Appetite for the Selfish Gene

Appetite 54 (2010) 442–449

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Appetite journal homepage: www.elsevier.com/locate/appet

Research review

Appetite for the Selfish Gene§ Iztok Ostan a,*, Borut Poljsˇak b, Marjan Simcˇicˇ c, L.M.M. Tijskens d a

Faculty for Maritime Studies and Transportation, University of Ljubljana, Pot pomorsˇcˇakov 4, 6320 Portorozˇ, Slovenia University College of Health Studies, University of Ljubljana, Poljanska 26a, 1000 Ljubljana, Slovenia Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia d Horticultural Supply Chains, Wageningen University, Droevendaalse steeg 1, 6708 PD Wageningen, The Netherlands b c

A R T I C L E I N F O

A B S T R A C T

Article history: Received 29 October 2009 Received in revised form 30 January 2010 Accepted 29 March 2010

In developed countries, where the majority of the population has enough income to afford healthy diets, a large number of the inhabitants nevertheless choose unhealthy nutrition. WHO and FAO strategies to overcome this problem are mostly based on educational means. Implicitly, this approach is based on the presumption that the main causes of the problem are ignorance and culturally acquired bad habits. It has already been shown that wild animals, evidently acting solely on instinct without cultural effects, display tendencies that may damage their longevity: they tend to avoid healthy types of caloric restriction, prefer processed to raw food, and have an excessive intake of food stimulants and proteins when available (Ostan et al., 2009). This paper presents evidence for such nutritional patterns in humans as well and broadens the discourse to include proteins and fats and describes some human biological traits that present important differences between humans and other primates; among them are the human tendency for overeating and the inadequacy of a totally raw diet for human consumption (despite having some advantages for the human immune system). From an evolutionary perspective these strategies offer a biological advantage by enhancing the reproductive capability of the organisms, according to Dawkins’ theory of the Selfish Gene. Genomic-based pleasure of such nutrition seems to be the main cause of instinctive nutritional drives. Further research on the process of food acceptance is needed to determine the role and importance of genomic-based pleasure compared to epigenetic or culture-based pleasure. Both, however, seem to be important and very stable factors in human nutritional choice and seem to prevail over conscious factors in food acceptance. ß 2010 Elsevier Ltd. All rights reserved.

Keywords: Ethology Nutrition Caloric restriction Processed food Stimulants Protein consumption Nutritional pleasure Reproduction Health Longevity

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Unhealthy nutrition: involvement of genes? . . . . . . . . . . . . . . . . . . . . . . . . . . . . Environmental influences encoded through the epigenetic system . . . . . Genomic-based individual behavioural differences. . . . . . . . . . . . . . . . . . Genomic-based general human behaviour . . . . . . . . . . . . . . . . . . . . . . . . The instinctive drive for satiety and overeating . . . . . . . . . . . . . . . . . . . . . . . . . . The instinctive tendency for fast/easy food . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The role of pleasure in human food acceptance. . . . . . . . . . . . . . . . . . . . . . . . . . Examples of nutritional pleasure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pleasure by eating of food stimulants . . . . . . . . . . . . . . . . . . . . . . . Pleasure by consuming protein rich food . . . . . . . . . . . . . . . . . . . . How important is (genomic-based) pleasure in food acceptance? . Discussion: a need for an enlarged paradigm?. . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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§ This research received no specific grant from any funding agency in public, commercial or not-for-profit sectors. All authors contributed to this manuscript in equal parts. There are no conflicts of interest. * Corresponding author. E-mail address: [email protected] (I. Ostan).

0195-6663/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.appet.2010.03.015

I. Ostan et al. / Appetite 54 (2010) 442–449

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Introduction

Unhealthy nutrition: involvement of genes?

In developed countries, where the majority of the population has enough economic means to afford healthy food, the nutrition of a major part of the inhabitants is unhealthy.1 Let us list just some facts:

Human behaviour (nutritional or otherwise) is not just instinctive, but also a result of reflected choice. That is the main difference between human and animal behaviour. Nevertheless, for humans gene-based behaviour is also important. Genes are involved in different ways in choosing unhealthy nutrition.

In most developed countries about half of the population is overweight (BMI 25 or more), while about one fifth is obese (BMI 30 or more; Seidell & Flegal, 1997). In the developed world ‘‘obesity is a major and increasing health problem’’ (Ravussin & Bouchard, 2000). The problem is increasing in developing countries as well (Taubes, 1998). According to the WHO (1997), the problem of obesity has become ‘‘global epidemic’’. In developed countries the consumption of processed food is too high, while the consumption of fruits and vegetables is too low. According to the WHO and the FAO, a human being should eat at least 400 g of fruits and vegetables per day.2 In most countries (developed as well as undeveloped) the average consumption is below this advised value (FAO & WHO, 2004). Even in countries where the consumption of fruits and vegetables is high by tradition (the Mediterranean region) their consumption has decreased and the diet has evolved ‘‘towards a typical Western diet’’ (Lo´pez-Torres & Barja, 2008). In developed countries the consumption of food stimulants (like caffeine, alcohol and nicotine) is too high. According to Guidelines for Americans 2005 (U.S. DHHS & U.S. DA, 2005) the upper limit of alcohol consumption is 8.25 l of (pure) alcohol per adult person per year (men 11 l, women 5.5 l). In Europe, the alcohol intake exceeds this limit. According to WHO statistics the average consumption of alcohol in the 27 countries of the European Union (2003) is 9.1 l per person (WHO, 2008). These statistics include children and do not include illegally produced and consumed alcohol. So the real level of consumption is above the values mentioned in these reports. The consumption of tobacco products is also problematic. In the European Union, the percentage of regular (every day) smokers is between 16.4% (Portugal) and 34.6% (Slovenia). In more than half of European countries the fraction of every day smokers exceeds a quarter of the population (Eurostat, 2008). All these unhealthy nutritional patterns are risk factors for several diseases like cardio-vascular diseases, cancer, diabetes and others (FAO & WHO, 2004). Health also depends on non-nutritional factors, but that analysis is outside the framework of this paper. Why do people, who have enough income to choose healthier food, behave in a self-destructive way by choosing unhealthy nutrition? That is the central question of this paper. Any research or educational action that has the ambition of directing human nutritional behaviour away from unhealthy nutrition and overeating, should apply proper problem decomposition and discriminate between unchangeable behavioural factors and those that can be influenced (Sloof, 2001). In this paper some evidence is presented to support the hypothesis that an important part of health damaging nutritional behaviour is gene-based and therefore difficult to change. 1 It is well known that the nutrition of the majority of the world population is below the minimal quality standards of WHO (World Health Organization) and FAO (Food and Agriculture Organization). Especially in less developed countries, where the average family may spend up to two third of its budget on food (Bangladesh 64.5%, Sri Lanka 62%; Sˇosˇtaricˇ, 2008), the main cause of this problem is economic restrictions of the majority of population. But in developed countries, where according to OECD statistics the expenses for food present less than 25% of an average family budget (from 9.8% in USA to 21.9% in Spain; Sˇosˇtaricˇ, 2008), the majority of families have enough income to choose healthier, usually more expensive food. 2 In some countries official institutions advise higher minimal consumption of fruits and vegetable; for example the Ministry for Health of Republic of Slovenia (2004) advises from 400 to 650 g per day.

Environmental influences encoded through the epigenetic system Persistent individual differences in preferences may come from differences in habits acquired mostly during childhood. Recent research shows that these environmental impromptus also go through the mediation of genes: the structure of genes does not change in this case, but the state of activation of the genes does. This so-called epigenetic mechanism uses different substances to silence or to activate genes by adding or removing certain groups in complex molecules. The most known among these is the methyl group. ‘‘The carbon–carbon bond between the methyl group and the cystine residue is a stable, enduring ‘epigenetic’ mark’’ (Meaney & Szyf, 2005); that was ascertained in studies on the effects of maternal care on gene expressions in rat off-springs (Caldji, Diorio, & Meaney, 2000; Francis, Diorio, & Liu, 1999; Weaver, Cervoni, & Champagne, 2004). Many studies confirm the epigenetic effects of food (Dahlman, Linder, & Arvidsson Nordstro¨m, 2005; Kallio et al., 2007), physical exercise (Buttner, Mosing, & Lechtermann, 2007; Connolly, Caiozzo, & Zaldivar, 2004; Zieker, Fehrenbach, & Dietzsch, 2005) and other psycho-physical factors (Ornish, Magbanua, & Weidner, 2008). Epigenetic information received in childhood usually persists through the lifetime of an individual and is even biologically passed on to the next generation through a non-genomic way of inheritance (Caldji et al., 2000; Francis et al., 1999; Meaney & Szyf, 2005; Weaver et al., 2004). This mechanism has been asserted not only in humans and other mammals, but also in reptiles (Weaver et al., 2004), insects and even in plants (Agrawal, Laforch, & Tollrian, 1999). It is thus an instrument developed through ‘‘natural selection’’ (Francis et al., 1999) for a better adaptation of descendents to the environmental conditions that parents are coping with. This mechanism made it possible for humans to develop very different nutritional habits in different habitats (in a geographic, cultural sense). The epigenetic system also enables organisms to tune the nutritional behaviour to the required amount of food. In an environment with food shortage; children (and pups) will probably tune their threshold for satisfaction slightly below the normal level of energetic requirement, while the food abundance in today’s ‘‘obesigenic environment’’ (Ravussin & Bouchard, 2000) will result in an epigenetic increase of the individual limit for food satisfaction. It is possible to change in adulthood behavioural patterns fixed in childhood by epigenetic mechanisms. One-way is a persistent training of new (healthier) nutritional habits and lifestyles. It has been shown experimentally that having a different nutrition and lifestyle for only some weeks changes markers of more that 500 genes (Ornish et al., 2008). But the drive of old habits is strong and the majority of the adult population is reluctant to change. Another way of changing epigenetic markers is by using chemical substances that reverse the methylation mark. It has been shown for animals that markers acquired in childhood with a type of maternal care (licking or non-licking of pups) can be reversed in adulthood through the changing of epigenetic marks by chemicals. The results are behavioural and physiological patterns, typical for offspring that had the opposite type of maternal care in childhood (Meaney & Szyf, 2005). This type of treatment has not been tested on humans since it poses many ethical questions.

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Genomic-based individual behavioural differences The genome of each individual is unique. Human genomic diversity seems to increase: during the last tens of thousands of years humans have experienced an acceleration of evolution and a genetic divergence (Hawkes, Wang, & Cochran, 2007). Thus, in addition to the general human tendencies, described in next sections, part of the human population could prefer unhealthy nutrition because of specific genomic features. There are even individuals that crave for too much food because of ‘‘metabolic defects’’ of genes caused by mutations (Ravussin & Bouchard, 2000). A medical approach is needed to face this type of problems. Genomic-based general human behaviour It seems that genomic-based tendencies for unhealthy nutrition are common to a large part of the human population. A direct proof for such tendencies would be the specification of genes that promote such behaviour. This type of evidence, however, is not yet available. Therefore, two methods will be used, typical for human ethology; i.e., the science of human instinctive behaviour: cross cultural comparison and comparison of general human behaviour to animal behaviour, particularly to apes and other primates. Since neither method provides certainty that the investigated similarities in behaviour are biologically based, evidence will be presented for a common physiological basis of investigated similarities in human and animal nutrition behaviour. The instinctive drive for satiety and overeating To understand the instinctive drive for overeating in humans it is useful to look first to the tendency for satiety in animals. Studies performed on different species show that eating less then normal (at least from time to time) is beneficial for health and longevity (Ostan, Poljsˇak, Simcˇicˇ, & Tijskens, 2009 and references cited there). However instinctive mechanisms prevent the organism from doing just that. Restrictions on caloric intake produce stress hormones (Mattson, Duan, & Wan, 2003), inducing bad feelings that are part of the feeling called ‘‘hunger’’. Fasting selectively increases activation of the brain ventral stratum, amygdale, anterior insula, and medial and lateral orbitofrontal cortex (Goldstone et al., 2009). So animals are instinctively pushed toward a higher caloric intake. This apparently senseless selfdestructive nutritional behaviour is evolutionarily important: a higher (normal) level of caloric intake enhances fertility and sexual maturation (Gredilla & Barja, 2003; Missirlis, 2003). There is a logical explanation for the high energetic cost of reproduction. DNA is a very stable molecule (Watson & Berry, 2003/2007), more stable than other macromolecules (proteins, lipids). A lot of energy is therefore needed for DNA division and consequently for the division of the entire cell in animals, plants and humans alike. Undernourishment delays the onset of puberty (Olshansky & Carnes, 2001) and causes a ‘‘negative psychological and behavioural sequel’’ (Polivy, Herman, & Coelho, 2008). On the other hand, caloric restriction (without undernourishment) seems to have a positive effect on longevity as well. Only a few clinical studies on the effects of caloric restriction on humans have been reported. In a 6 month trial of 48 participants, the ‘‘findings suggest that two biomarkers of longevity (fasting insulin level and body temperature) decreased via prolonged caloric restriction in humans. . .Studies of long duration are required to determine if caloric restriction attenuates the aging process in humans’’ (Heilbronn, deJonge, & Frisard, 2006). Research on members of the Calorie Restriction Society (range 35–82 years) who have been for about 6.5 years on a diet, restricted in calories (about 30% compared to control individuals) ‘‘showed many of the

same alterations in metabolic and organ function previously reported in calorie-restricted rodents (. . .); in addition, left ventricular diastolic function (. . .) was similar to function in those who were approximately 16 years younger’’ (Fontana & Klein, 2007); Other studies seem to support the thesis of positive effects of caloric restriction on longevity in humans (Heilbronn & Ravussin, 2005; Holoszy & Fontana, 2007; Meyer, Kova´cs, & Ehsani, 2006; Redmann, Martin, & Williamson, 2008). Similar effects of caloric restriction could be explained by the processes of energy metabolism at the cell level, which is very similar in all humans and (other) animals. The main problem is not energy production itself, but the oxidative stress connected to it. Not only animals (including humans) but even yeasts undergo similar processes of intracellular oxidation. Some research results ‘‘indicate that yeasts are good model organisms for studying intracellular oxidation and oxidative stress’’ (Raspor, Plesnicˇar, & Gazdag, 2005). The main source of free radical production in all animals (humans included) is the mitochondrial electron transport chain. In this process, about 1–3% of the oxygen consumed is converted into superoxide radicals. Caloric restriction reduces this primary source of free radicals (Halliwell & Gutteridge, 2005). So, humans have in common with other animals, a physiology that causes positive effects of caloric restriction on health and longevity. But specific for the human species seems to be that calorie restriction has only minor effects on maximal lifespan. The increase in human longevity could be in a range of 2.1–6.8% of the total lifespan (calculation based on demographic data of Japanese population); for mice, caloric restriction could increase longevity much more, up to 67.5% of the average longevity ad libitum feeding levels (Phelan & Rose, 2006). From a longevity point of view, eating just a normal quantity of food every day is, therefore, already overeating. There are animal species that tend to eat more than is necessary for maintaining their normal body mass. Among them are humans. For species that depend on seasonal variation in food availability (squirrels, dormice, bears. . .) or on uncertainty of hunt success (wolfs, lynxes. . .), it is natural to eat more than required when food is available. They produce body fat deposits that are used up in time of food shortage. Thus, in normal life conditions, wild animals maintain on average a normal body mass. But in conditions of continuous food abundance instinct leads these animals to persistent in overeating. Experts estimate that today already 50% of dogs and cats have an increased body weight (Vidic, 2008). That is more or less the same overweight percentage as in the human population in developed countries. Overweight dogs and cats face an increased risk of contracting health problems like diabetes, heart diseases, skin and joint problems and others (Vidic, 2008) just like overweight humans (Zaletel Vrtovec, 2006). Being overweight causes therefore an additional decrease of life span expectancy (Zaletel Vrtovec, 2006). A specific feature of humans (and other animal species that tend to overeat) is that appetite does not cease when individuals ingest enough food to satisfy the normal daily energy requirements (Horrobin, 2001); appetite persists until the sensation of ‘‘fullness’’ (Murray & Vickers, 2009) is reached (satiety). In this point, humans are biologically different from other primates. The human organism is more capable of transforming nutrients into fats and has, at normal body mass, more body fat deposits than other primates (Horrobin, 2001). Based on the neural structure of emotions, evolutionary psychologists assert that we are born with a genetic structure efficient during the last million years or more (Goleman, 1999, p. 19). So, humans are to a great part still adapted to the diet of their hunter-gatherer ancestors. Our ancestors developed during millions of years of life in the uncertain conditions of the savannah, the ability to eat more then necessary and store more bodily energy reserves (Burgoine et al., 2009; Watson & Berry, 2003/2007).

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So, genomic-based overeating seems to be a special form of a more general genomic-based tendency for satiety. In a natural environment with a regular succession of periods of food abundance and food shortage, periodical overeating enables normal reproduction. But in conditions of continuous food abundance ‘‘human biology has become out of step’’(King & Thomas, 2007); this natural drive can impair, in addition to health, reproductive capabilities (Zaletel Vrtovec, 2006). The instinctive tendency for fast/easy food To understand why all human societies tend to consume more processed (grinded, cooked, refined) food, avoiding raw fruit and vegetables, it is useful to look at preferences of wild animals that were not adapted to any degree to processed food. Great apes also prefer cooked food to raw food (Wobber, Hare, & Wrangham, 2008), and many other wild animals are fond of cooked food as well. Different types of food processing (grinding, cooking) permit an easier and faster acquisition of energy (Boback, Cox, & Ott, 2007; Ostan et al., 2009 and references cited there). Also it has been illustrated (Ostan et al., 2009) that cooking (this term is used here for all types of heat treatment of food) destroys some types of micronutrients and even produces carcinogenic substances (reviewed in Ostan et al., 2009; Rajar, Gasˇperlin, & Zˇlender, 2006). This negative impact of cooked food on health does not prevent animals from eating it. The degenerative effects usually occur over a long-term, after the age of reproduction. Thus, for animals, it is an evolutionary advantage to consume health damaging cooked food: a faster absorption of energy permits faster reproduction. In many cases, the nutritional effects on humans are similar to the effects on animals. But humans have some specific metabolic features. Our ancestors were the first to introduce the systematic consumption of cooked food, so our species had more time to adapt to cooked food than most animal species. Have we, however, adapted enough to cooked food to be free from its negative health effects? There is a long human history of using fire in food preparation. It is widely accepted that our ancestors began to cook at least 250,000 years ago (Ragir, 2000). There are, however, different opinions with respect to the degree of genetic adaptation of humans to this type of prepared food. Some studies claim that human biology has not yet had time enough to adapt to modern human diets such as cooked food (Milton, 2002). But there are also quite opposite theories. According to Wrangham and his collaborators the ‘‘oldest date suggested for the adoption of cooking is 1.9 millions years ago’’ (Wrangham & Conklin-Brittain, 2003). They suggest that the earliest impact of cooking was a reduction of teeth and jaw size that accompanied the evolution of Homo ergaster approximately at that time. Another effect of cooking was the genetically based change in gut size and gut passage rate (Wrangham & Conklin-Brittain, 2003; Wrangham, Holl& Jones, & Laden, 1999). However, many scientists claim that 5000 years of a new diet or even less is long enough to affect human biology at least to some degree (Aoki, 1991; Cavalli-Sforza, Menozzi, & Piazza, 1994; Gould, 2002). It is thus quite safe to assume that there has been a shift in the human genome from the times of an all raw diet. All human societies cook food, even the most primitive ones (Wrangham & Conklin-Brittain, 2003). Koebnick and his collaborators (Koebnick, Strassner, & Hoffmann, 1999) studied raw-food eating urban Germans (some of them were vegetarians, while others included raw meat in their diet) who had lived on this type of food for at least 3 years. 18% of them were following an all raw-food diet. About 31% of all raw-food dieters were judged to be suffering from Chronic Energy Deficiency, while approximately 50% of women on

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an all raw diet were completely amenorrheic. Individual humans can still thrive on all raw food, but their reproductive functions are seriously weakened. Beside this, it is notoriously true that children, who act more instinctively than adults, prefer candies and sweets to their sweet alternatives - fruits. They act like that all over the world, even in remote cultures that traditionally eat a lot of fruits and usually consume a great portion of their food uncooked (Clark, 1957). Research namely shows that from birth on infants show clear preferences for sweet taste (Cowart, 1981) and that children and adolescents (even more than adults) prefer foods that are rich in calories (Sherewood, Story, Neumark-Sztainer, Adkins, & Davis, 2003; Killgore & Yurgelun-Todd, 2005), what sweets and candies are compared to fruits. It cannot, however, be assert that humans have adapted completely to cooked food. There is convincing evidence that sometimes the count of leukocytes increases after ingestion of cooked food (digestive leukocytosis), but not after ingestion of raw food (Kouchakoff, 1930, 1937). After millennia of consuming heat treated food, the human immune system still treats cooked nutrients as ‘‘strange’’ and defends the organism against them by an increased production of defensive cells. The history of human nutrition is somehow the history of more and more processed (fast) food: from grinding before the ‘‘domestication’’ of fire, to cooked food in Palaeolithic and agricultural societies and mostly refined food in the industrialised world. Many animals (not only pets, but seagulls, rats, mice. . .) ‘‘specialise’’ in the consumption of fast food as well, thriving on humans’ litter of processed food. But processed food is not always an evolutionary advantage. It might also produce degeneration in offspring. This ‘‘fast food’’ diet is less adequate for the preservation of the species. At first, humans also experienced a physical degeneration (observed mostly through dento-facial abnormalities) in their passage from huntergatherers’ nutrition to mostly plant-based agricultural nutrition (Larsen, 1998), and in the later development of cooked food from agricultural to industrial nutrition (Price, 1939/1989). But the survival of species would not have been possible if the nutrition would not have been ‘‘tuned’’ in some generations to at least the level of quality that allows the minimal health necessary for normal reproduction. The role of pleasure in human food acceptance Previous section showed that at least from two points of view, animals and humans share common features: (1) There is a physiological nutritional dichotomy: The same food has different effects on reproduction from those on healthy longevity: the nutritional needs for optimal reproduction and for optimal health and longevity are not the same. (2) There is a behavioural nutritional asymmetry: by instinctive impulses, organisms (animals and humans) tend to prefer food that optimises gene reproduction. In instinctive reactions, all choices are based exclusively on emotions: ‘‘Instinctive impulses. . .are directed to immediate and unconditioned satisfaction. . .The behaviour is totally subordinate to the principle of delight’’ (Musek, 1993). Food that produces bad feelings (has a bad smell or taste, causes pain. . .) is repulsive to animals, while food that produces pleasure attracts them. Anthropologists stress the evolutionary importance of pleasure: ‘‘Like the enjoyment in food, sexual pleasure is a reward that the evolution created to push to reproduction’’ (Fanelli & Lauro, 2008). Since human behaviour depends additionally on education and consciousness, psychology debates whether it is appropriate to speak of instincts in humans. There is, however, a widespread

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agreement on the existence of ‘‘instinctive impulses’’ in human behaviour (Musek, 1993). In the first part of this section more evidence will be provided for the validity of these principles. The discussion will than extend to the question regarding to what degree food is instinctively chosen.

Proteins and amino acids are more potent than carbohydrates and fats3 in inducing short-term satiety in animals and humans. High-protein diets lead to activation of noradrenergic–adrenergic neuronal pathway in the brainstem nucleus of the solitary tract and in melanocortin neurons of the hypothalamic arcuate nucleus (Tome´, Schwarz, Darcel, & Fromentin, 2009).

Examples of nutritional pleasure

How important is (genomic-based) pleasure in food acceptance? In the cases regarding nutritional behaviour so far presented, enjoying food is a means toward increasing the reproduction of genes. This kind of effect seems to be genomic-based. It has the same function in some other nutritional behaviour patterns common to humans and animals, although the link between joy and reproduction is sometimes more indirect.4 Another type of nutritional pleasure is culturally induced. This kind of pleasure is based on the preferences acquired (mostly) epigenetically during childhood and is rooted in the biological structure of the individual. It represents a kind of individual, ethnical variance around the genomic-based mean. Both types of pleasure – the genomic-based and cultural/ epigenetic-based pleasure – are intrinsic components of the emotional factors of the food acceptance process in humans (animals). Human decision making, however, depends on a third factor as well: consciousness. The question is how important are emotions (or simply: enjoying food) in choosing healthy or unhealthy nutrition? Maintaining good health is an important goal for humans. Inquiries into public opinion in various countries demonstrate that ‘‘health’’ is among the most important declared values (Bond, 1988; Musek, 1993; Schwartz & Bilsky, 1990; Tosˇ et al., 1999). Some studies show that a large part of the population, even among overweight people, is aware of the importance of nutrition for their health. But despite the awareness of the health risks of obesity, the majority is not willing to sensibly improve their diet (Kan & Tsai, 2004). In many countries, governments promote a higher consumption of fruits and vegetables through extensive campaigns for at least ‘‘5 portions of fruits and vegetables per day’’: however, without substantial success (FAO/WHO, 2004). Research on public health demonstrates that the population with a higher educational level has healthier nutrition (probably in part because of better economic living conditions). The sensorial aspect seems to have an important role in food acceptance as well: Preliminary results of an enquiry conducted among employees in Slovenia indicate that less than 10% of the participants are willing to permanently give up food that is noxious but enjoyable to eat. In the theory of food acceptance, the role of emotional and instinctive factors has so far been underestimated or treated as an influence that can be changed by education (Sloof, Tijskens, & Wilkinson, 1996/2004; Tijskens, 2004; Tijskens, 2001/2004). It is

Pleasure by eating of food stimulants Most people enjoy the consumption of food and drinks containing stimulants like alcohol, caffeine and others. This habit is culturally based but, amazingly, all wild animals eat and seek food stimulants as well (Engel, 2002; Rafert & Vineberg, 1997). The reproductive reasons for it were explained in more detail in Ostan et al. (2009). All drugs cause – both in animals and in humans – a breakdown of stored body energy (glycogen), which raises blood sugar levels (Holford, 2004; Ichazo, 1990). This is an important nutritional feature. All external sources of nutritional energy usually need some time to digest; some types of food take hours to digest. Food stimulants usually do not bring additional (external) energy, but trigger an immediate release of energy from the body energy stores. This provides an additional available (‘‘ready to use’’) energy to cells that is useful for successful cell reproduction. Thus, consuming food stimulants in limited quantities provides a reproductive advantage, but in the long-term it is damaging for health. It is well documented that stimulants are strong oxidants, triggering the production of free radicals in organisms (Boelsterli, Wolf, & Go¨ldlin, 2005; Pubill, Chipana, & Camins, 2005; Oliveira, Rego, & Morgadinho, 2002), not to mention the over-consumption of stimulants that is currently a widespread practice in human societies (Holford, 2004). Pleasure by consuming protein rich food For most humans, another source of intensive pleasure is the ingestion of protein rich food. The recommended dietary allowance (RDA) for proteins is 0.8 g/kg body weight per day (NRC, 1989). In the USA 97.5% of the population consume more proteins than recommended (Lo´pez-Torres & Barja, 2008). Even in developing countries, nutrition is turning more and more to the western protein rich diet (Campbell & Campbell, 2006). This tendency is not only culturally based; animals, which are similar to humans with respect to their digestive systems, seek protein rich food (Milton, 2003). Behind the pleasure in overeating of protein rich food, there is also the reproductive need. About 60% of dry matter of mammal cells are proteins (Alberts, Bray, Lewis, Raff, Robert & Watson, 1994), thus cell division is a protein demanding process. An abundance of proteins speeds up the onset of puberty in all mammals (Lo´pez-Torres & Barja, 2008). In humans, it extends the period of fertility. The average age at which women who consume a western protein rich diet have their first menstruation at an age of 11 years, while girls in rural China, where the average diet contains only the recommended level of proteins, have it on average at the age of 17 years. In the USA, women experience the menarche 3–4 years later than their rural Chinese counterparts (Campbell & Campbell, 2006). On the other hand, ten out of eleven studies on diets based on isocaloric protein restriction (from 40% to 85% below the normal level) in rats and mice reported an increase in the maximal lifespan. On average it increased by 20%. The effects of protein restriction on lifespan extension is thus minor (about 50%) compared to the effect of caloric restriction (Lo´pez-Torres & Barja, 2008; Pamplona & Barja, 2006). The first similar experiments on humans seem to confirm the positive effects of an isocaloric protein restricted diet on longevity markers (Kozlowska, Rosolowska-Huszcz, & Rydzewsky, 2004; Smith, Underwood, & Clemmons, 1995).

3 Fat appears to have the lowest satiating capabilities among macronutrients and it is the most energy dense (Je´quier and Bray, 2002), but is very palatable for humans (A´˚ berg, Edman, & Ro¨sner, 2008; Stubbs & Whybrow, 2004) and rodents (Warwick, Synowski, Rice, & Smart, 2003), thus individuals tend to eat more, when nourished with high fat diet (Robinson, Gray, Yeomans, & French, 2005). However, among scientist there is consensus that both excessive energy intake and decreasing energy expenditure are the primary culprits for current obesity epidemic, while the primacy of high fat diet is an object of scientific dispute (Foreyt & Walker, 2002). 4 In the case of a major lack of certain essential nutrients in the body, an organism enjoys eating food rich in these nutrients or increases the level of hunger in general (Ames, 2004). Nutritional pleasure appears in this case to be a function of survival and health. But this is in reality just a step to the final result—reproduction. In cases of energy and protein shortage, a ‘‘healthy’’ level of these nutrients is not enough for reproduction. Through enjoying additional eating the body is pushed to greater food intake. Similarly the pleasure of food for elder persons has no direct reproductive effect. But indirectly it is linked with reproduction: it is probably a remnant of the instinctive mechanism that has had a reproductive function in the reproductive age.

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true for epigenetically based pleasure, but not for genomic-based pleasure. Their particular role in acceptance has not been quantified yet, since the study of instinct-based human nutritional behaviour motivation has so far been a neglected scientific field. However, both types of pleasure seem to be very strong and very stable factors in the food acceptance process. Discussion: a need for an enlarged paradigm? The presented cases of self-destructive nutritional behaviour, possibly genomic-based, do not fit into the paradigm of the prevailing stream in nutritional science. Implicitly, the official nutritional policy is based on the presumption that by nature (instinctively) individuals tend toward self-preservation. So, unhealthy nutrition is regarded as a mistake caused by ignorance or bad habits that can be corrected by educational means. Evaluating this approach from the point of view of ethology, the science of instinctive (animal and human) behaviour, it stands implicitly on Hamilton’s thesis (Hamilton, 1964a,b) that Barash (1977) named ‘‘the central theorem’’ of ethology: ‘‘in their behaviour animals are expected to maximise their inclusive fitness’’. This theorem was later critically reviewed. In 1976, Dawkins first expressed direct criticism of it in the book ‘‘The Selfish Gene’’ (Dawkins, 1976/2006). He claimed that in their behaviour, animals tend to maximise the reproduction of genes, only ensuring a sufficient level of health for successful reproduction (Dawkins, 1982/1999). From this point of view, the selfdestructive behavioural patterns that are common to humans and animals and that yield a reproductive advantage, might not be just a mistake but an evolutionarily advantageous choice. This new paradigm does not reject the old one but rather enlarges it: the instinct toward self-preservation is still considered an important natural drive, but evaluated from the broader evolutionary framework it appears to be more a means of reproduction than a central behavioural drive. The evidence for instinctive nutritional behaviour presented in this paper provides more extensive support to Dawkins’s than to Hamilton’s ethological theorem. The presented cases of nutritional practice show that from the physiological point of view there is a nutritional dichotomy: the same food has different effects on the reproductive capabilities of an organism from those it has on health and longevity. In the cases presented, nutrition that is better for reproduction causes a higher production of free radicals as a condition needed for cell division (Halliwell & Gutteridge, 2005), but also as a source of self-destructive oxidative stress. Animals tend to that nutrition that is better for reproduction (nutritional asymmetry). Given contemporary scientific specialisation it is not easy to connect achievements of different disciplines. However, biology is the basic science for a variety of disciplines, including nutritional science. Dawkins’s biological paradigm of ‘‘The Selfish Gene’’ has been known for decades, but has not had much effect on thought regarding nutrition science. Probably the new paradigm could help to better understand the causes of the increasing nutritional problems, like obesity, that ‘‘experts struggle to explain’’ (Taubes, 1998). However, a behaviour pattern like the tendency toward obesity, which impairs fertility (Catenacci, Hill, & Wyatt, 2009; Lichtenstein et al., 1998; Nelson & Fleming, 2007; Norman et al., 2004; Wilkes & Murdoch, 2009) might lead to the question as to whether this instinctive drives really leads to better genes reproduction, as the theory of the Selfish Gene asserts. The contradiction, in our opinion, perhaps reveals that the theory of the Selfish Gene should be understood as part of a broader theoretical frame of the biological theory of the ‘‘Imperfect adaptation of beings to environment’’. In contrast to the theory of perfect adaptation of beings to environment (Cain, 1979) the theory of imperfect adaptation to

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environment treats ‘‘constraints on perfection’’ (Dawkins, 1982/ 1999, p. 30) as essential features of the morphology, physiology and behaviour of animals. The key principle of Dawkins’ theory is the principle of ‘‘malevolence,’’ mostly known as the already mentioned theory of the Selfish Gene (Dawkins, 1976/2006). The other principles (their review exceeds the purpose of this paper) explain why neither the goal of gene reproduction (not to mention the goal of healthy longevity) is reached perfectly, but in most cases indirectly, approximately, and with a lot of failures at individual levels. In this paper we just mention the principle of ‘‘time lags’’ (genes of present beings were selected in some earlier era when conditions were different)’’ (Dawkins, 1982/ 1999, p. 35), suitably explaining the human tendency to overeat. Humans, like every being, need a considerable amount of evolutionary time to adapt to new conditions of food abundance, which is from the reproductive view objectively better that food scarcity. Further research is needed to confirm the value of the hypotheses of a gene-based drive for unhealthy nutrition. Conclusions The majority of populations in wealthy countries choose unhealthy nutrition. Official campaigns based on WHO educational programs for better nutrition (Maucˇec Zakotnik, Koch, & Pavcˇicˇ, 2001) have produced only limited results. Epidemiological studies show that many people who are aware of the risks of unhealthy nutrition are nevertheless reluctant to give it up. It seems that the immediate pleasure, provided by many types of unhealthy diets, is for most people a more important factor for food acceptance than the awareness of the long-term risk of damage. Arguments have been presented for two possible types of gene involvement in this widespread human behaviour. Recent research shows that environmental influences, mostly those experienced in childhood, are epigenetically encoded in the biological structure of the individual, persisting through adulthood as difficult-to-change habits. The habits acquired in childhood (including bad nutrition practice) produce a strong emotional push (enjoyment) that can prevail despite the awareness of their possible (self) damaging effects. The other type of gene involvement in preferences for unhealthy diets seems to be genomic-based. Scientific research shows that wild animals prefer unhealthy diets as well, and that we share with animals the same physiology that forms the basis of such behaviour. However, human biology (physiology, morphology and instinctive drives) presents some peculiarities that distinguish us from other primates (an innate tendency to overeat, biological incapacity to procure enough energy just on all raw nutrition). In our opinion these specifics should also be taken into account in further research and in planning activities for solving the widespread nutritional problems of developed countries. These instinct-driven behaviour patterns enhance the organisms’ chance for reproductive success. Therefore they could not be seen simply as a mistake, but a behaviour that provides an evolutionary advantage to organisms. These findings are in accordance with Dawkins’ theory of the Selfish Gene as a part of its theory of imperfect adaptation to environment that has been known in biology for decades but has been neglected until now in nutrition science

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