Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy

Abstract

Maternal experience before and during pregnancy is known to play a key role in offspring development. However, the influence of social cues about disease in the maternal environment has not been explored. We indirectly exposed pregnant mice to infected neighbours by housing them next to non-contagious conspecifics infected with Babesia microti. We examined the effect of this indirect immunological exposure on both the females and their adult offspring. Exposed females had higher levels of serum corticosterone and increased kidney growth compared with those with uninfected neighbours. These exposed females subsequently produced offspring that as adults showed an accelerated immune response to B. microti and less aggression in social groups. We suggest that ambient information regarding disease is used adaptively to maximize offspring survival and reproductive success in a challenging environment. Our results shed light on the impact of social information and maternal effects on life histories, and have important consequences for our understanding of epidemiology and individual disease susceptibility in humans and other animals. They also lead us to question the suitability of some laboratory housing conditions during experimental procedures, which may impact negatively upon both animal welfare and the validity of animal science.

Infection before pregnancy affects immunity and response to social challenge in the next generation

“…The results support the findings of our previously reported study [51] in which females were indirectly exposed to infection by co-housing with non-contagious conspecifics.…”

“…While our findings do not perfectly mimic those found following an indirect challenge by co-housing pregnant females with infected neighbours [51], consistent trends have emerged. In both cases, maternal exposure led to physiological changes in the female, which ultimately filtered down, affecting the responses of offspring to social challenge (either behaviourally or physiologically) and to infection.…”

“…In our experiment, following clearance of infection (time to clearance was less than or equal to 14 days (see [51])), each female was co-housed with a sire male for 6 days. Mated females were then removed to single-housing cages until parturition.…”

“…An important possible source of indirect information about infection risk in the environment comes from visual or olfactory cues associated with infected conspecifics [50]. In a previous experiment [51], we examined whether such indirect cues, when perceived by mothers, actually impact on offspring phenotype. We showed that housing pregnant female mice next to infected neighbours led to the production of offspring that were more resistant to disease and less aggressive as adults.…”

Proactive strategies to avoid infectious disease

“…The closest level of interaction occurs with transgenerational immune priming [4]. Here, maternal exposure to a pathogen promotes immunocompetence in her offspring in at least three ways: (i) by the direct transfer of antibodies or immunoglobulins from mother to offspring; (ii) by alterations in maternal reproductive behaviour (e.g.…”