Prenatal maternal stress effects in wild Assamese macaques (Macaca assamensis)Doctoral thesis
Date of Examination:2022-06-08
Date of issue:2022-11-22
Advisor:Dr. Oliver Schülke
Referee:Prof. Dr. Peter M. Kappeler
Referee:Prof. Dr. Julia Ostner
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EnglishAcross mammals, adverse conditions experienced during specific ontogenetic sensitive periods can have persisting effects on neurodevelopment, acquisition of cognitive and motoric skills, immune function, and systemic diseases. Non-genetic maternal effects are among the most pronounced and lasting environmental effects on individual health and fitness and from conception onwards, maternal adversity can affect offspring developmental trajectories depending on the degree of the adversity, the timing of challenges, and sex of the offspring. Thus, sometimes the adult’s health states are better explained by early adversity rather than by their interactions with the current environment. The effects induced by adversity during sensitive phases of ontogeny could be interpreted as the product of constraints during development or as adaptive responses to conditions of future life-phases. According to the internal predictive adaptive response (iPAR), early adversities induce developmental constraints which translate into disadvantaged somatic states and consequent reduction in life expectancy. However, the offspring is thought to recalibrate its life-history pace in an effort to counter the reduced life expectancy. The recalibration would accelerate growth and reproduction at the cost of quality-related attributes and lower investment in maintenance functions that normally enhance offspring’s health and thus longevity. Using data on a wild long-lived mammal species, I tested the internal consistency of the iPAR hypothesis, and competing hypotheses on developmental plasticity induced by epigenetic prenatal maternal stress. The lack of available long-term data on life-time reproductive success did not allow to test for the presence of fitness-crossovers, and thus I focused on the adaptive trade-offs. Crucially, the timing of the exposure confirmed the central factor within the debate on the persistence of maternal effects and the adaptive nature of developmental plasticity. Early-preGC (prenatal maternal GC levels during the first half of gestation) was a better predictor when compared with late-preGC (second half of gestation) and postGC (postanal phase during lactation). Across different statistical models and in all the studies, the results indicated that if experienced during early gestation, even moderate variation in maternal GC levels can lead to variation in offspring physiological phenotype without the need for catastrophic events. Elevated early-preGC were associated with: (i) an hyperactivation of the HPA axis activity, (ii) a reduced diversity of the gut microbiome community with increased relative abundance of potentially pro-inflammatory organisms and reduced SCFA-producers; (iii) lower Firmicutes to Bacteroidota ratio; (iii) accelerated body growth and increased body-size index. Importantly, the variation in all these traits persisted into adulthood with strong indications against short-term effects, and in favor of persisting phenotypic variations in response to maternal GCs during early gestation. These findings suggest a higher allostatic load and “wear and tear” and gut-microbial dysbiotic states combined with accelerated growth. Overall, they indicate a trade-off in favor of an acceleration of the pace of life paid at the cost of reduced investment in maintenance functions and health in prenatally challenged individuals. Finally, the results confirmed previous findings on the trade-off between growth and immune response in immature wild Assamese macaques. They also indicate that such trade-offs are not limited to the first phases of life but are part of a long-term programmed life-history recalibration under the assumptions of the iPAR hypothesis.
Keywords: stress; prenatal; developmental; plasticity; gut microbiome; growth; glucocorticoids; primates; health; disease; prenatal stress