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Our ancestors were drinking alcohol before they were human

It is possible to trace the evolution of boozing back to the common ancestor of humans and chimpanzees

By Richa Malhotra, BBC Earth

http://www.bbc.com/earth/story/20170222-our-ancestors-were-drinking-alcohol-before-they-were-human

23 February 2017

Between 2005 and 2007, the suburbs of Los Angeles, California, saw several avian casualties. The victims
were 90-odd cedar waxwings and the cause of their death was drunk flying. The tipsy birds had
accidentally rammed into windows, walls, and fencing – and died of trauma.

Before they met their tragic end, the birds had been feasting on the bright red berries of the Brazilian
Peppertree. A post-mortem report on some of the birds revealed that their mouths, food pouches, and
stomachs were full of whole berries and seeds. The birds had become so intoxicated by gorging on the
naturally-fermenting berries that alcohol content in the liver of one reached 1,000 parts per million.

Overall, fruits make up about 84% of the waxwings' diet – but during the colder months, that is pretty much
all they eat. Since fresh, ripe fruit is in short supply, especially during late winter and early spring, the birds
occasionally encounter – and readily devour – over-ripe berries, and then end up drunk.

Birds are not the only animals to come across fermented produce out in the wild. Mammals, in particular,
often feed on fruit, nectar and sap – all of which are rich in sugars that can ferment and be potentially
intoxicating.

If animals consuming forest produce can get inebriated, does that mean our ancient forest-dwelling
ancestors felt the effects of alcohol too? Has alcohol been a continuous presence throughout our
evolution?

In 2000, Robert Dudley of the University of California in Berkeley proposed the idea of a deep historical
link between fruit-eating animals and alcohol intake. With his curiously-titled "Drunken Monkey
Hypothesis", Dudley suggested that our early ancestors were introduced to alcohol in fermenting fruit, and
that this might underlie our current taste for it.

Fruit has formed an important part of the primate diet for perhaps 45 million years. Even though our more
recent ancestors moved from a plant- to a meat-based diet about 2.6 million years ago, they continued to
eat fruit. Our closest cousins – the chimpanzees – spend a lot of time feasting on fruits even today. Other
primates like gorillas, orangutans and gibbons, relish fruits as well.

Ripe fruits ferment and decay because of yeast that grows inside and on the fruits. Yeast breaks down
sugar into alcohol, primarily ethanol – the alcohol in beer and wine. As yeast cells multiply, the fruit sugar
content decreases and ethanol content increases.

In studies published in 2002 and 2004, Dudley reported the alcohol content in wild fruits of
the Astrocaryum palm, which Panama's mantled howler monkeys eat. The unripe fruits contain zero
ethanol, ripe hanging fruits contain 0.6%, ripe fallen fruits contain 0.9% and over-ripe fallen fruits contain
4.5% ethanol (by weight) on an average.

In Dudley's view, such dietary consumption of alcohol likely shaped the evolution of fruit-eating primates for
several million years. The ethanol wafting from fermenting fruits may have been a cue to locate sugary
rewards in a vast forest. Besides, ethanol may itself be a source of calories and perhaps even stimulate the
appetite.

Dudley's Drunken Monkey theory initially faced criticism on a couple of grounds.

One, primates prefer ripe fruits over rotting and the alcohol content of ripe fruits is so poor, it is not enough
to get them "drunk". Two, if they do get drunk, balancing on trees under the influence of alcohol would be
risky, particularly for babies. A third argument was that high-alcohol, low-sugar fruits should deter, rather
than attract, primates. Added to that is the fact that primates had rarely been seen getting wasted on
fermented fruits in the wild.

But these criticisms did not really get to the heart of Dudley's idea. His main argument was that our ability to
digest alcohol is well-developed today because exposure to alcohol happened early on in our ancestory.
Digesting ethanol quickly would have been life-saving for our ancestors

Evidence of this can be seen in our genetic make-up. A study published in 2014 looked at evolution of an
alcohol dehydrogenase enzyme named ADH4, which is one of many that break down alcohol in our bodies.
Because it is present in the mouth, food pipe and stomach, ADH4 is the first such enzyme to face off with
the alcohol we consume.

Crystal structure of human ADH4


https://www.rcsb.org/structure/3COS

Matthew Carrigan of Santa Fe College in Gainesville, Florida, and his team found that a genetic mutation
in our evolutionary past made ADH4 40 times better at breaking down ethanol.

The mutation was effectively ubiquitous in our ancestors by 10 million years ago, which might be
significant. This is around the time that those ancestors started adapting to a terrestrial lifestyle and
probably first encountered high ethanol content in fruits rotting on the forest floor. This point in prehistory
also coincided with a period of climate change that saw forests in Africa shrink while grasslands expanded.
In the new environments, fresh fruit would have been harder to come by.

Fallen, over-ripe fruit often lies uneaten for longer than the sought-after fresh and hanging ripe fruit, so it
contains more ethanol. As the shift to a terrestrial life was underway, digesting ethanol quickly would have
been life-saving for our ancestors, who were still spending half of their time climbing and swinging in trees
some 10 to 20m above ground, says Carrigan.

So, an ADH4 that could better utilise alcohol-


rich fruits would have been favoured in our
evolution. Additionally, the calories in alcohol
would have likely provided the extra energy
required by our ape ancestors to move on the
ground when their bodies were still adapted to
living in trees.

The mutation in ADH4 also means that the


enzyme in our more ancient, arboreal ancestors
about 40 million years ago was bad at digesting ethanol – "stinking bad", as Carrigan puts it. This raises the
question that, if ADH4's ability to deal with ethanol was dramatically improved 10 million years ago, what
was it doing in the first place?

"ADH4 in our very distant ancestors 40 million years ago was very good at metabolising a different alcohol
called geraniol," says Carrigan. "And it turns out geraniol is not the only alcohol that the ancient ADH4 was
good at metabolising. It also metabolised cinnamyl, coniferyl and anisyl alcohols. These alcohols have
similar structures, are large hydrophobic alcohols, and as the name implies are found in geranium,
cinnamon, conifer and anise plants."

These alcohols can be harmful if consumed in high concentrations, and are produced by plants to deter
animals from eating their leaves.

"This makes sense because our arboreal ancestors 40 million years ago were eating leaves (and fruits). So
being able to metabolise the chemicals in leaves would have been a really big advantage," says Carrigan.
The exposure to ethanol would have been minimal for these ancestors as they had access to unfermented
fruits, he adds.

Millions of years later, when ADH4 encountered ethanol in high concentrations in fermenting fruit, it
adapted to digesting it really well. "It went from an enzyme that metabolised ethanol incredibly slowly to one
that metabolized ethanol 40-fold more efficiently," says Carrigan. This was due to a single tweak in the
enzyme (single point mutation). This change in ADH4 that occurred 10 million years ago enabled the last
common ancestor of humans, chimpanzees and gorillas to break down ethanol.

This finding certainly seems to back a key part of Dudley's theory that our alcoholic tendencies stem from
our fruit-eating ancestors. It also shakes the idea that humanity's tryst with alcohol is fairly recent, dating
back only about 9,000 years, to when humans first produced alcoholic beverages from grain, honey
and fruit.

Some other research indirectly supports Dudley's ideas too. For instance, in 2015, a long-term
study spanning 17 years reported that wild chimpanzees booze on fermenting tree sap.

In the village of Bossou in Guinea, West Africa, locals crop the crown of mature raffia palms and hang
plastic jugs to collect the sap dripping from it. The sugary sap soon ferments into alcohol, which is a
popular drink among the locals. It is known as palm wine. On an average, the wine contains 3.1% ethanol
(by volume) but it can go up to 6.9% depending on how long it is left to ferment.

While the wine is brewing, it can draw the attention of chimpanzees living or foraging nearby. The uninvited
guests help themselves to the free drinks, with either an individual hogging the jug or two drinking buddies
alternating their take, while others wait.

To get the wine, chimps use a tool: they crush some


leaves in their mouth, dunk the leaves into the wine and
put them back into their mouth to squeeze wine out, like a
sponge. This way, the wine is drunk by young and old,
male and female chimps alike – and they come back for
more. Some even get tipsy.

Kimberley J. Hockings of Oxford Brookes University in


the UK, writes in an email from Guinea-Bissau that,
though she has not formally recorded the behavioural
effects of alcohol, she did notice some signs of
intoxication: chimps lying down or becoming agitated after drinking too much.

The chimpanzees cannot tap the raffia palm on their own: they rely on the sap collection set-up prepared
by villagers. But the study shows that they readily imbibe fermenting sap when it is available – and chimps
are picky when trying new foods. The chimps also down the sap repeatedly in large quantities, which
means it is not accidental but deliberate, habitual intake.

To be sure, the behaviour is rare. It was seen only in 50% of the local Bossou chimp population. The 13
remaining chimps were teetotallers, even though palm wine was available year-round.

The research did not put Dudley's ideas to the test. Whether the chimps use their sense of smell to home in
on the wine or gain any nutritional benefit from drinking it, it does not show. But it does confirm that wild
chimpanzees are not averse to alcohol.

Chimpanzees, like humans, have an efficient form of the ADH4 enzyme to metabolise alcohol, though it
varies across populations. This is because we both inherited the modified gene coding for a faster version
of the enzyme from a common ancestor. But there is one distant primate that acquired the same ADH4
mutation, independent of the lineage that led to us.

Aye-ayes split from our branch of the primate evolutionary


tree 70 million years ago. We do not know when they
acquired the same ADH4 mutation as us. But the fact that
modern aye-ayes have it hints to a past where these animals
too were exposed to alcohol. According to Carrigan, who
carried out the work on ADH4 enzymes, if this was indeed
the case, then aye-ayes might consume alcohol in the wild
even today.

Indirect proof suggests they might. One 2016


study confirmed that two aye-ayes in captivity do have a
taste for alcohol.
Aye-ayes are small, rather weird-looking primates with a thin and unusually long middle finger, which they
use to locate and catch grubs in deadwood. But during the rainy season aye-ayes spend about 20% of their
feeding time drinking nectar of the traveller's palm. Their long middle finger helps here too, in searching
and scooping out the nectar.

It is believed that the nectar contained in bracts and flowers of the traveller's palm ferments. Though its
alcohol content is yet to be established, the nectar is similar to that of another palm: the bertam palm.
Bertam nectar contains up to 3.8% alcohol on natural fermentation by yeast. It gives out a strong whiff
and is drunk by pen-tailed treeshrews, common treeshrews and slow lorises, among other mammals.

Samuel R. Gochman, a student at Dartmouth College in Hanover, New Hampshire, and his team offered
aye-ayes a choice of liquid foods made of sugar water and varying concentrations of alcohol (0 to 5%). The
two captive aye-ayes could differentiate between the different alcoholic foods. They preferred to drink from
the containers with higher alcohol doses of 3 and 5% over those with 1% and zero alcohol.

When the containers holding higher alcohol contents had run out, the aye-ayes continued to compulsively
dip and lick their fingers. "This suggests that they really like those concentrations," says Gochman.

But the animals did not show any obvious signs of inebriation, which goes back to their ability to breakdown
alcohol because of a super-efficient ADH4 enzyme.

"Natural selection would favour this special ability because it allows these animals to access calories that
would normally be toxic to other animals. Those organisms would avoid alcohol because it can impair
judgement and is a chemical toxin," says Gochman.

Unlike aye-ayes, chimps and humans, other animals that consume ethanol do not necessarily have an
ethanol-active version of ADH4. Take the common treeshrews that drink from the bertam palm,for instance.
Their alcohol intake is considered potentially risky. How do they cut it? We do not know for sure.

Whatever allows these animals to tolerate the effects of alcohol, it is sobering to know that we are not the
only habitual drinkers out there. And even if some of us are teetotallers, our ancestors were probably not.