Food Aversions and Cravings during Pregnancy on Yasawa ...

[Pages:36]Food Aversions and Cravings during Pregnancy on Yasawa Island, Fiji

Luseadra McKerracher1 (corresponding author), Mark Collard1,2, and Joseph Henrich3 1Department of Archaeology and Human Evolutionary Studies Program, Simon Fraser University. EDB 9635, 8888 University Dr., Burnaby, BC, Canada, V5A 1S6 2Department of Archaeology, University of Aberdeen, UK. Meston Bldg., Old Aberdeen, Scotland, UK, AB24 3UE 3Departments of Psychology and Economics, University of British Columbia, Canada. 1236 West Mall, Vancouver, BC, Canada, V6T 1Z4

Contact Information for corresponding author: Email: ljm8@sfu.ca Department phone: 778 782 3135 Department fax: 778 782 5666

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Keywords

Pregnancy; diet; aversions; cravings; Fiji

Abstract

PURPOSE: Women often experience novel food aversions and cravings during pregnancy. These appetite changes have been hypothesized to represent adaptive responses to challenges posed by pregnancy, including maternal immune suppression, metabolic changes, and oxidative stress and fetal organogenesis and growth requirements. Here, we assess the extent to which data from an indigenous population in Fiji accord with predictions of this hypothesis. METHODS: We use interview data from 70 Fijian women from Yasawa Island to qualitatively assess the predictions that aversions focus preferentially on foods likely to aggravate the challenges of pregnancy and that cravings focus preferentially on foods containing nutrients likely to be depleted by these challenges. We also use the 2 test to quantitatively test the prediction that women experiencing nutrient losses due to aversions are more likely than other women to crave foods containing missing nutrients. RESULTS: Aversions focus predominantly on foods expected to exacerbate the challenges of pregnancy such as fish and cassava. Cravings usually focus on bananas/plantains, fruits, and other foods that provide calories and micronutrients while posing few threats to mothers and fetuses. Women that experience aversions to specific foods are more likely than other women to crave foods that meet similar nutritional needs as those provided by the aversive foods. CONCLUSIONS: Our data support the hypothesis that food aversions and cravings experienced by many pregnant women reflect adaptive responses to challenges of pregnancy. The aversions and cravings may operate in tandem with culturally transmitted information that also offers pregnant women adaptive guidance regarding diet.

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1 1. Introduction

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3 In this paper, we report new evidence regarding appetite changes during pregnancy in an 4 indigenous population from Yasawa Island, Fiji. In particular, we focus on the development 5 of aversions to foods that the women usually like but found unpalatable during pregnancy 6 as well as on the development of strong, specific cravings for foods during pregnancy. The 7 patterning in the aversions and cravings data from the Yasawa women is consistent with 8 the hypothesis that appetite changes in pregnancy are an adaptive strategy for dealing with 9 challenges to maternal and offspring fitness posed by gestation.

10 Relative to other life stages, pregnancy presents a major opportunity for selective processes 11 to operate on both genes and culture in humans (Brown et al. 2013). For mothers and 12 offspring, pregnancy poses at least five unique immunological, endocrinological, 13 metabolic, and developmental challenges. These five challenges of pregnancy are: adaptive 14 immune suppression, embryo tissue differentiation, genetic conflict, oxidative stress, and 15 changes in energy budget. We describe these challenges in detail below:

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1) Adaptive Immune-Suppression: To facilitate the tolerance of non-self fetal tissue,

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mothers down-regulate their own immune functions following conception. This

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immune system suppression leaves mothers and embryos particularly vulnerable to

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exploitation by pathogens (Flaxman & Sherman 2000; Fessler 2002a; Svensson-

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Arvelund et al. 2013).

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2) Embryo Tissue Differentiation: Embryonic tissues differentiate and

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organogenesis occurs in early pregnancy. Developmental insults due to illness or

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exposure to chemical toxins during this phase can have particularly radical

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downstream negative effects on offspring phenotype (Langley-Evans 2006; Myatt

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2006; Rillamas-Sun 2010).

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3) Genetic Conflict: Pregnancy requires mother and offspring to share maternal

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resources, but offspring interests usually differ from those of their mothers because

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they have only ~50% of their genes in common (Trivers 1974; Haig 1993). As such,

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offspring generally demand more energetic investment than mothers are willing to

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supply. This genetic conflict can negatively impact maternal metabolic function and

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offspring health and survivorship if the result favours either the mother or the

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offspring rather than equitably partitioning resources (Haig 1993; Crespi &

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Badcock 2008; Das et al. 2009; Crespi 2010; 2011). Unchecked fetal manipulation

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of maternal endocrinology can dangerously elevate maternal blood pressure and

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rates of protein excretion (preeclampsia) and/or impair sugar absorption and elevate

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circulating sugar levels (gestational diabetes mellitus).

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4) Oxidative Stress: Normal cell metabolism produces reactive oxygen-based

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molecules ("reactive oxygen species") that can cause cell damage and DNA

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degradation. Presence of antioxidants (compounds that neutralize reactive oxygen

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species so that they can be safely excreted) limits the toxicity of such molecules.

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However, placental tissues produce particularly high volumes of reactive oxygen

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species, often to the extent that they outnumber stored or normal dietary

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antioxidants, resulting in oxidative stress. Oxidative stress in pregnancy is

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associated with several negative health and survivorship outcomes for both mothers

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and offspring including egg cell degradation, degradation of the uterine lining,

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increased risk of spontaneous abortion, preeclampsia, and fetal growth restriction

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(Jauniaux et al. 2006; Al-Gubory 2013; Paine et al. 2013).

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5) Changes in Energy Budget: Support of a fetus increases a mother's energy and

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nutrient requirements (Dufour & Sauther 2002; Fessler 2002a). Intake requirements

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increase during or immediately following a time in which maternal diet is often

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circumscribed by nausea, vomiting, and the development of novel aversions to

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foods, making it more difficult for pregnant women relative to other adults to secure

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and mobilize needed energy and nutrients.

54 All of these pregnancy challenges affect and/or are affected by diet and eating behaviours. 55 At the same time, eating presents its own set of adaptive challenges throughout the 56 lifecourse for both males and females (Sherman & Flaxman 2001). Many edible 57 compounds necessary for growth, development, and body maintenance can result in 58 toxicity or poisoning if ingested at rates above a size-specific and development-stage59 specific dose threshold (Gerber et al. 1999). Furthermore, most plant-based foods have 60 evolved to produce toxic compounds to reduce the risk of exploitation by fungi, parasites, 61 pathogens, and invertebrate and vertebrate predators (Billing & Sherman 1998; Flaxman 62 & Sherman 2000; Sherman & Hash 2001; Sherman & Flaxman 2001; Fessler 2002a; 63 Flaxman & Sherman 2008). Such compounds can disrupt or even shut down cellular 64 function in humans. Lastly, eating provides food-borne pathogens ready access to the 65 bloodstream (Sherman & Flaxman 2001).

66 Evidence suggests that humans have evolved a number of physiological, psychological and 67 cultural solutions to the challenges associated with eating (Eaton & Konner 1985; Patil & 68 Young 2012). With respect to physiology, ingestion of biochemical toxins and/or high 69 levels of food-borne pathogens can trigger a number of symptoms, most notably vomiting 70 and diarrhea, which facilitate the rapid expulsion of toxic or contaminated food items 71 (Flaxman & Sherman 2000). Psychologically, we experience appetite sensations such as 72 the development of aversions to foods previously associated with physiologic expressions

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73 of nausea, vomiting, or diarrhea and the development of cravings for foods that contain 74 difficult-to-obtain nutrients (Williams & Nesse 1991; Patil & Young 2012). Such aversions 75 and cravings appear to be associated with, respectively, motivations to avoid or motivations 76 to seek particular foodstuffs (Drewnowski 1997; Sclafani 1997). Culturally, many human 77 populations possess food taboos ? prohibitions against eating certain foods ? that appear to 78 focus preferentially on foods especially likely to pose health risks (Fessler & Navarrete 79 2003). Moreover, many populations have developed food preparation techniques that 80 involve heating foods to temperatures sufficiently high to denature bacterial proteins and/or 81 adding spices that contain antimicrobial compounds at levels sufficient to slow the 82 proliferation of food-borne pathogens (Billing & Sherman 1998; Sherman & Flaxman 83 2001; Sherman & Hash 2001). Also in the cultural realm, in many populations, particular 84 food items and recipes are associated with desirability, and such food items frequently 85 contain difficult-to-access essential nutrients (Rozin & Vollmecke 1986).

86 Given that selection is strong during pregnancy and that human diet generally appears to 87 have been shaped by both genetic and cultural evolution to adaptively reduce exposure to 88 food-borne pathogens and toxins and to increase procurement of essential nutrients, we 89 should expect humans to have developed specific dietary adaptations in relation to the 90 unique challenges of pregnancy.

91 A number of hypotheses have been put forward in the literature that propose functional and 92 evolutionary links between pregnancy-related changes in visceral appetite sensations (food 93 aversions and cravings not mediated by conscious, rational thought) and one or more of the 94 challenges associated with pregnancy. These hypotheses, their main predictions, and to 95 which challenges of pregnancy they relate are summarized in Table 1 as well as described 96 in the text that follows.

97 [Table 1]

98 The maternal-embryo protection hypothesis holds that the development of novel food 99 aversions during pregnancy reflects a set of evolved mechanisms that motivate women to 100 avoid foods that are especially likely to contain pathogenic and chemical toxins during 101 maternal adaptive immune suppression and during embryo tissue differentiation (see also 102 Hook 1978; 1980; 1988; Profet 1992; 1997; Flaxman & Sherman 2000; Fessler 2002). 103 According to Fessler (2002), this phenomenon may extend beyond visceral aversions, such 104 that culturally evolved food taboos also function to reduce maternal and embryo exposure 105 to toxins during the vulnerable developmental window.

106 The compensatory placental growth hypothesis proposes that pregnancy-related food 107 aversions result from fetal manipulation of maternal physiology that motivates mothers to 108 avoid energy-dense foods. Counter-intuitively, maternal energy restriction benefits fetuses

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109 because energy-restricted mothers prioritize allocating whatever resources they have 110 available to embryo and placental development (Huxley 2000).

111 Brown et al. (2013) outline a hypothesis that we call the gestational metabolic syndrome 112 avoidance hypothesis. This hypothesis holds that food aversions during pregnancy may 113 have evolved in part to motivate women to avoid eating foods that increase the risk of 114 developing gestational diabetes mellitus and preeclampsia. These two pregnancy 115 complications appear to represent extreme, pathological expressions of genetic conflict in 116 which fetuses promote placental artery restriction and inhibit maternal sugar absorption so 117 as to secure relatively high levels of maternal investment (Haig 1993; Haig 1999). But, 118 according to the hypothesis, mothers may also have evolved various counter-adaptations 119 to reduce the risk of developing these pathologies.

120 The nutrient-seeking hypothesis proposes that pregnancy-related cravings motivate 121 women to find and eat foods containing energy, macro-, and micro- nutrients essential to 122 fetal development (Hook 1978; 1980; Tierson et al. 1985). Fessler (2002) suggests an 123 important addendum to this hypothesis: pregnant women may have particular propensities 124 to seek nutrients that are depleted in or missing from their diets due to food aversions and 125 vomiting.

126 Lastly, we propose the antioxidant procurement hypothesis. According to this 127 hypothesis, some pregnancy-related cravings represent evolved motivations to consume 128 foods that contain high levels of antioxidants so as to mitigate the effects of oxidative stress 129 related to placentation and placental maintenance. Consumption of foods containing large 130 quantities of antioxidants such as most fruits and greens increases the availability of 131 antioxidants to bind with and neutralize reactive oxygen species that would otherwise 132 disrupt or damage cellular function in pregnant women and fetuses.

133 Each of these hypotheses has some empirical support, although few formal tests have been 134 carried out to date. Data from a number of studies regarding within or among population 135 variation in diet composition and expression of food aversions in pregnancy are consistent 136 with the maternal-embryo protection hypothesis. The data in question suggest that such 137 aversions focus preferentially on animal foods ? which are subject to high rates of spoilage 138 if refrigeration is not available, especially in hot climates ? and/or on plant foods that are 139 high in toxins (Flaxman & Sherman 2000; Fessler 2002a; Pepper & Roberts 2006; Weigel 140 et al. 2011; Steinmetz et al. 2012; Mckerracher et al. 2014). Evidence from a cross-national 141 study carried out by Pepper and Roberts (2006) is consistent with the compensatory 142 placental growth hypothesis. These authors found that women are more likely to develop 143 nausea during pregnancy in countries with more nutrient dense diets. Additionally, a 144 veterinary medicine study published in 1998 found that sheep fed more restricted diets

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145 produced offspring with larger placentas, seemingly favouring early fetal growth (Lunney 146 1998). Regarding the gestational metabolic syndrome avoidance hypothesis, evidence from 147 more than one million births in New York between 1995 and 2003 suggests that women 148 from populations with long histories of farming are less likely to develop gestational 149 diabetes mellitus (Savitz et al. 2008), perhaps indicating the evolution of a maternal 150 counter-adaptation to fetal energy demands in environmental contexts in which calories are 151 abundant (Brown et al. 2013). In addition, some recent studies on populations without long 152 histories of farming have found that, in such populations, women frequently find starchy 153 cereal crops aversive. The nutrient-seeking hypothesis is supported by several studies that 154 suggest the most aversive foods are also the least likely to be craved and vice versa (e.g. 155 Flaxman & Sherman 2000; Weigel et al. 2011; Steinmetz et al. 2012). This pattern may be 156 consistent with the view that women have evolved a pregnancy-specific mechanism to seek 157 out sources of energy and possibly other nutrients when they are experiencing nutrient 158 losses due to aversions. Lastly, pertaining to the antioxidant procurement hypothesis, it 159 appears that, in the overwhelming majority of populations surveyed to date, fruits and fruit 160 juices are among the most frequently reported pregnancy-related cravings (Flaxman & 161 Sherman 2000; Olusanya & Ogundipe 2009; Weigel et al. 2011). Fruits and fruit juices not 162 only represent sources of calories that are relatively low risk in terms of pathogenesis and 163 chemical toxicity but also represent sources of a wide variety of necessary but hard-to-get 164 antioxidants, especially vitamin A and zinc.

165 As the foregoing discussion implies, the hypotheses are not necessarily mutually exclusive. 166 It is possible that all the challenges of pregnancy play a role in driving within- and among167 population variations in expression of aversions and cravings during pregnancy. Some of 168 the challenges may also underpin among-population variation in cultural phenomena such 169 as food taboos relating to pregnancy, female-specific food taboos, and socially transmitted 170 information about foods that may improve maternal and/or fetal health outcomes. Despite 171 this possible compatibility among the hypotheses and despite proposed links between 172 aversions and cravings, to our knowledge, no previous study has empirically treated food 173 aversions and food cravings of pregnancy (and/or their cultural equivalents) as an adaptive 174 complex that co-evolved to solve the suite of ecological and physiologic challenges 175 imposed by gestation.

176 In our study, we aimed to integrate these multiple hypotheses pertaining to the physiologic 177 challenges of pregnancy as we investigated patterning in food aversions and cravings of 178 pregnancy as described by indigenous women from Yasawa Island, Fiji.

179 The remainder of the paper is organized into four sections. In the next section, section 2, 180 we provide background information on the study site and on the lifeways and diets of the 181 people of Yasawa Island, and discuss our methods. In section 3, we present the main results

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182 of two sets of analyses in which we describe rates of foci for food aversions and cravings 183 and we assess how cravings pattern in relation to aversions. In section 4, we partition the 184 diets of Yasawa Islanders into three higher order categories ? animal foods, starchy plant 185 foods, and fruits and vegetables ? and discuss the patterning of aversions and cravings 186 within each of these higher order categories and offer suggestions as to how such patterning 187 may relate to variation in expression of one or more of the physiologic challenges of 188 pregnancy. In the final section, we engage in a broader discussion in which we summarize 189 the available evidence regarding the evolutionary ecology of pregnancy-related food 190 aversions and food cravings among the women of Yasawa Island, focusing particularly on 191 possible interactions between the visceral changes in appetite reported in this paper and 192 cultural regulation of pregnancy diet (reported in Henrich & Henrich 2010).

193 2. Population, data, and methods

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195 The data for this study were collected as part of a larger, ongoing research project led by 196 JH on social organization, ecology, life history, and culture on Yasawa Island, Fiji. Over 197 several years, the team has gathered information from the men, women, and children of 198 Yasawa about local subsistence economy, diet, food taboos, reproductive histories and 199 demography, and cultural learning and transmission (Henrich & Henrich 2010; Henrich & 200 Broesch 2011; Kline et al. 2013; Broesch et al. 2014; McKerracher et al. in press).

201 The 70 women interviewed regarding appetite sensations in pregnancy are from three 202 villages located on Yasawa Island, on the northwest end of the Fijian archipelago. The 203 climate on the island is warm year-round, but there are two seasons ? a wet and a dry ? 204 marked sharply by variation in precipitation. The soils of the island are sandy and dry, but 205 sufficient to produce a variety of root and fruit crops (see data supplement for Henrich & 206 Henrich 2010).

207 The people of Yasawa are primarily small-scale fisher-farmers. Men in these communities 208 fish and maintain garden plots while the women, with the assistance of older children, 209 gather shellfish and other littoral resources and also carry out the majority of the domestic 210 work. Additional details on the ethnographic context for this project are available in 211 Henrich and Henrich (2010) and Henrich and Broesch (2011).

212 The diets of Yasawa Islanders are predominantly local. Cassava provides the majority of 213 calories, although yams, plantains, breadfruit, and imported wheat and sugar also make 214 important energetic contributions. Marine foods provide the bulk of the protein in the 215 Yasawan diet. Fat derives from coconut milk and fish as well as from imported oil and 216 small amounts of imported or local terrestrial meat. Local fruits and vegetables from the

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