Taste is afforded the greatest relevance to nutrition as it is posited to have improved the probability of survival, helping screen safe and potentially toxic properties of foods; this teleology is dubious

Taste, teleology and macronutrient intake. Richard D Mattes. Current Opinion in Physiology, Volume 19, February 2021, Pages 162-167. https://doi.org/10.1016/j.cophys.2020.11.003

Abstract: Among the human sensory systems, taste is afforded the greatest relevance to nutrition as it is posited to have aided the identification and ingestion of nutrients in the environment and thereby improved the probability of survival. With respect to the macronutrients, sweet, umami and oleogustus (fat taste) reportedly facilitated meeting energy, essential amino acid and essential fatty acid requirements. However, such a teleological view fails to account for the fact that humans are largely blind to the primary sources of the macronutrients in the environment (starch, protein and triacylglycerol) and, in the case of protein and fat, the effective taste stimuli are generally unpleasant degradation products. Additional challenges to the prevailing teleology are also presented. Some have proposed that the sense of taste serves as a palatability screen that functions more basically by signaling safe and potentially toxic properties of potential foods. However, it is well documented that sensory qualities are unreliable predictors of food safety (sweet foods can be toxic and bitter foods nutritious). Instead, it is proposed that taste contributes to food choice by acquiring predictive information about wholesomeness through innate and learned mechanisms.

Sweet taste

Humans are limited to carbohydrates, fats and proteins as substrates to meet energy needs. Knowledge of the composition of ancient human diets is incomplete, but recent evidence supports a substantive contribution of starchy foods in many pre-agricultural populations [12] though it likely varied widely between subpopulations [13]. Access to simple carbohydrates would have been extremely low [14].

A functional role for sweet taste is forcefully made by reduced conservation of the sweet taste receptor and evidence of insensitivity to this quality by vertebrates not exploiting sweet foodstuffs (e.g. cats, sea lions, whales, pandas, horses, western clawed frog, vampire bats) as well as reemergence of sensitivity by hummingbirds who are exclusive nectar feeders while other birds lack this capability and food choice [15•,16,17••]. However, a broader analysis reveals a lack of association between losses of sweet taste sensitivity and diet [17••].

There are multiple additional observations that challenge the view that sensitivity to sweetness would be a functional mechanism to access carbohydrate. First, there is no essential mono or disaccharide and those are the predominant effective sweet taste stimuli. Thus, sweet taste is not tuned to an essential nutrient. Second, sources of sweet carbohydrate were extremely rare in the environment throughout most of human evolution. With the exception of limited access to honey and seasonal fruits, a receptor tuned to simple sugars would have served little purpose post-weaning. Even its role in promoting milk ingestion pre-weaning is uncertain. Fat is the primary determinant of the energy density of breast milk and studies with gruels varying in energy density and sweetness reveal intake is more closely related to energy density [18]. Also, interestingly, kittens who are carnivores and lack a functional sweet receptor nurse effectively [19] on mature cat milk that is approximately 4% lactose and only 6.3–8.6% protein [20]. Third, a more functional taste contribution to locating and promoting carbohydrate intake would have been sensitivity to starch which was abundant. There is preliminary evidence of human sensitivity to short chain oligosaccharides of 7 and 14 units (not 44) [21], but the sensation is not mediated by the T1R2–T1R3 (sweet) receptor and the sensation they evoke is not sweetness.

Further, it is clear that sweetness is an imperfect indicator of safe and available carbohydrate as sweet fruits are not necessarily rich sources of carbohydrate or energy (i.e. they have low energy density due to their high water content), not all sweet stimuli are carbohydrate (e.g. Monellin, Thaumatin, Brazzine are proteins) and some sweet molecules are toxic (e.g. lead acetate).

In summary, sweetness lacks the sensitivity and specificity to identify and promote the consumption of wholesome carbohydrates in the environment. However, it is not disputed that sweetness is rewarding and an appetitive signal that promotes feeding generally [18,22,23].

Umami taste

Proteins are comprised of amino acids, nine of which are considered essential that is, cannot be synthesized in humans so must be acquired from the diet. Rarely are free amino acids encountered in the environment because protein synthesis is extremely efficient. Amino acids are synthesized when needed to build proteins and in requisite proportions. Proteins play many roles in the body. They serve as enzymes, hormones, neurotransmitters, nutrient transporters, structural elements and are crucial for growth and development, pH balance, fluid balance, immune function and when consumed in excess of need, can provide energy.

Given these multiple essential roles, a teleological view would support a sensory system tuned to protein sources in the environment. However, the importance of taste in this regard is questionable. Some evidence suggests taste alone allows rapid identification of dietary protein sources in protein-depleted rats [24], but the preponderance of evidence indicates selection in rodents and other animals depends on post-ingestive learning where the sensory signal only acquires predictive power based on an association with a corrective post-ingestive outcome [25,26]. Second, a number of essential amino acids are effective taste stimuli, but a number of these elicit unpleasant sensations (e.g. methionine, leucine, tryptophan) and render protein hydrolysates unpalatable. This would discourage ingestion of the required nutrient.

The more specific case of Umami taste has attracted considerable attention. The prototypical stimulus for Umami taste is monosodium glutamate (MSG). Psychophysical studies in infants [27] and adults [28] indicate the stimulus is rejected when presented in water. In suprathreshold concentrations the quality of D-MSG is soapy-metalic and L-MSG is described as predominantly bitter [29], generally negative qualities. It is only in selected food contexts that it contributes a positive quality [30] and then this is augmented by the co-presence of 5′ ribonucoleotides [31]. Despite the low palatability of MSG, the teleological argument has been made that sensitivity to the compound signals the presence of protein sources in the environment and presumably the desirability of consuming them [32••]. Consistent with this view, herbivores generally lack the umami taste receptor [16]. However, the necessity of this signaling system is not supported. Selected animals have lost taste responsivity to umami (e.g. pig, horse, rabbit, tree shrew, mouse lemur, marmoset, tarsier, hyrax, sea lion, bottlenose dolphin) but all animals require protein [17••,33]. Additionally, if the teleological perspective that umami sensitivity aids acquisition of needed protein is true, individuals with low or marginal protein status should exhibit augmented hedonic responses to MSG containing foods. Heightened hedonic responses to other nutrients during periods of deficit have been documented [34]. While there is a report to this effect [35] for protein, the broader literature is not supportive [28,36]. Indeed, palatability is diminished in this state and is relatively heightened in the protein replete state [32••], counter to the hypothesis. An additional teleological argument holds that there would have been a survival benefit of detecting and consuming purine-rich foods which would contain higher concentrations of ribonucleotides. These foods can lead to elevated uric acid concentrations with consequent physiological responses that could have mitigated famine-related threats to survival [37]. If true, then, it is problematic now where famines are less common and diseases of overconsumption predominate, including gout, hypertension and glucose intolerance. If gustatory wisdom held in this case, it appears to have been lost or rendered non-functional in the current environment.

Taken together, the evidence indicates food choices related to satisfying protein requirements are guided more by non-protein specific signals that become associated with post-ingestive cues that protein needs are met and umami taste, in particular, serves to promote the overall palatability of the diet and thereby encourages food intake generally [38].

Fat taste (Oleogustus)

Linoleic acid and alpha-linolenic acid (ALA) are essential fatty acids (EFA) for humans, that is, they cannot be synthesized in the body and must be obtained via the diet. Eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) can be synthesized from ALA, but the conversion efficiency is low so a dietary source is beneficial. These fatty acids serve multiple purposes in the body. They have anti-inflammatory activity, are structural elements in cell membranes and are precursors to a range of bioactive compounds. Additionally, fats, in general, are the most energy dense macronutrient. Thus, a system to detect them and promote their consumption would hold survival value.

Though there have been isolated claims that there is a taste for fat, this view received little empirical support until recently [39••]. The predominant signals from dietary fat were considered visual, somatosensory and olfactory. The somatosensory contribution from triacylglycerols, the predominant form of dietary fat, include sensations such as creaminess, viscosity, lubricity, and mouth-coating and are largely rated as appetitive (i.e. palatable). In contrast, the olfactory cues, stemming primarily from free fatty acids (FFA) derived from triacylglycerol, are largely considered aversive. Consequently, for most foods, concentrations of free fatty acids are purposefully held below detection thresholds during product development. Of course, through experience even strong fat-based odors can acquire a positive valence. Work demonstrating dietary fat can elicit an early spike in plasma triacylglycerol concentrations when somatosensory and olfactory cues were largely controlled, suggested a role for taste [40]. Studies in mice indicate FFA, not triacylglycerol, are the effective taste stimuli [41]. Subsequent studies documented measurable and differential taste threshold for various fatty acids [42] in humans and the qualities appear to change with fatty acid chain length. Short-chain fatty acids are largely sour (<C:6) while longer chain fatty acids (>C:16) evoke an unpleasant sensation that is unique from other primary taste qualities [43] and has been termed oleogustus. The essential fatty acids are consistently rated as unpleasant. They would be encountered in the environment largely through rancid foods and it has been posited that they act more as warning signals than appetitive signals. This is inconsistent with a teleological perspective that the function of oleogustus is to aid in the acquisition of EFA and/or energy. Indeed, it has further been proposed that high fat intake occurs because of insensitivity to the taste of fatty acids [44]. There is the possibility that the taste of low concentrations of long-chain FFA could contribute positively to the overall flavor profile of some foods, just as bitter notes, unpleasant in isolation, contribute to the palatability of selected foods (e.g. wines, chocolate, coffee). Of course, if one accepts this caveat, it is also true that bitterness cannot be regarded as a uniformly aversive signal protecting against toxin exposure.

Whether oleogustus qualifies as a taste primary is not settled science. If it is accepted, the effective taste stimulus would most likely occur in rancid foodstuffs. The quality of the sensation would discourage ingestion and hinder meeting EFA and energy needs.