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Edited by Gene E. Robinson, University of Illinois, Urbana, IL, and approved December 18, 2008 (received for review September 4, 2008)
Abstract
Exposure to adversity in utero at a sensitive period of development can bring about physiological, structural, and metabolic changes in the fetus that affect later development and behavior. However, the link between prenatal environment and offspring outcomes could also arise and confound because of the relation between maternal and offspring genomes. As human studies cannot randomly assign offspring to prenatal conditions, it is difficult to test whether in utero events have true causal effects on offspring outcomes. We used an unusual approach to overcome this difficulty whereby pregnant mothers are either biologically unrelated or related to their child as a result of in vitro fertilization (IVF). In this sample, prenatal smoking reduces offspring birth weight in both unrelated and related offspring, consistent with effects arising through prenatal mechanisms independent of the relation between the maternal and offspring genomes. In contrast, the association between prenatal smoking and offspring antisocial behavior depended on inherited factors because association was only present in related mothers and offspring. The results demonstrate that this unusual prenatal cross-fostering design is feasible and informative for disentangling inherited and prenatal effects on human health and behavior. Disentangling these different effects is invaluable for pinpointing markers of prenatal adversity that have a causal effect on offspring outcomes. The origins of behavior and many common complex disorders may begin in early life, therefore this experimental design could pave the way for identifying prenatal factors that affect behavior in future generations.
Footnotes
- 1To whom correspondence may be addressed. Email: f.rice{at}ucl.ac.uk or thapar{at}cardiff.ac.uk
Author contributions: G.T.H. and A.T. designed research; F.R. performed research; F.R. and G.T.H. analyzed data; and F.R., G.T.H., J.B., D.F.H., M.v.d.B., and A.T. wrote the paper.
↵2Present address: Clinical, Educational and Health Psychology Research Department, Division of Psychology and Language Sciences, University College London, London WC1E 6BT, United Kingdom.
↵3Present address: Centre for Research on Children and Families and the Department of Psychology, University of Otago, Dunedin, New Zealand.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Freely available online through the PNAS open access option.
- © 2009 by The National Academy of Sciences of the USA
Disentangling prenatal and inherited influences in humans with an experimental design
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