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Abstract
Recent reports suggest that dietary ethanol, or alcohol, is a supplemental source of calories for some primates. For example, slow lorises (Nycticebus coucang) consume fermented nectars with a mean alcohol concentration of 0.6% (range: 0.0–3.8%). A similar behaviour is hypothesized for aye-ayes (Daubentonia madagascariensis) based on a single point mutation (A294V) in the gene that encodes alcohol dehydrogenase class IV (ADH4), the first enzyme to catabolize alcohol during digestion. The mutation increases catalytic efficiency 40-fold and may confer a selective advantage to aye-ayes that consume the nectar of Ravenala madagascariensis. It is uncertain, however, whether alcohol exists in this nectar or whether alcohol is preferred or merely tolerated by nectarivorous primates. Here, we report the results of a multiple-choice food preference experiment with two aye-ayes and a slow loris. We conducted observer-blind trials with randomized, serial dilutions of ethanol (0–5%) in a standard array of nectar-simulating sucrose solutions. We found that both species can discriminate varying concentrations of alcohol; and further, that both species prefer the highest available concentrations. These results bolster the hypothesized adaptive function of the A294V mutation in ADH4, and a connection with fermented foods, both in aye-ayes and the last common ancestor of African apes and humans.
Highlights
Mounting evidence suggests that dietary ethanol, or alcohol, is a prevalent component in the natural diets of non-human primates [1,2,3,4,5,6,7,8,9]
We found that members of two species of nectivorous primate—the aye-aye (D. madagascariensis) and slow loris (N. coucang)—can discriminate between varying concentrations of alcohol in nectar-simulating solutions; and further, that both species prefer the highest concentrations of alcohol available to them
ADH4 is unstudied in slow lorises, the only verified consumer of fermented nectar among primates [34]
Summary
Mounting evidence suggests that dietary ethanol, or alcohol, is a prevalent component in the natural diets of non-human primates [1,2,3,4,5,6,7,8,9]. A single amino acid change (A294V) in some species resulted in a 40-fold increase in ethanol oxidation, substantially improving enzymatic efficiency This mutation arose independently in two distantly related primates, the aye-aye (Daubentonia madagascariensis) and the last common ancestor of African apes and humans. Carrigan et al [11] proposed that increasing terrestrial travel exposed the last common ancestor of African apes and humans to fermented fruits on the forest floor; and further, that consuming such fruits favoured retention of the A294V mutation This adaptive hypothesis is alluring [13] but some observers have inferred or imputed a primate aversion to fermented resources [10]. Access to one or both liquids raises the possibility that aye-ayes consume non-trivial quantities of alcohol on a seasonal basis Speculative, this hypothesis [11] agrees well with observations of another nocturnal primate, the slow loris (Nycticebus coucang). The protein sequence and corresponding kinetic activity of ADH4 are unknown for slow lorises
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