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. Author manuscript; available in PMC: 2013 May 8.
Published in final edited form as: Behav Genet. 1997 Jul;27(4):373–387. doi: 10.1023/a:1025692031673

Heritable Variation in Food Preferences and Their Contribution to Obesity

Danielle R Reed 1,3, Alexander A Bachmanov 2, Gary K Beauchamp 2, Michael G Tordoff 2, R Arlen Price 1
PMCID: PMC3647229  NIHMSID: NIHMS459061  PMID: 9519563

Abstract

What an animal chooses to eat can either induce or retard the development of obesity; this review summarizes what is known about the genetic determinants of nutrient selection and its impact on obesity in humans and rodents. The selection of macronutrients in the diet appears to be, in part, heritable. Genes that mediate the consumption of sweet-tasting carbohydrate sources have been mapped and are being isolated and characterized. Excessive dietary fat intake is strongly tied to obesity, and several studies suggest that a preference for fat and the resulting obesity are partially genetically determined. Identifying genes involved in the excess consumption of dietary fat will be an important key to our understanding of the genetic disposition toward common dietary obesity.

Keywords: Obesity, food preferences, dietary fat intake, saccharin, sweet, taste

INTRODUCTION

The study of the genetic basis of food preferences is an important but difficult endeavor. Personal and cultural experiences with foods play a strong role in the development of food preferences, and it is difficult to parse out the contribution of genetic variability from experience and environment. This review summarizes what is known about the genetic basis of food preferences and how these preferences might influence body weight. Although genes probably influence individual differences in alcohol and protein ingestion, this review focuses on the intake of carbohydrate and fat because the proportion and amount of these nutrients in the diet have the clearest and most widely studied role in the development of obesity.

THE PREFERENCE FOR MACRONUTRIENTS IS MORE HERITABLE THAN THAT FOR INDIVIDUAL FOOD ITEMS

Choosing to eat a particular food is a function of the types of foods available at a given moment and is guided by previous personal experience and beliefs about the properties of the food. Given these strong nongenetic determinants of food selection, is there any evidence that individual differences in food preferences are genetically mediated? It is possible that food preferences are genetically determined (e.g., the innate preference for sweets) but there may be little or no genetic variation among humans. Studies designed to test the contribution of genetic variability, experience, and environment to food selection fall into two categories: family members are compared to see if the degree of biological relatedness covaries with similarities in behavior (a family study) or if monozygotic twins pairs are more behaviorally similar compared with dizygotic twins pairs (a twin study).

Studies of the preferences for individual food items and studies of total macronutrient intake provide different types of information about food preferences. Preferences for individual foods are generally assessed by pencil-and-paper questionnaires and may not reflect the subjects’ actual behavior with regard to those foods. Some foods are preferred much more strongly by all subjects than are other foods. If all members of a population under study (e.g., all monozygotic and dizygotic twin pairs) like a food very much, then ceiling effects may limit the ability of the test to assess genetic heritability. Food diaries provide a more accurate estimate of the foods subjects eat, but because food intake is usually measured for only a brief period (3–7 days), it may not be representative of the subjects’ food selection habits. It may also be inaccurate due to reporting biases of subjects.

With these limitations in mind, studies of preferences for individual food items, followed by studies of macronutrient selection patterns, are reviewed below. Although this paper concentrates primarily on carbohydrate and dietary fat selection and its role in obesity, studies that have included a broad variety of foods are reviewed. Most foods are a composite of macronutrients and can be hard to classify as high-carbohydrate or high-fat, so all foods studied are included in Table I.

Table I.

Twin Studies of Preferences for Individual Foods or Tastants

Food item N (MZ/DZ) Heritabilitya Reference
Spicy foods
 Chili peppers (how hot?) 38/34 + Rozin & Millman, 1987
 Spicy foods 48/48 + Faust, 1974
 ”Strong”-tasting foods 16/0 +b Glanville & Kaplan, 1965
Sweet foods
 Candy 232/223 ns Fabsitz et al., 1978
 Cereal, sweetened 14/21 + Falciglia et al., 1994
 Doughnut 13/10 ns Krondl et al., 1983
 Honey 13/10 ns Krondl et al., 1983
 Ice cream 13/10 ns Krondl et al., 1983
 Jam 13/10 ns Krondl et al, 1983
 Jam, jelly, syrup 232/223 ns Fabsitz et al., 1978
 Peppermint 38/34 ns Rozin & Millman, 1987
 Snack cake 14/21 ns Falciglia et al., 1994
 Soda/cola 14/21 ns Falciglia et al., 1994
 Sucrose 146/165 ns Greene et al., 1975
 Sugar 38/34 ns Rozin & Millman, 1987
 Sugar in coffee 232/223 + Fabsitz et al., 1978
 Sugar in tea 232/223 + Fabsitz et al., 1978
Salty foods
 Anchovies 48/48 ns Faust, 1974
 Salt use (heavy) 255/179 + Austin et al., 1987
 Sodium chloride 146/165 ns Greene et al., 1975
Complex carbohydrates
 Cereal, unsweetened 14/21 ns Falciglia et al., 1994
 Cereals 232/223 ns Fabsitz et al., 1978
 French fries 14/21 ns Falciglia et al., 1994
 Potato chips 13/10 ns Krondl et al., 1983
 Potatoes 232/223 ns Fabsitz et al., 1978
 Rice 232/223 ns Fabsitz et al., 1978
 Spaghetti 14/21 ns Falciglia et al., 1994
Vegetables
 Beans 14/21 ns Falciglia et al., 1994
 Black olives 38/34 ns Rozin & Millman, 1987
 Broccoli 13/10 + Krondl et al., 1983
 Broccoli 14/21 ns Falciglia et al., 1994
 Brussels sprouts 13/10 ns Krondl et al., 1983
 Cabbage 13/10 ns Krondl et al., 1983
 Cauliflower 13/10 ns Krondl et al., 1983
 Cooked vegetables 232/223 ns Fabsitz et al., 1978
 Corn 14/21 ns Falciglia et al., 1994
 Green beans 13/10 + Krondl et al., 1983
 Lima beans 38/34 ns Rozin & Millman, 1987
 Parsnips 48/48 ns Faust, 1974
 Peanut butter 232/223 ns Fabsitz et al., 1978
 Radish 38/34 ns Rozin & Millman, 1987
 Raw onion 38/34 ns Rozin & Millman, 1987
 Salads 232/223 ns Fabsitz et al., 1978
 Spinach 13/10 ns Krondl et al., 1983
 Tomatoes 48/48 ns Faust, 1974
 Turnips 13/10 ns Krondl et al., 1983
Fruits and fruit juices
 Apple 14/21 ns Falciglia et al., 1994
 Fruit 232/223 ns Fabsitz et al., 1978
 Lemon 38/34 ns Rozin & Millman, 1987
 Lemon juice 13/10 ns Krondl et al., 1983
 Melon 48/48 ns Faust, 1974
 Orange juice 14/21 + Falciglia et al., 1994
 Strawberry 13/10 + Krondl et al., 1983
 Unsweetened apple sauce 13/10 + Krondl et al., 1983
 Unsweetened grapefruit juice 13/10 + Krondl et al., 1983
 Unsweetened orange juice 13/10 + Krondl et al., 1983
Pharmacologically active foods and beverages
 Alcohol (not beer or wine) 232/223 + Fabsitz et al., 1978
 Alcohol 255/179 + Austin et al., 1987
 Beer 13/10 ns Krondl et al., 1983
 Beer 232/223 ns Fabsitz et al., 1978
 Black coffee 13/10 ns Krondl et al., 1983
 Black coffee 38/34 ns Rozin & Millman, 1987
 Black tea 13/10 ns Krondl et al., 1983
 Coffee 255/179 + Austin et al., 1987
 Coffee 232/223 + Fabsitz et al., 1978
 Iced or hot tea 232/223 + Fabsitz et al., 1978
 Tonic water 13/10 ns Krondl et al., 1983
 Wine 232/223 + Fabsitz et al., 1978
Meats and dairy products
 Bacon 13/10 + Krondl et al., 1983
 Beef liver 38/34 ns Rozin & Millman, 1987
 Cheese 48/48 ns Faust, 1974
 Cheese, American 14/21 ns Falciglia et al., 1994
 Chicken 14/21 ns Falciglia et al., 1994
 Consomme 13/10 ns Krondl et al., 1983
 Cottage cheese 14/21 + Falciglia et al., 1994
 Eggs 232/223 ns Fabsitz et al., 1978
 Gravy 232/223 ns Fabsitz et al., 1978
 Ham 13/10 ns Krondl et al., 1983
 Hamburger 14/21 ns Falciglia et al., 1994
 Liver 48/48 ns Faust, 1974
 Liverwurst 38/34 ns Rozin & Millman, 1987
 Milk, low fat 14/21 ns Falciglia et al., 1994
 Milk, whole 14/21 ns Falciglia et al., 1994
 Pork, ham bacon 232/223 ns Fabsitz et al., 1978
 Skim, chocolate milk 232/223 ns Fabsitz et al., 1978
 Soft boiled eggs 38/34 ns Rozin & Millman, 1987
 Steak, pot roast 232/223 ns Fabsitz et al., 1978
 Yogurt 48/48 ns Faust, 1974
 Yogurt 38/34 +c Rozin & Millman, 1987
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a

Individual studies differed in data analysis methods, so direct comparisons are difficult; if the investigators reported a p value <.05 for the chosen method of analysis, it is denoted in this table by a +; p values >.05 are denoted as not significant (ns).

b

Glanville and Kaplan (1965) did not examine DZ twin pairs but reported a high correlation between MZ twins.

c

This positive result is based on a negative correlation between DZ twin pairs and a small positive correlation between MZ twin pairs.

Twin and Family Studies of Preferences for Individual Food Items

Overall, studies of food preferences using families and twins have suggested that the heritable component for individual foods is low (Rozin, 1991). Although most of the literature supports this assertion, several lines of evidence suggest a heritable component to the liking or disliking of individual food items; studies of inbred rat strains suggest that preferences for individual foods commonly consumed by humans (such as ham) can breed true in rats and, therefore, have a genetic determination (Runyan and Koschorreck, 1990).

There is not very much agreement among twin studies in their conclusions concerning the heritability of food preferences, with disparate results for the same food being commonplace (Table I). The most robust preference is for pharmacologically active food items such as alcohol and coffee. A liking of spicy and hot foods has been demonstrated (Faust, 1974; Rozin and Millman, 1987; see Rozin, 1991). The liking for orange juice was more similar between monozygotic compared with dizygotic twins in two studies, but it is not clear what property of orange juice may have produced these results. It is also unclear what role spicy foods or orange juice might have in the genesis of obesity.

Studies of family resemblance for individual food items have demonstrated modest or no correlations between first-degree relatives (Birch, 1980; Burt and Hertzler, 1978; Oliveria et al., 1992; Pliner, 1983; Pliner and Pelchat, 1986; Ritchey and Olson, 1983; Rozin et al., 1991). However, a limitation of these studies is that taste preferences change over the life span (e.g., Beauchamp and Cowart, 1987), and thus studies of parent–child correlations may be at some disadvantage in detecting any genetic differences.

A Bitter Taste Polymorphism and Food Preferences

Some people are able to taste very low concentrations of the bitter compound phenylthiocarbamide (PTC) and its chemical relative 6-n-propylthiouracil (PROP), while other people are much less sensitive to its bitter taste. This taste polymorphism is heritable and is thought to be determined by a single gene, although the gene has not yet been identified (e.g., Merton, 1958; Reed et al., 1995). Several investigators have suggested that nontasters of this bitter substance may have different taste experiences, food habits and food preferences than do tasters (for a review see Drewnowski and Rock, 1995; Anliker et al., 1991; Bartoshuk, 1979; Bartoshuk et al., 1988; Forrai and Bánkövi, 1984; Gent and Bartoshuk, 1983; Glanville and Kaplan, 1965; Hall et al., 1975; Jerzsa-Latta et al., 1990; Looy and Weingarten, 1992; Fischer et al., 1961; Niewind et al., 1988; but see Mattes and Labov, 1989). Overall, tasters of PTC and PROP appear to have more food dislikes than do nontasters (Fischer et al., 1961; Glanville and Kaplan 1965). Therefore, to the extent that a food preference is conferred by this taste polymorphism, it should be heritable. Stable individual differences in the perceived intensity of other bitter compounds have also been reported (Yokomukai et al., 1993); the possible role of these differences, which may or may not be under genetic control, on food choice needs to be examined.

Twin and Family Studies of Macronutrient Intake

The studies described above have attempted to determine the heritability for individual food items, but other studies have focused on overall macronutrient intake. Several studies have compared the nutrient intake over a period of several days for monozygotic and dizygotic twin pairs. Unlike studies of individual food preferences, studies of macronutrient intake almost uniformly show an increased similarity between monozygotic compared with dizygotic twins, and the reported heritabilities are generally higher than those for individual food items (Table II).

Table II.

Twin Studies of Dietary Carbohydrate and Dietary Fat Preferences and Intakes

Macronutrient N (MZ/DZ) 2 (rmz − rdz) Method Reference
Carbohydrate (% energy) 13/10 .67a 3-day food diary Wade et al., 1981
Carbohydrate (% energy) 59/60 .42 3-day food diary Perusse et al., 1988
Carbohydrate (% energy) 106/94 .32 4-day food diary Heller et al., 1988
Carbohydrate (g/day) 13/10 .66a 3-day food diary Wade et al., 1981
Carbohydrate (g/day) 232/223 .62 Food freq. quest Fabsitz et al., 1978
Carbohydrate (g/day) 59/60 .46 3-day food diary Perusse et al., 1988
Carbohydrate (g/day) 109/86 .30 7-day food diary De Castro, 1993
Fat (% energy) 13/10 .48a 3-day food diary Wade et al., 1981
Fat (% energy) 106/94 .24 4-day food diary Heller et al., 1988
Fat (% energy) 59/60 .04 3-day food diary Perusse et al., 1988
Fat (g/day) 232/223 .56 Food freq, quest Fabsitz et al., 1978
Fat (g/day) 109/S6 .30 7-day food diary De Castro, 1993
Fat (g/day) 59/60 10 3-day food diary Perusse et al., 1988
Fat (g/day) 13/10 Not given 3-day food diary Wade et al., 1981
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a

Wade et al., (1981) do not provide r values for twin pairs; these values in this table are obtained from the Holzinger index of heritability and are not directly comparable. Although the method of doubling the difference between MZ and DZ twin r values makes assumptions about heritability which may not be warranted, it does allow direct comparison of the results of different studies.

Studies of family resemblance in macronutrient intake have also demonstrated some evidence for a heritable component but have been handicapped in their reduced power to parse genetic and environmental sources of variance in part because of high spousal correlations for nutrient intake (Oliveria et al., 1992; Pérusse et al., 1988). It is unclear if these high spousal correlations reflect initial assortative mating or a strong influence of shared family environment (for a discussion of this issue see Fabsitz et al., 1978).

Cavalli-Sforza (1990) reviewed family and twin studies of food preferences and concluded, “Food preferences are largely determined by cultural transmission and individual experience. It is hard, however, to exclude genetics entirely” (p. 44). Likewise, Pérusse and Bouchard (1994) concluded that 20% of the variance associated with fat and carbohydrate preference is genetic, and they further concluded that “the literature…indicates a rather moderate role of heredity in energy intake and food preferences” but “a low heritability level does not mean that genes have nothing to do with nutritional habits.” Based on the evidence currently available, we also conclude that for individual food items, genetic heritability is low but that overall macronutrient intakes are more heritable.

CARBOHYDRATE AND FAT PREFERENCE AND THEIR GENETIC DETERMINATION

A detailed description of human studies that provide insight into the genetic basis of carbohydrate and fat preference behaviors is given below. Progress in the use of rodent models to identify genes important in these behaviors is also described.

Relationship of Sweet Taste and Carbohydrate Intake

There are many more published studies examining the genetics of the preference for sweet-tasting carbohydrates than exist for nonsweet carbohydrates, but it would be misleading to extrapolate any observations about the genetics of sweet taste hedonics to complex carbohydrate sources. Sweet taste may or may not be a signal that animals use to make inferences about the carbohydrate content of foods, and it is not known how applicable the results for sweet-tasting items would be for nonsweet carbohydrate sources. In particular, inbred strains of mice show a clear pattern of single-gene mediation of sweet taste preferences, but there is no evidence for or against the hypothesis that the same gene influences complex carbohydrate intake. This is an important caveat to keep in mind when evaluating the subsequent discussion.

Twin and Family Studies on the Genetics of Sweet Taste Sensitivity and Preference

Greene et al. (1975) studied the hedonic evaluation of sucrose, lactose, and sodium chloride solutions by young monozygotic and same-sex dizygotic twin pairs. They reported no heritable component for sucrose preference, although they do report a strong racial difference in the liking for sweet tastes, which may be caused by differences in genes between the populations. (This racial difference in sweet preference was replicated by Bacon et al. (1994)) Krondl et al. (1983) measured the taste recognition thresholds for sweet tastes in monozygotic and dizygotic twin pairs; they reported that the heritability for sweet sensitivity was 0.52, which approached but did not achieve statistical significance. Ritchey and Olson (1983) report that preschool childrens’ degree of liking for sweet foods was not correlated with the degree of parental liking for sweet foods, although this is not surprising, given that children prefer higher concentrations of sweet compared with adults (e.g., Desor et al., 1975). Comparisons between the similarity of monozygotic twin pairs and that of dizygotic twin pairs have revealed no pattern of generic inheritance for sweet-tasting foods (Table I). Human studies of families and twins show little evidence for a genetic influence on sweet taste perception or liking, but it should be pointed out that these types of preference measurements may not be indicative of the food habits of these subjects. Other problems, such as the lack of reliability of food preference questionnaire data, may have hampered investigators in obtaining the most accurate measurement of heritability for individual food items (for a discussion see Allison, 1995).

Bitter Taste Polymorphism May Influence Sweet Perception in Humans

Subjects who perceive propylthiouracil as extremely bitter also perceive sucrose to be sweeter and rate it as hedonically less pleasing than do medium propylthiouracil tasters or nontasters (Looy and Weingarten, 1992), perhaps because the extreme intensity of the sweet taste is offensive (Duffy et al., 1995). This observation has not been replicated in some reports. Kang et al. (1967) grouped Korean subjects by whether or not they liked sugar; among the group who disliked sugar, there was a trend toward a higher frequency of nontasters. Likewise, Drewnowski et al. (1997) failed to detect a relationship between the hedonic appreciation of sucrose and the perception of the bitter taste of propylthiouracil.

Individual Variation Provides Weak Evidence for Genetic Variability for Sweet Taste Perception in Humans

Substantial individual variation in humans’ hedonic response to sweet has been observed; Thompson et al. (1977) categorized subjects into one of two types, based on their reaction to a series of sucrose concentrations. Type I subjects had a rise, and then a decline, in liking for sucrose as the concentration increased; Type II subjects had a rise in the liking for increasing concentrations, and as the concentration rose higher, there was a plateau rather than a decrease in pleasantness ratings. In summing up the food habits of humans with regard to sweet food, Meiselman (1987) has remarked on the extreme degree of individual variation in sweet preferences. Pangborn (1980) also writes, “It is well recognized that subjects differ widely in affective responses to sweetness…, no doubt due to variation in sensitivity, and in cognitive and experiential factors.” Likewise, Witherly and Pangbom (1980) observe that large within-group variation overshadowed between-group differences when obese and lean adults gave hedonic rating for sweet stimuli. Faurion (1987) tested human subjects for their sweetness recognition thresholds or their perceived intensity of sweet-tasting stimuli and concluded that variance among individuals is small compared with variability within individuals. There is diversity in the hedonic and sensory experience of humans to sweet tastes; some of this diversity may be genetic in origin, but most studies designed to demonstrate heritable variation in sweet sensitivity and preference in humans have been negative.

Just as one should be cautious about extrapolating from sweet carbohydrate sources to complex carbohydrate sources, one should be cautious about generalizing results using sweet, noncaloric compounds. There has been little examination of the genetic contribution to the liking for noncaloric sweeteners in humans, but in rodent models, saccharin is the most widely used compound in studies designed to test the contribution of genes to taste-mediated behaviors. Studies that examine both caloric and noncaloric sweet compounds are valuable in determining how applicable the results of studies that use saccharin are to the preference for carbohydrate sources.

Sweet Preference in Rodent Models Is Under Strong Genetic Control

Many studies have demonstrated that inbred strains of rodents differ in their preference for saccharin and, furthermore, the liking for saccharin can breed true in outbred strains of rodents; these studies suggest a strong genetic determination of this behavior (Capretta, 1970; Dess and Minor 1996; Hoshishima et al., 1962; Lieblich et al., 1983; Nachman et al., 1959; Overstreet et al., 1993; Pelz et al., 1973; Ramirez and Fuller, 1975; Vartiainen, 1967). Fuller (1974) attempted to understand and describe the inheritance pattern of sweet intake in the mouse by breeding two inbred strains that differed in saccharin preference. He bred C57BL/6J and DBA/2J mice and described the behavior of the F1, F2, and backcross generations for the avidity with which they drank saccharin. Fuller concluded that an allele of a gene existed in the C57BL/6J strain (Sacb) that conferred an increased “incentive value” to ingested saccharin; the results of his breeding experiments suggested a dominant mode of inheritance for the Sacb allele.

Stockton and Whitney (1974) also investigated sucrose and glucose preferences of several inbred strains of mice and their F1 generations. Inbred strains of mice showed differences in their preference and intake of both sucrose and glucose solutions; for some concentrations of sucrose, the amount of variance accounted for by genes was over 50%. The sucrose preferences of the F1 mice were between the high- and the low-preferring strains for some concentrations and resembled the high sucrose-preferring strain for other concentrations, suggesting an additive or dominant mode of inheritance. Glucose preference yielded lower levels of heritability compared with sucrose preference; glucose is less sweet than sucrose to humans at similar concentrations and the lower heritability values of glucose may be a result of this attenuated sweet taste.

Identification of Genes that Can Influence Sweet Preference and Intake

Lush (1989) furthered this line of research substantially by confirming the existence of the Sac locus; mice from the high and low preference strains were mated, then the F1 progeny were backcrossed to the low saccharin-preferring strain. All of the resulting mice fell into two groups (likers and nonlikers) based on their intakes of acesulfame (a high-intensity, nonnutritive sweetener) and saccharin.

To try to localize the gene, Lush examined the backcross progeny for linkage between saccharin preference and coat color and found no linkage between the brown (b) locus on chromosome 4 or the dilute (d) locus on chromosome 9. A cluster of genes that are thought to be important in bitter taste perception map to chromosome 6 in the mouse. Lush compared the strain distribution pattern of recombinant inbred (RI) mouse strains (originating from C57BL6 and DBA strains; BXD) that avoided bitter with the strain distribution pattern of mice who avoided saccharin and found that they were quite different, which ruled out the bitter taste gene cluster on chromosome 6 as the location of the Sac gene.

The Sac locus, as described by Fuller (1974), was first mapped to the distal portion of mouse chromosome 4 by measuring the saccharin preference of 19 strains of BXD RI mice (Phillips et al., 1994); this location was confirmed by BXD RI mapping and genotyping of backcross progeny from strains of mice high and low in sweet preference (Lush et al., 1995). Subsequently, Bachmanov et al. (1996) have mapped the Sac locus to a region near the microsatelite marker D4Mit42 using the F2 generation of strains from a high saccharin-preferring strain (C57BL/6) and a low saccharin-preferring strain (129; D4Mit42 is 81 cM from the centromere). A preliminary report from Blizard et al. (1996) also suggested that the Sac locus maps very near D4Mit42.

Some inbred strains of mice find the amino acid D-phenylalanine(D-Phe) to be sweet, while other strains do not (reviewed by Ninomiya and Funakoski, 1993). Subsequent breeding experiments of tasters and nontasters of D-Phe sweetness and their F1 and F2 generations suggested that a single genetic locus largely determined this phenotype (dpa). Linkage tests using coat color as a marker suggested that the dpa locus mapped close to the b (brown) locus on chromosome 4.

Because the Sac locus and the dpa locus both influenced the preference for sweet substances, it was unclear whether they represented alleles of the same gene or whether Sac and dpa were distinct genes, each with two or more alleles. Capeless and Whitney (1995) attempted to resolve this issue by testing five inbred strains of mice for their preferences for D-Phe and saccharin. They concluded that if Sac and dpa loci are allelic, then at least three alleles exist, but they did not rule out the possibility that two independent loci, each with two alleles, could also account for their observations. Subsequent linkage studies by Bachmanov et al. (1996) have resolved this issue and have tentatively placed the dpa locus near D4Mit4 (13.6 cM) and the Sac locus as a separate locus, about 60–70 cM distal to dpa on mouse chromosome 4 (see above).

Other investigators have phenotyped F2 animals or measured the amount of sweet solutions drunk by mice from RI strains and have mapped several other chromosomal regions which cosegregate with sweet preference (Table III).

Table III.

List of Loci Linked to Sweetness Preferencea

Species Chromosome Locus Position (cM) Tastant Reference
Mouse 1 D1 Mit5 32.8 Saccharin Phillips et al., 1994
Mouse 1 Mylf; D1Byu1 34.1 Saccharin Phillips et al., 1994
Mouse 3 D3Mit5 23.3 Saccharin Phillips et al., 1994
Mouse 3 Amy1, 2 50.0 Saccharin Belknap et al., 1992
Mouse 3 Pmv39 53.1 Saccharin Belknap et al., 1992
Mouse 3 Fabpi 55.0 Saccharin Belknap et al., 1992
Mouse 3 cdm 64.7 Saccharin Belknap et al., 1992
Mouse 3 Pmv26 75.0 Saccharin Belknap et al., 1992
Mouse 4 D4Mit4 13.6 Sucrose Bachmanov et al., 1996
Mouse 4 Pmv30 16.1 Saccharin Belknap et al., 1992
Mouse 4 Xmmv8 20.5 Saccharin Belknap et al., 1992
Mouse 4 Ly-32g (Cd72) 22.5 Saccharin Belknap et al., 1992
Mouse 4 Lyb-2h (Cd72) 22.5 Saccharin Belknap et al., 1992
Mouse 4 Lyb-2 (Cd72) 22.5 Saccharin Belknap et al., 1992
Mouse 4 D4Mit42 81.0 Sucrose Bachmanov et al., 1996
Mouse 4 Tel4q 81.5 Saccharin Phillips et al., 1994
Mouse 4 Tel4q 81.5 Saccharin Lush et al., 1995
Mouse 4 D4Smh6b 82.0 Saccharin Lush et al., 1995
Mouse 4 D4Bir1 82.5 Saccharin Phillips et al., 1994
Mouse 6 Hoxa 25.5 Saccharin Belknap et al., 1992
Mouse 6 Ggc 26.0 Saccharin Belknap et al., 1992
Mouse 8 Xmmv29 60.0 Saccharin Phillips et al., 1994
Mouse 9 Gnat1 59.0 Saccharin Belknap et al., 1992
Mouse 9 Bg1 66.0 Saccharin Belknap et al, 1992
Mouse 12 D12nyu1 23.0 Saccharin Belknap et al., 1992
Mouse 13 D13Mit9 41.0 Saccharin Phillips et al., 1994
Mouse 13 Rasa 45.0 Saccharin Phillips et al., 1994
Mouse 13 As1 48.0 Saccharin Phillips et al., 1994
Mouse 13 Lth1 52.0 Saccharin Phillips et al., 1994
Mouse 13 D13Bir1 57.5 Saccharin Phillips et al., 1994
Mouse 15 Pmv42 70.5 Saccharin Belknap et al., 1992
Mouse 18 D18Mit14: Grl1 18.0 Saccharin Phillips et al., 1994
Drosophila 93B6 mv1 3–[70] Sucrose, fructose Rodrigues et al., 1995
Drosophila 13F sd 1–51.5 Sucrose Inamdar et al., 1993
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a

For the mouse genome, all distances are given in cM from the centromere and all locus names reflect revised information from the Mouse Genome Database maintained at Jackson Laboratories, as of July 1996. Information on the Drosophila genome was extracted from FlyBase (http://cbbridges.harvard.edu:7081).

Rodrigues et al. (1995) reported a Drosophila mutant, malvolio, which has an unusual response to sweet tastes in that adult mutant flies do not show a preference for sugar. The gene in the fly has been cloned and the mouse homologue of this gene is Nramp1, which maps to mouse chromosome 1 [39.2 cM (Mouse Genome Database July 1996)]. At least one report has suggested that a locus in this vicinity of mouse chromosome 1 may influence saccharin intake [D1Mit5; 33 cM (Phillips et al., 1994)]; these two observations suggested that Nramp1, as well as the Sac and dpa loci, may participate in the genesis of saccharin preference in the mouse.

Likewise, the scalloped locus in Drosophila, when mutated, produces flies which are nonresponsive to sucrose. The scalloped locus encodes a protein which binds DNA; the gene homologue in mice (Tcf13) and in humans (TCF 13) has been sequenced but not mapped (Blatt and DePamphilis, 1993; Xiao et al., 1991). Because the map location of this gene is currently unknown, it is unclear whether this gene could be equivalent to the Sac or dpa locus. The sensory neurons in both the malvolio and the scalloped mutants appear to be normal, and therefore the defect leading to the behavioral differences is thought to occur after the initial sensory transduction. Neither of these loci are likely to be the homologues of the Sac or dpa locus in the mice, however, because Bachmanov et al. (1996) have evidence to suggest that alleles of the Sac and dpa loci alter the peripheral sensory neurons’ response to sucrose.

Dietary Fat Preference Is Heritable in Mice and Rats

The genetics of sweet taste preference is well studied compared with the scant number of studies that have assessed the role of genetic variability in dietary fat preference. Clearly, there is evidence for a heritable component to human dietary fat intake (Table II), but it is less strong than the evidence for carbohydrate preference. Furthermore, there is much disagreement among studies concerning the strength of genes compared with the strength of environment and experience; estimates of heritability range from 0.04 to 0.56. Studies in rodent models have yielded more homogeneous results, but the literature is not as well advanced as that for sweet taste preference. No major gene effects have been described, no mapping studies of genetic loci have been published, and no single-gene mutants with unusual phenotypes with regard to dietary fat preferences have been discovered.

The role of genes in the preference for dietary fat has been studied by comparing the differential rate of body weight gain in strains of inbred mice and rats fed a high-fat diet (Fenton and Dowling 1953; Okada et al., 1992; Rothwell et al., 1982; Schemmel et al., 1970, West et al., 1992, 1995). Rodents gaining more weight while fed a high-fat diet may be consuming more of the diet or they may eat similar amounts of the diet compared with rodents gaining less weight but retain more of the diet as stored carcass energy. Schemmel et al. (1970) measured the intake of the high-fat diet and demonstrated that one strain of inbred rats ate twice as much of a high-fat diet and become much fatter compared with other strains. Larue-Achagiotis et al. (1994) measured the self-selection of macronutrients by an inbred strain of rats (Dark Agouti) compared with an outbred strain of rats (Wistar) and reported large strain differences in dietary fat intake. Likewise, Smith et al. (1997) have demonstrated that one strain of mice (AKR/J) consumed roughly three times more fat than did another inbred strain of mice (SWR/J).

INTERACTION BETWEEN NUTRIENT PREFERENCE AND OBESITY IN RODENT MODELS AND HUMANS

Substantial progress has been made in the characterization of the molecular genetics of sweet preference, but the increased preference for sweets is not associated with an obese phenotype. Although the liking for sweets is popularly held to be a significant cause of obesity, in fact, the opposite relationship is observed.

Sweet Preference Is Not Associated with Obesity in Rodents or Humans

Epidemiologic evidence strongly suggests that the more sugar individuals consume as a percentage of their total calories, the lower their body weight (reviewed by Hill and Prentice, 1995). The bulk of the studies reviewed by Hill and Prentice rely on self-reported food intakes and are, therefore, less reliable than measured intakes; nevertheless, the large sample sizes in some studies and the agreement between studies support this conclusion.

Rodent models also support a reciprocal relationship between obesity and sucrose intake. For instance, sucrose licking rates are negatively correlated with body weight in a genetically heterogeneous group of rats; the more rats “liked” sucrose (as measure by lick rate), the more likely they were to be leaner (Ramirez, 1977). Ramirez and Sprott (1979a) demonstrated that mice with mutations of the obese gene (ob/ob) drank less sucrose-sweetened liquids compared with their lean littermates, and so did obese mice with mutations of the agouti gene (Ramirez and Sprott, 1979b); other investigators have described the decreased consumption of a sweet carbohydrate source in a macronutrient self-selection experiment by genetically obese mice compared with lean mice of the same strain [ob/ob (Romsos and Ferguson, 1982)]. Sclafani and Assimon (1985) selectively bred rats to be prone to either obesity or leanness; when offered a diet high in fat, obesity-prone rats ate more food and gained more weight than leanness-prone rats, but when the rats were offered a sucrose-based diet, obesity-prone rats ate less than did the leanness-prone rats. Similarly, an inbred mouse strain with a propensity to develop dietary obesity (AKR), preferred saccharin much less than did an inbred strain of mice resistant to dietary obesity (SWR) (Smith et al., 1997; Lush, 1989; West et al., 1992, 1995).

An interesting exception to the observation that obese rodents avoid sweets compared to their lean littermates comes from work done recently by Ninomiya et al. (1995). Ninomiya and his colleagues report that mice with mutations of the diabetes gene (db/db) show an increased preference for sugars. In related experiments of taste nerve function, the chorda tympani nerves of the db/db mouse were more responsive to sugars compared with littermates homozygous for the wild-type allele. This work was completed prior to the identification and description of the db gene (Tartaglia et al., 1995) and it is difficult to reconcile the function of the gene (a receptor for the newly discovered leptin protein), with these observations.

In humans, many studies have been undertaken to discover whether obese individuals have a heightened preference, liking, detection, or recognition threshold for sweet-tasting food and drinks. Most studies do not support differences in these variables between obese and lean human subjects (Drewnowski et al., 1991; Malcolm et al., 1980; Thompson et al., 1977; Witherly et al., 1980; but see Rodin et al., 1976; Warwick and Schiffman, 1990; for a review of the older literature see Grinker, 1978). The balance of the literature in both rodent models and human subjects suggest that, overall, increased preference for sweet-tasting foods and fluids is associated with leanness, rather than obesity.

Carbohydrates, particularly sweet carbohydrates, were previously identified as a nutritional culprit in the development of obesity, but controlled experiments have not borne this relationship out. Dietary fat has replaced sucrose in both the popular and scientific arenas as the nutrient most likely to lead to obesity if overconsumed. The preference for dietary fat, its genetic determinants, and its role in the development of obesity are reviewed below.

Fat Preference Is Associated with Obesity in Humans

Obese humans consume a higher percentage of their diet as fat compared with lean humans (for a review see Hill and Prentice, 1995); obese subjects also generally report liking high-fat foods more than do lean subjects (Drewnowski et al., 1985; Mela and Sacchetti, 1991; but see Pangborn et al., 1985). As reviewed above, twin studies suggest a modest, heritable component for dietary fat intake (Table II), but few studies have tried to address the specific genetic contributions to dietary fat intake or fat preference. The measurement of fat preference is a difficult subject to study because, unlike sweet preference, the salient sensory attributes of fat are not known.

Drewnowski (1992) has suggested that different sensory profiles for the preferences for high-fat foods might distinguish subtypes of obesity. Drewnowski et al. (1991) divided obese subjects into two groups: those who developed obesity early in life and those who developed obesity as an adult. The logic for this division is based on an earlier report showing that the familial risk of obesity increases when obesity is evident earlier in life (Price et al., 1990). Drewnowski reported no differences in fat preferences between adults who had early-and those who had late-onset obesity and he concluded that people with a high familial risk for obesity do not have different preferences for dietary fat than do obese people with a tow familial risk of obesity. This interpretation may be questioned, however, because the presence of familial obesity in the first- or second-degree relatives of the early-onset obesity patients studied was not established.

Heitmann et al. (1995) studied weight gain and dietary fat intake of adult women who differed in their familial predisposition to obesity. A high dietary fat intake was associated with subsequent weight gain in women with a family history of obesity, compared with women with no family history of obesity. Interestingly, dietary fat intake was a predictor of the development of obesity for women who were initially lean, but only if they had obese family members. The results of this study suggest that a high preference for dietary fat can precede the development of obesity in genetically susceptible women.

Another line of investigation that may shed light on the genetic contribution to dietary fat preference is the examination of genetic disorders in humans. There are several genetic disorders that have obesity as a cardinal feature (Reed et al., 1995). The most well-known of these is Prader–Willi syndrome, which is caused by the inactivation of paternal genes on chromosome 15ql1-13 (Nichols et al., this issue). Rankin and Mattes (1996) tested the food preferences of subjects with Prader–Willi syndrome and compared their ratings with age- and sex-matched control subjects; overall, food preferences were similar between the two groups, although subjects with Prader–Willi syndrome tended to prefer foods high in fat. The food and taste preferences of subjects with other genetic syndromes involving obesity as a cardinal feature have not been studied; likewise, no genetic syndrome with a high dietary fat preference as a cardinal feature has been reported. Patients with elevated glucocorticoid levels (Cushing’s disease) prefer dairy products higher in fat than do normal-weight or healthy obese subjects (Castonguay, 1991), suggesting that individual variation in plasma glucorticoid levels may influence dietary fat intake.

Links among bitter taste perception, fat preference, and obesity have been established. Women who perceive the taste of concentrated PROP as intensely bitter (supertasters) have lower body mass indices (kg/m2) than do women who are medium or nontasters (Lucchina et al., 1995). The texture of milk products containing fat was perceived as more creamy by supertasters; moreover, supertasters were less likely to consume or have a preference for foods high in fat (Dabrila et al., 1995; Duffy et al., 1995; Lucchina et al., 1995). It thus appears that the genetically determined ability to taste one class of bitter substances extends to differences in the perception of dietary fat; subjects who are heavier are less sensitive to the textural cues provided by dietary fat and are less likely to be sensitive to the bitterness of PROP. The gene that determines this bitter taste polymorphism may either have effects on both dietary fat perception and body weight or be linked to genes contributing to these phenotypes.

Dietary Fat Is Preferred by Genetically Obese Rodents but Is Not Required for the Development of Obesity

Alleles of five genes in rodents have each been shown to be sufficient to cause obesity on an otherwise normal genetic background (Avy, ob, db, and fa, its homologue in the rat, fat, and tub). Over the last 4 years, all of these genes have been identified and described (Bultman et al., 1992; Chua et al., 1996; Kleyn et al., 1996; Lee et al., 1996; Naggert et al., 1995; Noben-Trauth et al., 1996; Tartaglia et al., 1995; Zhang et al., 1994). We know from studies conducted prior to the cloning of these genes that mice and rats with mutations of the ob and fa genes overconsume fat relative to lean littermates (Castonguay et al., 1982, 1984, 1986; Ramirez and Sprott, 1979a; Romsos et al., 1982 but see Maggio et al., 1984; Enns and Grinker, 1983). Mice with an allele of the agouti gene (Avy) do not prefer dietary fat more than lean mice of the same strain (Ramirez and Sprott, 1979b; but see Rytand, 1943).

When genetically obese mice are fed a high-fat diet, it exacerbates the development of obesity [ob (Fuller and Jacoby, 1955), fa (Lemmonier et al., 1974; Zucker and Zucker 1962), ob (Mayer et al., 1951), Avy (Carpenter and Mayer, 1958)]. When offered a fat-free diet to eat, mice with the ob/ob genotype become fatter than mice with the wild-type allele, but the presence of as little as 5% of calories as fat in the diet greatly increases the difference between lean and genetically obese mice (Genuth, 1976). The results of these studies, coupled with the observation that mice with mutations in the tub and fat genes become obese when fed a low-fat, standard mouse diet (Coleman and Eicher, 1990), suggest that the obesity genes studied so far do not depend on the presence of dietary fat for the expression of the phenotype. The preference for dietary fat in these genetic models may be generated by metabolic perturbations associated with the particular genetic lesion and are most likely not due purely to the hedonic appreciation of dietary fats’ physical properties (Reed et al., 1992).

CONCLUSIONS

There is good evidence to suggest that obese humans are likely to prefer and ingest more dietary fat and less sucrose than are lean humans; evidence also exists to, suggest that this increased liking for fat and disliking for sucrose may be genetically mediated. Studies of inbred strains of mice are currently in progress to map genes associated with the differential ingestion of sweet carbohydrates and fat, and the genes identified should provide important clues about the biology of dietary obesity.

Acknowledgments

The assistance of Dolly Vargesee, Claudia Vaughn, Elizabeth Joe, and Andrew Krakowski in obtaining reference material is gratefully acknowledged. This work was supported by grants from the St. Luke’s/Roosevelt NY Research Center to D.R.R. and Grants NIH-ROI-DK-44073 and NIH-ROI-DK48095 to R.A.P. and NIH ROI-TC-00882 to GKB. The advice of David West and Linda M. Bartoshuk enhanced the quality of this work.

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