Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: An evolutionary perspective
Highlights
► Prenatal stress tends to increase both anxiety and stress responses in females. ► It tends to reduce stress responses and may increase ADHD in males. ► We suggest there may be evolutionary reasons for these differences. ► Females, with children, may benefit from vigilance in a more stressful environment. ► Males may benefit from less stress responsiveness and more ability to confront danger.
Introduction
It is well known that males and females tend to differ in their pattern of psychopathology [1]. Males are more likely to be aggressive and break rules, and to suffer from attention deficit hyperactivity disorder (ADHD) [2] or autism [3]. Females are more likely to experience anxiety and depression [4]. Many of the psychiatric disorders that are more prevalent in females have an etiological association with stress and hyperarousal, and there is evidence for sex differences in the molecular responses and brain circuitry that underlie this [5]. There is also evidence that males and females differ in their cortisol response to social stress [6].
Prenatal stress has been shown to increase the likelihood of the child and later adult suffering from a range of psychopathologies, and also to alter their stress responses. It can alter the sex ratio, with more females being born than males, as has been shown for example with prenatal exposure to infectious disease [7]. In this article we will briefly review findings on the effects of prenatal stress on behaviour, learning, and on stress responses, the sex differences in these effects, and then explore possible evolutionary reasons for these differences.
Section snippets
Animal evidence for the differential effects of prenatal stress on males and females
The association between prenatal stress and offspring outcome is best shown to be causal in animal models. With rat experiments, offspring from both prenatally stressed mothers and unstressed mothers can be cross fostered to new mothers on day one after birth and postnatal effects controlled for [8]. In monkeys both prenatally stressed and control offspring can be nursery reared together [9]. Animal experiments from many different laboratories, have shown that prenatal stress can increase
The effects of prenatal stress on child outcome
Prospective studies from several different laboratories around the world have shown that if the mother is stressed, anxious or depressed while pregnant her child is more likely to have symptoms of anxiety or depression, ADHD, conduct disorder, or reduced cognitive abilities [30], [31] and increased stress reactivity [32].The evidence for these associations is very strong. In some studies the associations have been found to be particularly with prenatal anxiety rather than depression e.g. [33],
Stress reactivity
Physiological stress responses can be determined by prenatal stress and other early life predictors such as low birth weight [50]. Smaller size at birth can be an index of an adverse fetal environment, and has many causes including prenatal stress e.g. [51]. It is of interest that low birth weight has been to be shown to be associated with later altered cardiovascular responses to stress, and in most studies these changes are sex specific [52]. In general low birth weight has been found to be
Sex specific differences in placental function
The mechanisms underlying the effects of prenatal stress are not yet understood, but alterations in the function of the placenta probably contribute [55]. The placental changes may allow greater passage of cortisol [56] or other factors such as 5-HT [57], to the fetus, and these may change neurodevelopment. In animal studies, prenatal stress has been shown to cause a down regulation of the cortisol metabolising enzyme 11β-hydroxysteroid dehydrogenase type II (11β-HSD2} [58] and we have evidence
Evolutionary perspectives on fetal adaptation, stress reactivity and psychopathology
According to the fetal origins hypothesis of adaptation and disease, programming of physiological systems by the intrauterine environment equips the fetus for anticipated conditions following birth, but increases risk of disorder if the extra-uterine environment is markedly different. This mismatch hypothesis has proved powerful in the investigation of medical disorders where long term effects of low birth weight on obesity, diabetes, and cardiovascular disease are thought to arise from
Evolutionary perspectives on sex differences and implications for development
Ever since Darwin wrote ‘On The Origin of Species’ sexual selection has been central to the theory of evolution depending “not on a struggle for existence, but on a struggle between the males for possession of the females; the result is not death to the unsuccessful competitor, but few or no offspring” [66]. While there are numerous differences across species, Darwin's generalization has been supported that males, in contrast to females, at certain times give priority to competition and
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