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Reproductive Immunosuppression and Diet F 21 Current Anthropology Volume 43, Number 1, February 2002 ᭧ 2002 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved 0011-3204/2002/4301-0002$3.50 Around the world, people recognize that pregnancy is Reproductive associated with nausea, vomiting, and marked changes in dietary preferences, a pattern termed pregnancy sick- ness (Flaxman and Sherman 2000).2 Nausea and vomiting Immunosuppression generally serve to protect the individual from the harm- ful effects of ingested toxins and toxin-producing path- and Diet ogens; vomiting expels the offensive substance, while nausea, a highly aversive experience, anchors remarkable one-trial learning, motivating future avoidance of the substance (Bernstein 1999). The complex and coordi- An Evolutionary Perspective on nated nature of these features, the specificity of their eliciting conditions, and the obvious benefits that they Pregnancy Sickness and Meat provide all suggest that normal nausea and vomiting are Consumption1 part of an adaptation, a trait that has evolved through natural selection because of the advantages that it fur- nishes to its possessors. However, in contrast to the usual circumstances associated with nausea and vomiting, by Daniel M. T. Fessler many pregnant women experience these symptoms after ingesting foods which others around them eat without ill effect—indeed, it seems that pregnant women often become nauseated before ingestion has occurred and, Pregnancy sickness, a suite of “symptoms” that frequently co-oc- most notably, experience nausea and vomiting at far cur during pregnancy, may be an adaptation providing behavioral higher frequencies than do other members of their com- prophylaxis against infection. Maternal immunosuppression, nec- munities. The striking differences between the circum- essary for tolerance of the fetus, results in gestational vulnerabil- ity to pathogens. Throughout the period of maximal vulnerabil- stances of normal nausea and vomiting and those of preg- ity, dietary behavior is significantly altered via changes in nausea nancy (or “morning”) sickness call for explanation. susceptibility and olfaction and the development of marked aver- A large body of research addresses possible physiolog- sions and cravings. Of food types, meat is both the most likely ical mechanisms underlying pregnancy sickness. Recent to carry pathogens and the principal target of gestational aver- sions and pregnancy taboos. Because meat was prominent in an- cestral human diets but hygienic procedures that effectively individuals provided helpful comments on a draft of this paper: Paul eliminate the risk of meat-borne infection are recent, such path- Sherman, Jonathan Haidt, David Haig, Susan Perry, Jim Moore, Rob ogens likely constituted a source of selective pressure on preg- Boyd, Joe Manson, Dustin Penn, Thomas McDade, Nicholas Blur- nant females throughout human history. Both the relatively low ton Jones, and five very diligent anonymous referees. I also benefited protein and energy demands of the first trimester and the exis- from conversations with Jennifer Fessler, Joan Silk, Leda Cosmides, tence of nonmeat alternatives would have allowed for the evolu- and Sarah Hrdy. Paul Arguello and Karen Hunt Ahmed provided tion of time-limited gestational meat-avoidance mechanisms. research assistance, and John Fessler and Andre Kramerov provided Complementing these mechanisms, gestational cravings target translation assistance. Portions of this project were presented at substances that may influence immune functioning and affect the 2000 meeting of the Human Behavior and Evolution Society. the availability of iron in the gastro-intestinal tract, thereby limi- 2. The Bengkulu of southwestern Sumatra term pregnancy “the ting the proliferation of iron-dependent pathogens. Clinical and good sickness,” a reference to the nausea, vomiting, and strange ethnographic findings are examined in light of these proposals, aversions and cravings which appear early in gestation. For the and directions for future research are outlined. !Kung San of the Kalahari desert, these are diagnostic criteria for pregnancy (Shostak 1981). Soranus of Ephesus, a 2d-century Greek gynecologist, described the same pattern in association with early daniel m. t. fessler is Assistant Professor of Anthropology pregnancy (Temkin 1991), and the Maasai (Spencer 1988) and Tiv at the University of California, Los Angeles (Los Angeles, Calif. (Bohannan and Bohannan 1969) do likewise. Cravings, nausea, and 90095-1553, U.S.A. [[email protected]]). Born in 1963,he vomiting are hallmarks of early pregnancy among the Hokkien Tai- was educated at the University of California, San Diego (B.A., wanese (Barnett 1971) and Tongans (Ostraff et al. 2000, Morton n.d.); 1985; M.A., 1988; Ph.D., 1995). He has conducted ethnographic Culpepper’s 1651 Directory for Midwives notes the same (Fair- research in Indonesia, including a 32-month study of a fishing weather 1968), and these symptoms also occur among the Saraguro village in Bengkulu, Sumatra. His publications include “Toward (Finerman 1985) and Hawaiians (Green and Beckwith 1924). Unique an Understanding of the Universality of Second-Order Emo- gestational cravings are recognized by the Jivaro (Harner 1972) and tions,” in Beyond Nature or Nurture, edited by A. Hinton (New the Tahitians (Levy 1973). Present-day midwives from such diverse York: Cambridge University Press, 1999), “Emotions and Cost/ countries as Sierra Leone, Chile, the Netherlands, Pakistan, Va- Benefit Assessment: The Role of Shame and Self-Esteem in Risk nuatu, Iran, Jamaica, and Nicaragua agree that nausea and vomiting Taking,” in Bounded Rationality, edited by R. Selten and G. Gig- occur in early pregnancy (O’Brien, Relyea, and Lidstone 1997), and erenzer (Cambridge: MIT Press, 2000), and “Pseudoparadoxical anthropologists report the same for highland Ecuador (Weigel et al. Impulsivity in Restrictive Anorexia Nervosa: A Consequence of 2000) and Truk (Fischer 1998 [1963]). Clinical surveys report nausea the Logic of Scarcity” (International Journal of Eating Disorders, and vomiting in association with pregnancy in 75 groups in Western in press). The present paper was submitted 17 viii 00 and ac- Europe, North America, Japan, India, Kenya, Nigeria, Sri Lanka, cepted 20 vi 01. and Hong Kong (Flaxman and Sherman 2000), and ethnographers record the same among indigenous groups in North and South 1. Paul Sherman and Samuel Flaxman graciously shared their pre- America, the Caribbean, Oceania, Australia, Asia, the Middle East, publication results with me. C. David Navarrete wrote the resam- and Africa (reviewed in Weigel 1985 and Flaxman and Sherman pling program and performed the statistical analysis. The following 2000). 19 20 F current anthropology Volume 43, Number 1, February 2002 investigations focus on specific isoforms of human cho- quent publication (2000) also documents the incidence rionic gonadotrophin (hCG) (cf. Jordan et al. 1999; also of pregnancy sickness in a large number of societies and O’Connor et al. 1998), with attention being paid to the summarizes patterns of gestational cravings. influence of hCG on thyroid functioning (Tareen et al. This paper builds on and complements Flaxman and 1995). While some investigators have employed evidence Sherman’s important work in a number of ways. First, regarding proximate mechanisms to argue that preg- seeking additional evidence of the unique salience of nancy sickness is merely a nonfunctional or even dys- meat during pregnancy, I survey the targets of pregnancy functional by-product of hormonal changes accompa- taboos in 73 cultures. Second, because adaptations are nying pregnancy (see Weigel 1985 for review and Profet thought to arise in response to highly specific selection 1992 and Flaxman and Sherman 2000 for additional dis- pressures, I document that (a) the timing of nausea, vom- cussion), others have postulated that pregnancy sickness, iting, and aversions coincides with the period of maximal like normal nausea and vomiting, is a functional adap- immunovulnerability and (b) meat-borne pathogens pos- tation. Specifically, the greater sensitivity of the mother sess attributes that make them particularly dangerous has been explained as a means of compensating for the during precisely this period. Third, because adaptations special vulnerability of the embryo or fetus (hereafter arise only in response to recurrent selection pressures, I generically termed the “developing organism”). present evidence that meat-borne pathogens have prob- To date, adaptationist explanations have taken a num- ably constituted a source of selective pressure through- ber of forms. Hook (1976, 1978, 1980) and Tierson, Olsen, out much of human history. Fourth, because intrinsic and Hook (1985) initially proposed that pregnancy sick- trade-offs are thought to constrain the efficiency with ness protects the developing organism from a heteroge- which any single adaptive goal is pursued, I demonstrate neous collection of toxins such as those thought to occur that the benefits of avoiding meat during early pregnancy in coffee. Weigel (1985) generalized this list to include a are likely to have generally exceeded the costs. Fifth, range of teratogens and pathogens. Noting that preg- because adaptations are best identified on the basis of nancy sickness is concentrated in the first trimester, the complex nature of their designs, extending sugges- when the developing organism is most vulnerable to in- tions made by Profet and others I introduce evidence
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