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Pregnancy Sickness and Embryo Quality Opinion TRENDS in Ecology & Evolution Vol.17 No.3 March 2002 115 or mutagens [8–11]. Third, NVP occurs during Pregnancy sickness organogenesis, when the developing embryo is at greatest susceptibility [9] to mutagens. Fourth, the incidence of NVP correlates with diet [8–11], being largely absent in and embryo quality societies where maize and/or corn are food staples [10,12]. The fifth and most direct evidence is the correlation of NVP with pregnancy outcome: mothers with NVP Scott Forbes experience lower rates of stillbirth, early pregnancy loss, preterm delivery and low birth weight than do mothers without [15–17], a pattern attributed to the prophylactic Nausea and vomiting are routine features of early pregnancy in humans. But are benefit of food aversions associated with NVP. they adaptive or pathological? Several lines of evidence suggest that they The case for embryo protection therefore appears protect mothers and developing embryos from dietary mutagens and sound. But might there be another explanation? Haig pathogens. Nausea and vomiting in pregnancy (NVP) coincide with the has suggested that pregnancy sickness might arise as a vulnerable period of embryogenesis, are associated with food aversions, and are by-product of maternal–embryo conflict [18,19]. There predictors of positive pregnancy outcomes. Here, I argue that NVP is not directly are numerous potential conflicts between embryo and adaptive, but arises as a byproduct of genetic conflict between mother and mother during pregnancy, and pre-eclampsia and embryo. The negative correlation between first-trimester spontaneous abortion gestational diabetes can be direct results [10,11]. One and NVP is not the result of protection of embryos from environmental mutagens conflict in particular is directly relevant to pregnancy or pathogens, but the result of intrinsic chromosomal defects. These low-quality sickness: who decides whether the pregnancy continues? embryos produce subnormal levels of human chorionic gonadotropin, a hormone For the embryo, and occasionally the mother, it might be involved in pregnancy maintenance, and the probable proximate trigger for NVP. a struggle for life or death (Box 1). Here, the pregnancy hormone HUMAN CHORIONIC GONADOTROPIN (hCG) is Lassitude, sleepiness and loss of appetite signaled the key. Haig describes it as an allocrine hormone [10] onset of pregnancy for the Kwakiutl women of the Pacific produced by one individual to manipulate the coast of Canada. A pregnant woman was careful about endocrine system of another. And hCG does exactly her diet. She would eat dry salmon, fat and berries, but that. Closely related to LUTEINIZING HORMONE (LH), hCG avoided whale meat, squid, and salmon eggs. If she regulates early CORPUS LUTEUM function. It is secreted had food cravings, her husband attempted to provide by the preimplantation embryo, and subsequently by these foods. And qualmishness and appetite loss were the placental TROPHOBLAST in early pregnancy. Without early signs that the forthcoming child was a girl [1]. hCG, the corpus luteum regresses. Without the corpus For most mothers in most societies, food aversions luteum, PROGESTERONE production falls. And, without and some nausea and vomiting are routine features progesterone, the pregnancy fails. of early pregnancy [2]. And, for a small fraction, the Maternal endocrine control of gestation is open nausea and vomiting is prolonged and debilitating to subversion by the embryo. Consider an ancestral (HYPEREMESIS GRAVIDARUM: see Glossary), and if left mother and her offspring. She alone regulates early untreated can be fatal [3,4]. But is pregnancy sickness pregnancy with LH. But the embryo has the same beneficial? Might it be an adaptation rather than complement of genes as its mother and placental pathology? In the late 1970s, Hook and Little access to the maternal bloodstream. Imagine further postulated that nausea and vomiting during a mutation that causes an embryonic gene encoding pregnancy (NVP or morning sickness) protected LH production to be turned on, thus adding to the developing embryos from alcohol (a potent dietary maternal supply. Some embryos that would have teratogen) and tobacco smoke [5,6]. Walker et al. [7] been aborted because of low maternal LH production examined NVP in relation to dietary aversions and would now survive. (This neat embryonic trick is cravings, and documented aversions to meat, fish, not exclusive to humans, but is rare in eutherian coffee and fatty foods, and cravings for sour, savory mammals, having arisen on at least three separate and sweet foods, and also for fruits and meat. Profet occasions [18]: in horses, guinea pigs and primates.) [8,9] later argued that NVP shielded embryos from an With a substantial selective advantage, such a array of dietary mutagens and pathogens, particularly mutation would quickly become fixed, triggering an plant toxins. Most recently, Flaxman and Sherman evolutionary arms race. Mothers that now carry suggested that NVP deters the ingestion of spoiled and embryos that they would ‘prefer’ in an evolutionary burned meats, fish and eggs that might affect not only sense to abort (no conscious choice implied) reduce their the developing embryo, but also mothers who are own LH production and/or increase the level of hormone immunocompromised during pregnancy [10,11]. required for pregnancy maintenance. Embryos respond Scott Forbes Five lines of evidence support this embryo–maternal by elevating LH production even further. This appears Dept of Biology, protection hypothesis. First, pathogens and mutagens to be exactly what has happened through a series of University of Winnipeg, occur naturally in the diet and some foods have gene duplications [18]. Mothers retaliate, and so it Winnipeg, MB, harmful effects [8–14]. Second, NVP is associated continues, coming to an end when further escalation Canada R3B 2E9. e-mail: with food aversions, and strong and pungent odors becomes too costly for one or both parties. Human [email protected] are often correlated with the presence of pathogens mothers and their embryos just might have reached http://tree.trends.com 0169-5347/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(02)02428-4 116 Opinion TRENDS in Ecology & Evolution Vol.17 No.3 March 2002 Box 1. When does genetic conflict in pregnancy occur? Flaxman and Sherman [a] argue that if genetic conflict holds it both obligate brood reduction and early spontaneous abortion are should occur late in pregnancy when the resource demands of the prospective adaptations. fetus are greatest, rather than early in pregnancy when nausea Offspring and parent interests, however, can diverge. By and vomiting in pregnancy (NVP) actually occurs. But this producing elevated levels of human chorionic gonadotropin argument fails to recognize the pluralistic nature of genetic conflict (hCG), embryos avert the pregnancy loss that is surprisingly in human pregnancy. Conflict over the division of resources common: between one third and three quarters of human between mother and embryo does occur later in pregnancy, and conceptions are spontaneously aborted [f]. Intriguingly, the manifests as pre-eclampsia and gestational diabetes [b,c]. The most common chromosomal birth defect – trisomy 21 conflict that occurs early in gestation, however, is about survival (Down syndrome) – is associated with abnormally high hCG rather than the allocation of current resources. That is, should the production [b,f], further implicating hCG in a system that avoids pregnancy be terminated or continued? According to the theory maternal spontaneous abortion. of parent–offspring conflict [d], the mother should hold a more References conservative view about such decisions than should the offspring a Flaxman, S.M. and Sherman, P.W. (2000) Morning sickness: a mechanism (from an evolutionary rather than a conscious perspective). Here, for protecting mother and embryo. Q. Rev. Biol. 75, 113–148 a striking parallel occurs between early spontaneous abortion in b Haig, D. (1993) Genetic conflicts in human pregnancy. Q. Rev. Biol. 68, 495–532 humans and obligate brood reduction in birds, where a maximal c Haig, D. (1996) Altercation of generations: genetic conflicts of pregnancy. benefit is obtained from early brood reduction before any Am. J. Reprod. Immunol. 35, 226–232 proximate food limitation occurs [e]. When, for whatever reason, d Mock, D.W. and Parker, G.A. (1997) The Evolution of Sibling Rivalry, Oxford the circumstances for continued pregnancy are, from a mother’s University Press e Forbes, L.S. and Ydenberg, R.C. (1992) Sibling rivalry in a variable perspective, adverse (e.g. significant food shortfall), she could environment. Theor. Popul. Biol. 41, 335–360 potentially avoid the major costs by early spontaneous abortion f Forbes, L.S. (1997) The evolutionary biology of spontaneous abortion in before substantial resources are committed to the embryo. Thus, humans. Trends Ecol. Evol. 12, 446–450 this point. The cost is pregnancy sickness, a mild sickness, given that it is more common when the fetus inconvenience for most mothers (but see [20]), but in a is female than when it is male [26]. minority of cases, hyperemesis gravidarum results. Establishing a direct link between hCG and pregnancy sickness has been difficult, partly because The link between hCG and pregnancy sickness hCG exists in multiple forms, and hyperemesis Is there a hormonal link to NVP, as would be expected gravidarum might be linked to abnormal hCG
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