The evolution of sour taste. Hannah E. R. Frank, Katie Amato, Michelle Trautwein, Paula Maia, Emily R. Liman, Lauren M. Nichols, Kurt Schwenk, Paul A. S. Breslin and Robert R. Dunn. Proceedings of the Royal Society B: Biological Sciences, February 9 2022. https://doi.org/10.1098/rspb.2021.1918
Abstract: The evolutionary history of sour taste has been little studied. Through a combination of literature review and trait mapping on the vertebrate phylogenetic tree, we consider the origin of sour taste, potential cases of the loss of sour taste, and those factors that might have favoured changes in the valence of sour taste—from aversive to appealing. We reconstruct sour taste as having evolved in ancient fish. By contrast to other tastes, sour taste does not appear to have been lost in any major vertebrate taxa. For most species, sour taste is aversive. Animals, including humans, that enjoy the sour taste triggered by acidic foods are exceptional. We conclude by considering why sour taste evolved, why it might have persisted as vertebrates made the transition to land and what factors might have favoured the preference for sour-tasting, acidic foods, particularly in hominins, such as humans.
(e) Consequences of sour taste preferences for hominins
Regardless of whether rotting fruits played a role in the shift of the acid preference curve in hominins, we hypothesize that the existence of acid taste preference may have strongly influenced the later relationship between hominins and rotten fruits and other rotten foods. Based on studies in the laboratory, three groups of microorganisms compete during the rot of fruits [78], single-celled budding yeasts (most of which are from the Saccharomycetales clade of fungi), filamentous fungi (such as Penicillium) and lactic acid bacteria. While all of these organisms produce short-chain fatty acids when they ferment fruit, yeasts also tend to produce alcohol, and lactic acid bacteria produce lactic acid. Rotten fruits that become dominated by filamentous fungi can be dangerous [79]. However, rotten fruits that become dominated by yeasts and lactic bacteria are often ‘improved’ from the perspective of consumers. Rot due to lactic acid bacteria and yeasts often increases food caloric, free amino acid and vitamin content and hence improves digestibility by breaking down fibre and plant toxins [80–84]. Therefore, in challenging nutritional environments, fruits rotted by yeasts or lactic acid bacteria likely represented a valuable food source that could increase chances of survival [4]. If the acid-preference of the MRCA (whenever acquired) allowed it to more readily consume heavily fermented fruit, or at least the subset of that fruit rotted by lactic acid bacteria, they might have been able to take advantage of a novel source of safe calories.
There exists molecular evidence that the last common ancestor of gorillas, chimpanzees and humans consumed fermented fruits. For example, a single amino acid replacement in the ADH4 gene in the lineage shared by humans and African apes resulted in a 40-fold improvement in ethanol oxidation [85]. This change would have allowed the MRCA to consume yeast-fermented fruits on the ground with higher concentrations of both ethanol and acids [85] without concomitant neurological toxicity (or drunkenness; [53]). This ability may have allowed the MRCA to survive and reproduce more effectively in nutritionally challenging, seasonal environments, particularly as climate change resulted in more fragmented and open habitats. At about the same time, the MRCA acquired a third copy of the HCA3 gene encoding G protein-coupled receptors for hydroxycarboxylic acids, such as lactic acid, produced by the fermentation of dietary carbohydrates by lactic acid bacteria [86]. While this gene is found in all great apes, it is most strongly activated in chimpanzees, gorillas and humans, with humans exhibiting the strongest effects, suggesting that, in some form acid-producing bacteria (and the detection of their products) played a larger role in apes than in other primates and in humans than in non-human apes. As has been considered elsewhere, a fondness for acidic foods, particularly when combined with preferences for umami tastes, may have predisposed ancestral humans to eventual intentional control of rotting to yield more favourable outcomes, which is to say, fermentation [4,87].
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