Is there a viability–vulnerability tradeoff? Sex differences in fetal programming
Open accessAbstract
Objective In this paper we evaluate the evidence for sex differences in fetal programming within the context of the proposed viability-vulnerability tradeoff.Methods We briefly review the literature on the factors contributing to primary and secondary sex ratios. Sex differences in fetal programming are assessed by summarizing previously published sex difference findings from our group (6 studies) and also new analyses of previously published findings in which sex differences were not reported (6 studies).Results The review and reanalysis of studies from our group are consistent with the overwhelming evidence of increasing risk for viability among males exposed to environmental adversity early in life. New evidence reported here support the argument that females, despite their adaptive agility, also are influenced by exposure to early adversity. Two primary conclusions are (i) female fetal exposure to psychobiological stress selectively influences fear/anxiety, and (ii) the effects of female fetal exposure to stress persist into preadolescence. These persisting effects are reflected in increased levels of anxiety, impaired executive function and neurological markers associated with these behaviors.Conclusions A tacit assumption is that females, with their adaptive flexibility early in gestation, escape the consequences of early life exposure to adversity. We argue that the consequences of male exposure to early adversity threaten their viability, effectively culling the weak and the frail and creating a surviving cohort of the fittest. Females adjust to early adversity with a variety of strategies, but their escape from the risk of early mortality and morbidity has a price of increased vulnerability expressed later in development.
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Infant biological sex will be used in analyses of infant outcomes as male sex is associated with less optimal outcomes, maternal prenatal depression and impaired neonatal motor behavior, and female sex is associated with prenatal maternal depression and increased anxiety.
“Infant biological sex will be used in analyses of infant outcomes as male sex is associated with less optimal outcomes [40], maternal prenatal depression and impaired neonatal motor behavior [41], and female sex is associated with prenatal maternal depression and increased anxiety.”
From The mastery lifestyle intervention to reduce biopsychosocial risks for pregnant Latinas and African Americans and their infants: protocol for a randomized controlled trial (2022) · cites this paper as [40]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredFemales, but not males, exposed to elevated levels of maternal cortisol early in pregnancy had significantly enlarged amygdala and increased levels of anxiety in childhood.
“Additionally, females, but not males, exposed to elevated levels of maternal cortisol early in pregnancy had significantly enlarged amygdala and increased levels of anxiety in childhood [123].”
From Stress and the HPA Axis: Balancing Homeostasis and Fertility. (2017) · cites this paper as [123]
Effects of female fetal exposure to stress persists into preadolescence, as reflected in increased levels of anxiety, impaired executive function, and neurological markers associated with these behaviors.
“The effects of female fetal exposure to stress persists into preadolescence, as reflected in increased levels of anxiety, impaired executive function, and neurological markers associated with these behaviors [123].”
From Stress and the HPA Axis: Balancing Homeostasis and Fertility. (2017) · cites this paper as [123]
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“Infant biological sex will be used in analyses of infant outcomes as male sex is associated with less optimal outcomes [40], maternal prenatal depression and impaired neonatal motor behavior [41], and female sex is associated with prenatal maternal depression and increased anxiety.”
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Self-citation
- Authors
- Sandman, C. A., Glynn, L. M., & Davis, E. P.
- Affiliations
- University of California, Irvine (US)
- Chapman University (US)
- University of Denver (US)
- Corresponding author
- Sandman, Curt A
- Venue
- Journal of Psychosomatic Research
- Publisher
- Elsevier BV
- Published
- 2013-10
- Volume
- 75
- Issue
- 4
- Pages
- 327-335
- ISSN
- 0022-3999 (ISSN-L)
- PMC
- PMC3796732
- OpenAlex
- W2140404034
- Cited by
- 343
- References
- 55
- Citations by year
- 2026: 20 · 2025: 14 · 2024: 30 · 2023: 29 · 2022: 36 · 2021: 30 · 2020: 44 · 2019: 34 · 2018: 28 · 2017: 29 · 2016: 19 · 2015: 20 · 2014: 9 · 2013: 1
- FWCI
- 15.20
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Psychosomatic Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Chapman University Digital Commons (Chapman University) (submittedVersion, cc-by-nc-nd)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (P50MH096889, MH096889)
- National Institute of Neurological Disorders and Stroke (NS-41298;, R01NS041298)
- National Center for Research Resources (M01RR000827)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD028413, HD 51852, R01HD051852, HD-28413, R01HD040967, HD-50662, R01HD065823, HD40967, R01HD050662, HD065823)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- fetal programming, sex differences, childhood adversity, prenatal stress, sex ratio, anxiety, executive function, brain development
- MeSH terms
- Adaptation, Psychological, Anxiety, Brain, Child, Child Development, Corticotropin-Releasing Hormone, Fear, Female, Fetal Viability, Gestational Age, Humans, Hydrocortisone, Hypothalamo-Hypophyseal System, Male, Milk, Human, Organ Size, Pituitary-Adrenal System, Placenta, Predictive Value of Tests, Pregnancy, Prenatal Exposure Delayed Effects, Prospective Studies, Psychomotor Performance, Sex Characteristics, Stress, Psychological, Biomarkers, Pregnant People, Fetal Development, Executive Function
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