Ferment in the family tree

Dominy, Nathaniel J.

doi:10.1073/pnas.1421566112

Cited by 25 publications

(13 citation statements)

References 27 publications

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“…Ethanol is therefore common in over-ripe fruit but typically occurs heterogeneously and at low concentrations (Dudley, 2004;Levey, 2004). Precise data on ethanol concentration are, however, available only for some fruit species consumed by animals (Dominy, 2015).…”

Section: Introductionmentioning

confidence: 99%

Feeding on ripening and over-ripening fruit: interactions between sugar, ethanol and polyphenol contents in a tropical butterfly

Beaulieu

Franke

Fischer

2017

Journal of Experimental Biology

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In ripe fruit, energy mostly derives from sugar, while in over-ripe fruit, it also comes from ethanol. Such ripeness differences may alter the fitness benefits associated with frugivory if animals are unable to degrade ethanol when consuming over-ripe fruit. In the tropical butterfly Bicyclus anynana, we found that females consuming isocaloric solutions mimicking ripe (20% sucrose) and over-ripe fruit (10% sucrose, 7% ethanol) of the palm Astrocaryum standleyanum exhibited higher fecundity than females consuming a solution mimicking unripe fruit (10% sucrose). Moreover, relative to butterflies consuming a solution mimicking unripe fruit, survival was enhanced when butterflies consumed a solution mimicking either ripe fruit supplemented with polyphenols (fruit antioxidant compounds) or over-ripe fruit devoid of polyphenols. This suggests that (1) butterflies have evolved tolerance mechanisms to derive the same reproductive benefits from ethanol and sugar, and (2) polyphenols may regulate the allocation of sugar and ethanol to maintenance mechanisms. However, variation in fitness owing to the composition of feeding solutions was not paralleled by corresponding physiological changes (alcohol dehydrogenase activity, oxidative status) in butterflies. The fitness proxies and physiological parameters that we measured therefore appear to reflect distinct biological pathways. Overall, our results highlight that the energy content of fruit primarily affects the fecundity of B. anynana butterflies, while the effects of fruit consumption on survival are more complex and vary depending on ripening stage and polyphenol presence. The actual underlying physiological mechanisms linking fruit ripeness and fitness components remain to be clarified.

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Section: Introductionmentioning

confidence: 99%

Feeding on ripening and over-ripening fruit: interactions between sugar, ethanol and polyphenol contents in a tropical butterfly

Beaulieu

Franke

Fischer

2017

Journal of Experimental Biology

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“…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 ]. At the same time, chimpanzees are known to ingest the fermented exudates of some plants [ 8 , 14 ].…”

Section: Introductionmentioning

confidence: 99%

Alcohol discrimination and preferences in two species of nectar-feeding primate

2016

Self Cite

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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.

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“…Honey is the most energy-dense natural food and is a prized component of living hunter-gatherer diets (except where bees are rare or absent)-even great apes have a 'honey tooth' (27). Energy-dense foods like sugars are sought by larger-brained primates (28) Neandertals and present-day humans share functional adaptations in nutrient metabolism including starch digestion that are not found in our closest ape relatives (29). The high response to vanilla odors suggests a potential response to sweet things-an odor-taste pairing common in present-day humans (30).…”

Section: Discussionmentioning

confidence: 99%

Genetic and functional odorant receptor variation in the Homo lineage

March

Matsunami

Cobb

et al. 2021

Preprint

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The largest and rapidly evolving gene family of odorant receptors detect odors to variable degrees due to amino acid sequence and protein structure. Hybridization between humans, Neandertals, and Denisovans implies shared behavior, although some speculate that Neandertals were poor smellers. We identified genetic and functional variation in humans and extinct lineages in 30 receptors with known function. We show that structural changes in receptor proteins altered odor sensitivity not specificity, indicating a common repertoire across lineages. In humans, variation in receptors may change odor perception or induce odor-specific anosmia. Variation in sensitivity may reflect local adaptations (e.g., Denisovan sensitivity to honey, Neandertals sensitivity to grass and sulphur). Extinct human lineages had highly conserved receptor genes and proteins. We observe a similar pattern in the Neandertal OR5P3 variant, which produced no response to ~350 odors. Our data suggest that receptor structure was highly conserved in our closest relatives, but not in living humans. The diversity of geographic adaptations in humans may have produced greater functional variation, increasing our olfactory repertoire and expanding our adaptive capacity. Our results provide insight into odorant receptor function and shed light on the olfactory ecology of ancient humans and their extinct relatives. By studying the function of ancient odorant receptor genes, we have been able to get a glimpse of the sensory world of our extinct ancestors and relatives, with some of the variants giving specific insights into potential adaptations shown by these long-dead populations. The functional variability we have identified in the molecular structure of the odorant receptor proteins will aid in the more general problem of understanding the function of odorant receptor proteins and the neurons they are carried by, opening the road to linking receptor function to perception.

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Ferment in the family tree

Cited by 25 publications

References 27 publications

Feeding on ripening and over-ripening fruit: interactions between sugar, ethanol and polyphenol contents in a tropical butterfly

Feeding on ripening and over-ripening fruit: interactions between sugar, ethanol and polyphenol contents in a tropical butterfly

Alcohol discrimination and preferences in two species of nectar-feeding primate

Genetic and functional odorant receptor variation in the Homo lineage

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