaded square 
represent a PD2 that does not match the PD1). The setup allows winter survival of F2 to be tested 
for: the population density during the winter (PD2; (c)), the population density in which the F2 was 
born and grew up in (PD1; (b)), and the intergenerational effects of the maternal F1 ELE (a). 
Uncoloured voles indicate F0 individuals; orange colour indicates F1 as pups and adults; purple 
indicates F2 as egg cells, pups and adults. 
  
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Fig. 2: Variation in F2 bank vole fitness traits (adult body mass and survival) whose maternal early life 
environment either had frequent social confrontation or not, competing in different population 
densities during the summer (PD1) and winter (PD2). a) 25 day old body mass of 414 F2 individuals 
(111 SC- and 121 SC+ in low density; 91 SC- and 91 SC+ in high density) in the field during the 
summer; b) winter survival percentage of 160 F2 individuals (40 SC- and 40 SC+ in low density of 
which 10 SC- and 10 SC+ survived; 35 SC- and 45 SC+ in high density of which 3 SC- and 14 SC+ 
survived). Diamond shaped black dots represent the average value for SC- F2 individuals. Triangular 
shaped grey dots represent average value for SC+ F2 individuals.  
  
8.70 
9.28 
9.85 
10.43 
11.00 
Low Density (PD1) High Density (PD1) 
B
o
d
y 
m
as
s 
(i
n
 g
±S
E)
 
0% 
13% 
25% 
38% 
50% 
Low Density (PD2) High Density (PD2) 
Su
ri
vi
va
l r
at
e
 (
±S
E)
 
SC- 
SC+ 
a) b) 
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DISCUSSION  
The early life environment, defined here as the period between fertilization and weaning, can have a 
profound influence on the adult phenotype and thus impact fitness in different ways. For example, 
the quality of the early life environment may associate with fitness (silver spoon effect) or an 
individual’s fitness might be conditional upon the match in the environment experienced during 
early and late life (predictive adaptive response) or even a combination of both silver spoon effects 
and a predictive adaptive response (Bonduriansky & Crean, 2018). What is unclear, however, is the 
extent to which the early life experienced by the target individuals (i.e. first generation) (Burton & 
Metcalfe, 2014) can have intergenerational effects on the fitness of the next generation and 
whether these effects can be adaptive or not (Monaghan, 2008; Nussey, Wilson, & Brommer, 2007). 
This is especially important as we try and predict animal population response under climate change 
and extreme weather events (Donelson et al., 2018; Ghalambor, McKay, Carroll, & Reznick, 2007; 
Yeh & Price, 2004). By manipulating dietary protein and social confrontation during the early life of 
female bank voles we show that (1) maternal early life effects can persist to the subsequent 
generation (F2) where it influences adult body mass in an adaptive manner; moreover (2) winter 
survival of the F2 offspring tends to depend on the maternal early life environment (F1), rather than 
its own early life environment.  
Social confrontation was exerted on pregnant bank voles during the period that wild female bank 
voles would be most likely to aggressively defend their territory. The effects of social confrontation 
on body mass were similar to a previous study in bank voles (Marchlewska-Koj et al., 2003), but did 
not have any effects on the reproductive success. Social confrontation during early life also had a 
notable intergenerational phenotypic effect on the F2 that persisted to the adult stage. F2 
individuals were captured from the field not long after they are old enough to be independent from 
the mother, hence their body mass is largely dependent on the feeding of the mother. The ability of 
F2 to cope with the high population density could therefore be due to increased maternal care, 
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signifying that there would be a predictive adaptive response (Nettle et al., 2013) in the F1 maternal 
behaviour, although further investigation is needed to confirm this.   
Social confrontation during the early life of the F1 generation had a nearly statistically significant 
positive effect (p = 0.0537) on the F2 winter survival, indicating a predictive adaptive response in F2 
winter survival. In contrast, the early life environment of the F2 (i.e. PD1 density) had little effect on 
winter survival, implying that the maternal early life environment is of greater importance for the F2 
winter survival than the F2 individuals’ own early life environment. Two mechanisms could be 
mediating this effect (Burton & Metcalfe, 2014): (1) F1 mothers from the SC+ treatment changed 
some aspect of their parental care, leading to a higher survival rate of their offspring or (2) SC+ 
during the early life of F1 had in utero effects on the F2 egg cells. An example of the second 
possibility occurs in laboratory rats where in utero exposure to social stress has been linked to lower 
mass at birth and subsequent cardiometabolic diseases (Drake & Walker, 2004). While it might be 
intuitive to argue that the difference in F2 body mass relates to their winter survival, and hence 
maternal care would be the most likely mechanism, body mass in bank voles is not always related to 
winter survival (Helle et al., 2012). The specific mechanism by which the F2 survival is increased 
could due to selective predation, e.g. Tengmalm's owls (Aegolius funereus funereus) have been 
shown to prefer lighter prey that are in good condition (Koivunen, Korpimäki, Hakkarainen, & 
Norrdahl, 1996). Differences in physiology e.g. metabolic rate (Boratyński & Koteja, 2009) might also 
contribute to the difference in survival rate.  
It is important to note that, while SC+ F2 individuals had higher survival in the high density 
environment (i.e. a matching environment) compared to SC- individuals, SC+ individuals did not have 
a lower survival in the low density environment (i.e. a mismatching environment) compared to SC- 
individuals (Fig. 2b). This response is not fully in line with a predictive adaptive response (sensu 
Gluckman et al., 2005) and perhaps indicates a co-occurrence of more than one type of response 
(Bonduriansky & Crean, 2018). It is possible that the SC+ individuals were able to plastically adapt to 
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the less competitive, low density environment; while the SC- individuals were not able to plastically 
adapt to the more competitive, high density environment. Alternatively, it is possible that the costs 
of living in a mismatched low density environment were too small to be detected, at least in the 
variables measured in this study. 
Body size in female bank voles is positively correlated to fitness-related traits such as a faster onset 
and higher probability of breeding (Mappes & Koskela, 2004; Mappes, Ylonen, & Viitala, 1995). 
Additionally, dietary protein content has a major impact on mammalian phenotypes, such as mass at 
birth (Zambrano et al., 2005), hypertension (Harrison & Langley-Evans, 2009), and epigenetic 
patterns (Burdge et al., 2007; Lillycrop, Phillips, Jackson, Hanson, & Burdge, 2005). Changes in 
epigenetic patterns could potentially lead to intergenerational effects (Bonduriansky & Day, 2009; 
Burton & Metcalfe, 2014; Heard & Martienssen, 2014; Skvortsova, Iovino, & Bogdanovi, 2018; 
Youngson & Whitelaw, 2008). In our study, protein restriction during the early life of bank voles 
elicited negative effects on F1 body size both as new-borns and as adults. However, we did not find 
any impact on the reproductive success in F1 and no detectable impact on the F2 adult phenotype or 
overwintering survival probability. This is in contrast with laboratory rats (Pinheiro, Salvucci, Aguila, 
& Mandarim-de-Lacerda, 2008), where protein restriction increased F2’s mass at birth and 
decreased male F2 adult body mass. While we did not find intergenerational effects due to protein 
restriction, we might have overlooked other phenotypic traits, such as pathogen susceptibility 
(Monaghan, 2008), which can affect fitness-related traits in F2 besides winter survival, e.g. 
reproduction (Hakkarainen et al., 2007; Kallio, Helle, Koskela, Mappes, & Vapalahti, 2015; J. N. Mills, 
2006). We propose that a protein restricted early life impacts bank vole phenotype, but it is of little 
consequence to fitness in natural settings.  As such, protein restriction cannot be considered to have 
a ‘silver spoon effect’, at least not for the fitness traits measured here. 
 
 
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Conclusion 
High population density related cues experienced during the early life environment influence the 
phenotype of both the generation that experiences it (F1), and their offspring (F2). Social 
confrontation during the early life of the F1 individuals caused a predictive adaptive response that 
enabled their offspring to better compete (i.e. grow and survive) in a high population density. That 
the juvenile environment of F2 was less important for winter survival than the prenatal/early life 
environment of their F1 mothers, underlines the eco-evolutionary importance of intergenerational 
effects. Protein restriction during the early life of F1 had a negative effect on the body mass, but 
otherwise did not lead to a silver spoon effect or a predictive adaptive response. Protein restriction 
might affect other fitness-related traits or its impact can be overcome later in life via plasticity. This 
study provides clear evidence of the maternal early life environment having direct adaptive 
influences on the phenotype and fitness of the subsequent generation in an ecologically relevant 
setting of intraspecific competition at different population densities.  
 
ACKNOWLEDGEMENTS 
We would like to thank the animal care staff at the University of Jyväskylä and at the Konnevesi 
research station. This work was supported by the Academy of Finland and the University of Jyväskylä 
Graduate School. Use of study animals followed the ethical guidelines for animal research in Finland 
and all institutional guidelines and was conducted under permissions from the National Animal 
Experiment Board (ESAVI/7256/04.10.07/2014). The authors declare no conflict of interest.  
AUTHORS CONTRIBUTION 
J.V.C., E.K., T.M., A.S and P.W. designed the research and wrote the paper. J.V.C., E.K., T.M. and A.S 
performed the research and analysed the data. 
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DATA ACCESSIBILITY 
The datasets generated during and analysed during the current study are available in the Zenodo 
repository via the link https://doi.org/10.5281/zenodo.1040834 (Van Cann et al., 2019). 
 
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