Intergenerational fitness effects of the early life environment in a wild rodent

Abstract

The early life environment can have profound, long‐lasting effects on an individual's fitness. For example, early life quality might (a) positively associate with fitness (a silver spoon effect), (b) stimulate a predictive adaptive response (by adjusting the phenotype to the quality of the environment to maximize fitness) or (c) 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. To study both intra‐ and intergenerational 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). 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. Our setup allowed us to assess: (a) do early life population density cues elicit an intra‐generational adaptive response, that is a higher reproductive success when the density matches the early life cues and (b) can early life stimuli of one generation elicit an intergenerational adaptive response in their offspring, that is a higher growth and winter survival when the density matches the early life cues of their mother. 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 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.

Early life of fathers affects offspring fitness in a wild rodent

“…() and one by Van Cann et al. (), had a similar setup but only the latter found a negative relation between maternal social stress and offspring body mass.…”

“…D. melanogaster ; Piper & Partridge, ), humans (Polberger, Axelsson, & Räihä, ), rodents in the laboratory (e.g. rats (Zambrano et al., ); bank voles (Van Cann et al., )) and rodents in nature (e.g. deer mice Peromyscus maniculatus borealis (McAdam & Millar, )).…”

“…Moreover, the early life environment experienced by one generation can continue to exert phenotypic effects in the subsequent generation through parental effects, even in the absence of exposure to further stimuli (Burton & Metcalfe, ; Soubry, Hoyo, Jirtle, & Murphy, ). Such intergenerational environmental effects, that is when an early life environment exhibited on one generation has some effect on a subsequent generation (Emanuel, ), are well documented in several taxa, such as fish (Shama & Wegner, ), birds (Naguib & Gil, ), rodents (Drake & Walker, ; Skinner et al., ; Van Cann, Koskela, Mappes, Sims, & Watts, ) and humans (Pembrey, Saffery, & Bygren, ; Pembrey et al., ). There is clear evidence of lasting, intergenerational phenotypic impacts derived from, for example, the nutritional environment (Drake & Walker, ; Harrison & Langley‐Evans, ), disease burden (Denham, ; Drake & Liu, ), social environment (Franklin et al., ) and exposure to pollutants (Soubry et al., ).…”

Two hundred and fifty-four metagenome-assembled bacterial genomes from the bank vole gut microbiota

“…Bank voles are common in forest habitats of central and northern Europe and parts of Asia 21 . Also, bank voles are used as a model species in evolutionary ecology research 22 , 23 , for example with selection lines created to examine effects of physiology and diet on gut microbiota 24 .…”

The relevance of a rodent cohort in the Consortium on Individual Development

“…This facilitates the investigation of heritable traits (see e.g. Clinton et al, 2014 ; Stead et al, 2006 ) and cross-generational effects in the face of varying rearing environments ( Langenhof and Komdeur, 2018 ; Van Cann et al, 2019 ; van Steenwyk et al, 2018 ). For all of these reasons, the Consortium on Individual Development (CID) decided to run a rodent cohort in parallel with the many human cohorts.…”