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The Evolutionary Ecology of Ethanol Production and Alcoholism

Author(s): Douglas J. Levey


Source: Integrative and Comparative Biology, 44(4):284-289. 2004.
Published By: The Society for Integrative and Comparative Biology
DOI: http://dx.doi.org/10.1093/icb/44.4.284
URL: http://www.bioone.org/doi/full/10.1093/icb/44.4.284

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INTEGR. COMP. BIOL., 44:284289 (2004)

The Evolutionary Ecology of Ethanol Production and Alcoholism1


DOUGLAS J. LEVEY2
Department of Zoology, P.O. 118525, University of Florida, Gainesville, Florida 32611-8525

SYNOPSIS. Understanding the evolutionary ecology of ethanol production may yield insights into why humans are prone to excessive consumption of ethanol. In particular, Dudley (2000) suggested that human
ancestors developed a genetically based attraction to ethanol because they could use its odor plume to locate
fruiting trees and because of health benefits from its consumption. If so, ethanol should be common in wild
fruits and frugivores should prefer fruits with higher ethanol content. A literature review reveals that ethanol
is indeed common in wild fruits but that it typically occurs in very low concentrations. Furthermore, frugivores strongly prefer ripe over rotting fruits, even though the latter may contain more ethanol. (Data on
ethanol content of ripe and rotting wild fruit are lacking.) These results cast doubt on Dudleys hypothesis
and raise the question of how humans became exposed to sufficiently high concentrations of ethanol to allow
its excessive consumption. Because fermentation is an ancient and widespread practice, I suggest that humans discovered ethanol while using fermentation as a food preservation technique. They may have been
predisposed to consume ethanol from previous and beneficial exposure to much lower doses or they may
have become addicted to it at high concentrations because of fortuitous physiological responses.

INTRODUCTION

vides calories and can stimulate appetite and yield


health benefits via hormetic processes. Just as an evolutionarily-based attraction to highly caloric foods by
our ancestors may have predisposed humans to obesity
and Type II diabetes in modern societies with an abundance of fat and sugar rich food (Eaton and Eaton,
1999), the susceptibility to alcoholism may be viewed
as the result of nutritional excess. A variation of this
hypothesis was proposed by (Singh, 1985).
I address three issues related to Dudleys hypothesis.
First, I describe the evolutionary ecology of ethanol
production in wild fruits. In particular: What accounts
for the occurrence of ethanol? How common is it?
And, what are typical ethanol concentrations encountered by frugivorous vertebrates? Second, I review the
scanty literature on whether vertebrate frugivores prefer fruits with presumably higher levels of ethanol over
conspecific fruits with presumably lower levels of ethanol. The goal is to evaluate a central prediction of
Dudleys hypothesis: ethanol-rich fruits should be preferred over those with little or no ethanol. My third
objective is to propose a modification of the hypothesis. Specifically, I will argue that frequent consumption of ethanol-rich fruits is not a prerequisite for excessive ethanol consumption by humans.

Excessive consumption of alcohol is a major threat


to human health in many societies. Research on alcoholism generally focuses on physiological and psychological bases of addiction. This mechanistic approach,
which characterizes biomedical research in general, is
based on common sense: understanding how the body
responds to ethanol consumption allows development
of treatments that target key vulnerabilities or that take
advantage of existing detoxification mechanisms. Yet
despite its success and future potential, this approach
is handcuffed.
The handcuffs result from a general failure to incorporate evolutionary theory. Alcoholism did not
arise de novo and humans are not unique in their exposure to ethanol, the most common type of naturally
produced and consumed alcohol. Indeed, an evolutionary basis for susceptibility to alcoholism is suggested
by its heritability and by biogeographic patterns of alcohol dehydrogenase (ADH) occurrence (Goldman,
1993; Shen et al., 1997). As argued by proponents of
Darwinian medicine, consideration of both proximate
(mechanistic) and ultimate (evolutionary) factors holds
great promise for providing new insights about the origins and treatments of human diseases, including alcoholism (Nesse and Williams, 1994; Stearns, 1999).
This review addresses a recent evolutionary hypothesis for the evolution of alcoholism. Dudley (2000,
2002) posits that the highly frugivorous diet of hominids and their closest relatives chronically exposed
them to ethanol within fruits. These primates may have
keyed into ethanol because its odor plume can be used
to find fruiting trees, and because its ingestion pro-

ETHANOL PRODUCTION
Natural history of fruit rot
By far the most common natural source of ethanol
is fermentation of fruit sugars by yeasts. Indeed, yeast
is typically envisioned as an anaerobic organism and
credited for the following reaction, upon which the
beer and wine industries are based:
C6H12O6 2C2H5OH 1 2CO2

From the symposium In Vino Veritas: The Comparative Biology


of Alcohol Consumption presented at the Annual Meeting of the
Society for Integrative and Comparative Biology, 59 January 2004,
at New Orleans, Louisiana.
2 E-mail: dlevey@zoo.ufl.edu

Ecologically, however, yeasts are far more diverse;


only a small subset of species specialize on fruits and
of those that do, most can ferment carbon-rich substrates other than glucose (e.g., polysaccharides and
284

EVOLUTIONARY ECOLOGY
lipids; Phaff et al., 1966). None is reliant on anaerobic
metabolism alone and many can shift between fermentative and respiratory (aerobic) pathways, depending
on conditions (Cooke, 1979). In aerobic environments,
ethanol is oxidized by yeasts or Acetobacter bacteria,
often resulting in production of acetic acid (vinegar).
Both ethanol and acetic acid can inhibit further growth
of yeasts (Skinner et al., 1980). The important point
is that ethanol production is self-limiting and occurs
only in anaerobic environments. Functionally, this suggests that small fruits, which have relatively high surface-to-volume ratios, will be less likely to harbor
large colonies of ethanol-producing yeasts than large
fruits, which have a relatively high proportion of pulp
shielded from aerobic conditions. Small fruits are additionally unlikely to be an important ethanol source
because any ethanol they may contain is more prone
to evaporative loss than is the case in larger fruits,
which have relatively smaller surface areas. In a similar vein, ethanol content is likely to differ between
lipid-rich fruits and sugar-rich fruits, being higher in
the latter because simple sugars are more readily fermented than lipids. Unfortunately, predictors of ethanol content in ripe wild fruits remain unexplored.
How common are fruit rot fungi? Tang et al. (2003)
report a total of 102 taxa on eighteen species of wild
fruits in Hong Kong. In less thorough screenings of
fungi from surface-sterilized ericaceous and solanaceous fruits, 14 and 10 taxa, respectively, were isolated
from two North American sites (Cipollini and Stiles,
1993; Cipollini and Levey, 1997). Often more than one
species or genus of yeast is present on a given fruit
and different species may replace each other over
timei.e., there is a succession of species as the fruit
ripens or rots (Phaff et al., 1966; Cooke, 1979; Spencer and Spencer, 1997). Different species can also typify different types of fruits. For example, Candida is
most common on lipid-rich fruits and Saccharomyces
on sugar-rich fruits (Skinner et al., 1980). In the context of this review, it is noteworthy that Saccharomyces species are abundant, widespread, and champion
producers of ethanol; not coincidentally, brewers yeast
(S. cerevisiae) belongs to this genus.
Not all fungi associated with fruit cause rot. Some
species are latent or endophytic, infecting flowers or
immature fruits and persisting for long periods in an
asymptomatic state (Snowdon, 1990; Johnson et al.,
1992). Cipollini and Stiles (1993) hypothesize a mutualistic interaction between endophytic fungi and
fruiting plants, whereby the fungi benefit from nutrients within pulp and the plants benefit from the fungi
inhibiting growth of other species that would quickly
cause fruit rot or be otherwise pathogenic. Because
many species of Saccharomyces are endophytic, their
presence in fruits (and the production of ethanol that
accompanies it) should not be assumed to be detrimental to the fruiting plant.
Although it is tempting to assume that ethanol is
common because yeast spores and fruits are omnipresent, it is important to keep in mind that not all

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yeasts produce ethanol and those that do produce it


only under restrictive (anaerobic) conditions. Furthermore, fruits in the temperate zone are typically removed by frugivorous vertebrates before they become
damaged or show signs of rot (Jordano, 2000; McCarty et al., 2002). Of fruits that are not removed,
many are impervious to rot because they are protected
by secondary compounds, desiccate, or occur when
ambient temperatures are too low for microbial growth
(Cipollini and Levey, 1997; Jordano, 2000; McCarty
et al., 2002). In the tropics, where fruit diversity is
higher, fruit abundance typically less seasonal, and abiotic conditions generally more favorable for microbial
growth, ethanol production in fruits may be more common than at higher latitudes.
It takes three to tango: evolutionary ecology of fruits
and their consumers
A fundamental difference between plants and animals is that animals are mobile and plants are not.
Fruits are an evolutionary response to this lack of mobility in plants; they provide a mechanism by which
plants disperse seeds to new sites. Frugivorous vertebrates ingest fruits and the seeds within, later defecating the seeds. Frugivores gain nutrients from the fruit
pulp, while plants gain various benefits of seed dispersal. Fitness advantages to both participants have
been so strong and ubiquitous that mechanisms of seed
dispersal by vertebrates have evolved in almost all major lineages of extant seed plants and, conversely, reliance on fruit is evident in all major lineages of vertebrates (Herrera, 2002; Labandeira, 2002).
Because the interaction between fruiting plants and
frugivorous vertebrates described above is so visibly
apparent, it has dominated the research agenda of those
interested in the chemical composition of fruits. Unfortunately, it is a narrow and restrictive view of fruitfrugivore interactions. A central theme of this review
is that fruit-frugivore interactions should be viewed as
a triad between fruiting plants, vertebrate frugivores,
and invertebrate/microbial frugivores (Janzen, 1977;
Herrera, 1982; Cipollini and Levey, 1997) (Fig. 1).
Ironically, the most abundant frugivores, fungi, are
those that are most rarely considered in studies of frugivory. This oversight is especially pertinent, given
that fungi are the primary source of ethanol.
We have already considered the interaction between
fruiting plants and vertebrate frugivores. To place this
in the context of ethanol production requires consideration of frugivory from a microbial perspective. I
now summarize the remaining two sides of the triad:
interactions between microbes and fruiting plants and
between microbes and vertebrate frugivores.
Unlike the mutualistic interaction between fruiting
plants and vertebrate frugivores, the interaction between plants and frugivorous microbes is predatory.
Not only do microbial frugivores consume fruits and
fail to disperse seeds, but they often render fruits unattractive to vertebrate frugivores that do disperse
seeds. Thus, fruiting plants face an evolutionary dilem-

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DOUGLAS J. LEVEY

FIG. 1. Production of ethanol by microbes in fruit is best viewed as a component of a three-way interaction between fruiting plants, microbes
(yeast and other fungi), and frugivorous vertebrates. Arrows indicate effects of the organism at the arrows base on the organism at the arrows
tip, and 1 or 2 signs denote positive or negative effects, respectively. Explanations are in parentheses. The interaction between microbes
and vertebrate frugivores is poorly known.

ma: how to make their fruits simultaneously attractive


to vertebrate frugivores and unattractive to microbial
frugivores. A hypothesized means of solving this dilemma is directed deterrence, whereby plants produce compounds in fruits that negatively affect microbial growth and have little effect on vertebrates (Janzen, 1977; Herrera, 1982; Cipollini and Levey, 1997).
Directed deterrence provides an adaptive explanation
for why all wild fruits contain a rich array of secondary compoundswhy they are so much more than
packages of calories and proteins for vertebrate dispersers. Ethanol, however, should not be viewed in this
framework because it is not produced by the fruiting
plant.
The interaction between vertebrate and microbial
frugivores (hereafter, fungi) is largely unexplored and
more complex than generally appreciated. The two
types of frugivores are best viewed as competitors of
an ephemeral resource. Vertebrate frugivores consume
many fruits and are capable of extracting nutrients
from a given fruit in a matter of minutes, whereas
fungal frugivores are each restricted to a single fruit
and require days or weeks to profit via sporulation.
This asymmetry suggests that fruits are a dangerous
habitat for fungi; they may be consumed at any moment by a frugivorous vertebrate (Janzen, 1977; Herrera, 1989). Because the stakes are high for fruit fungi

(reproduction vs. death), fungi should defend themselves and their fruit as soon as possible after colonizing the fruit (Janzen, 1977). The result is fruit rot.
Its efficacy as a defensive mechanism for fruit rot fungi is as apparent as rotten fruit is repulsive.
Three lessons relevant to ethanol production emerge
from consideration of the evolutionary triad (Fig. 1).
First, if yeast or other frugivorous fungi win the battle for fruit pulp, both fruiting plants and frugivorous
vertebrates lose. All else equal, dual selection pressure by plants and vertebrates against frugivorous fungi and for each other, means that ethanol production
and other processes associated with fruit rot should be
rare. Second, frugivorous vertebrates are consistently
exposed to secondary metabolites from both fruiting
plants and frugivorous fungi. Vertebrate frugivores
should thus be physiologically adept at detoxifying
such compounds, including ethanol. Third, although
ethanol is an end product of fermentation, the fungi
that produce it are locked in a complex set of interactions with fruiting plants, frugivorous vertebrates,
and other microbes. Given that ethanol affects both
vertebrates and microbes (Janzen, 1977), it is likely to
have at least some adaptive basis. In particular, it may
be viewed as a defensive agent, used by yeasts to inhibit growth of competing microbes in much the same

EVOLUTIONARY ECOLOGY
way as penicillin is thought to give Penicillium fungi
the upper hand in competition with bacteria.
Ethanol concentrations in wild fruits
I am aware of only four studies of ethanol content
in wild fruits: Eriksson and Nummi (1982), Dudley
(2002), Dominy (2004), and Sanchez et al. (2004).
These studies provide data from across a fairly wide
range of fruit types: 18 species in 11 families. Ethanol
concentrations range from 0.04 to 0.72%. One way to
view these data is that ethanol is ubiquitous in ripe
fruit; frugivorous vertebrates cannot avoid ethanol ingestion.
Another way to view the same data is that ethanol
concentrations are extremely low by anthropomorphic
standards, 12 orders of magnitude below typical concentrations in beer and wine (36% and 811%, respectively). Such comparisons are potentially misleading, though. An animals physiological exposure to
ethanol is not only a function of the ethanol concentration of its food, but also of how much it consumes
and the dynamics of ethanol absorption and metabolism. Frugivorous birds and bats have particularly high
rates of fruit consumption, tied to similarly high fluxes
of digesta through the gut (Witmer and Van Soest,
1998; Levey and Martnez del Rio, 2001). They presumably absorb more ethanol than do less frugivorous
species of the same body size because their net absorption rates are higher. Balancing this, at least in
frugivorous birds, are unusually high activities of alcohol dehydrogenase (Eriksson and Nummi, 1982;
Prinzinger and Hakimi, 1996). Species that are more
highly frugivorous tend to have higher rates of alcohol
metabolism than do less frugivorous species (Eriksson
and Nummi, 1982; Prinzinger and Hakimi, 1996).
ETHANOL CONSUMPTION
We have seen that ethanol is common in ripe fruits
and that it is rapidly consumed and metabolized by
frugivorous vertebrates. Frequent ingestion of low ethanol concentrations likely typifies wild frugivores. At
the opposite extreme are rare but consistent accounts
of birds and mammals consuming fermented fruits and
becoming drunk (Siegel and Brodie, 1984; Fitzgerald et al., 1990). Although such accounts still stir debate about whether the animals uncoordinated behavior is due to ethanol or to other compound(s) (Prinzinger and Hakimi, 1996), it is safe to conclude that frugivores occasionally consume highly fermented fruits.
In the temperate zone, this tends to happen in the winter or early spring, when few other resources are available and fruit cells have ruptured due to freeze-thaw
cycles, making them susceptible to fungal attack. Of
more interest are situations in which frugivores have
the opportunity to select among conspecific fruits with
varying amounts of ethanol. This situation is undoubtedly common; probably every fruiting tree presents
unripe, ripe, over-ripe, and rotting fruits, which almost
certainly differ in ethanol content. In such cases, a key
prediction from Dudleys (2000, 2002) hypothesis is

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that frugivores should prefer fruits with higher ethanol


content.
Before summarizing the most relevant studies on
vertebrate fruit preferences, a disclaimer is necessary.
Because no study on fruit selection has considered
let alone measuredethanol concentration in fruits,
one is confronted with the awkward choice of dismissing the entire literature on fruit selection or making a key assumption about how ethanol levels change
as fruits ripen. For the purposes of this review, I will
assume that ethanol concentrations increase as fruits
progress from ripe to over-ripe to rotten. (These stages
of maturation are not discrete. Ripe fruits are typically
intact, symmetrical, and evenly colored, whereas rotten
fruits are characterized by broken skin, asymmetrical
shape, and non-uniform coloration. Over-ripe fruits are
intermediate.) Although this assumption seems intuitivethe more time yeast have to colonize and grow
in a given fruit, the more ethanol will be produced
it may well be false because it does not consider catabolism of ethanol by bacteria or vaporization of ethanol. The only data that address the assumption are
scant: in two species of fruits from Panama, Dudley
(2002) found ethanol concentrations were higher in
very ripe than ripe fruits.
When given a choice of conspecific fruits that vary
in maturation and presumably ethanol content, what
do frugivorous vertebrates prefer? Using artificial infructescences of solanaceous fruits placed in a Costa
Rican cloud forest, Valburg (1992) found a strong
preference for non-rotting over rotting fruits by both
birds and bats. Likewise, Levey (1987 and unpublished data) monitored removal of Hamelia patens
(Rubiaceae) fruits over an annual cycle and found an
extremely strong preference for non-rotted fruits: 76%
of unrotted ripe fruits were removed by vertebrates,
compared to 0% of rotten fruits.
The studies by Valburg and Levey are unique in that
they recorded preferences of wild frugivores for ripe
and rotting fruits. Other studies on fruit choice by wild
birds and mammals are less informative with respect
to ethanol because they focus on preferences between
intact fruits and insect-infested fruits that are not rotting in a way suggestive of ethanol production (e.g.,
Jordano, 1987). Nonetheless, these studies overwhelmingly conclude that frugivores prefer ripe, non-rotting
fruits over damaged or rotting fruits.
Trials with captive frugivores generally mirror results from field studies: frugivores typically reject rotting fruit, regardless the degree of rot (Buchholz and
Levey, 1990; Valberg, 1992; Cipollini and Stiles,
1993). In a particularly rigorous set of experiments,
Cipollini and Stiles (1993) surface sterilized four species of ericaceous fruits and inoculated them individually with one of ten species of fruit-rot fungi. Rotted
fruits were paired with conspecific non-rotted fruits
and presented to frugivorous birds. Overall, non-rotted
fruits were consumed at rates 23 times higher than
rotted fruits, regardless of fruit species. Fungal species,
however, had a major impact on the strength of pref-

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DOUGLAS J. LEVEY

erence for non-rotted fruits. Some species were toxic, severely reducing avian consumption of fruits
they infected (e.g., Alternaria alternata), whereas others had relatively little impact on avian fruit preference
(e.g., Botrytis cinerea). Of particular interest, Saccharomyces cerevisia (a major producer of ethanol), clearly belonged to the non-toxic group, suggesting that
fruits most likely to contain ethanol are also the rotting
fruits most likely to be consumed by birds.
To summarize, rotten fruits are typically discriminated against by frugivores, suggesting that wild frugivores do not prefer ethanol-rich fruits. The only
means of adequately addressing frugivore preference
for ethanol, however, is to conduct preference trials
with experimentally manipulated concentrations of
ethanol. Sanchez et al. (2004) provide the first such
test. They found that Egyptian fruit bats using olfactory cues selected feeders that contained mango juice
over feeders containing dilute solutions of ethanol
(0.001% to 1%).
A caveat about interpreting preference trials is that
a statistically significant preference for fruits with lower ethanol content does not preclude a biologically significant effect of ethanol consumption. Given that vertebrate frugivores typically have very high ingestion
rates (Levey and Martnez del Rio, 2001), that all frugivores tested thus far will consume at least some rotten fruits even when provided with non-rotted fruits
(references above), and that ethanol is present in ripe
but non-rotting fruits, it seems premature to conclude
that a typical frugivores daily rate of ethanol consumption is negligible. Nonetheless, the prediction
from Dudleys (2000) hypothesis that frugivores
should prefer ethanol-rich fruits is not generally supported if one accepts the assumption that ethanol content increases as fruits ripen, become over-ripe, and
rot. Future studies should examine preferences for ripe
versus over-ripe (not rotting) fruit and should experimentally manipulate ethanol concentrations in the
range typical of ripe and over-ripe fruit.
HUMANS, ETHANOL, AND ALCOHOLISM
On first appearance, the literature reviewed above
does not provide strong support Dudleys hypothesis.
Ethanol is ubiquitous in fruits but occurs in relatively
low concentrations. And, in situations where its concentrations are presumably the highest (rotting fruits),
frugivores strongly prefer other fruits; they do not appear naturally attracted to ethanol (see also Dominy,
2004; Sanchez et al., 2004). Assuming that human ancestors were similar to extant frugivores in their consumption of ethanol, a missing part of the hypothesis
becomes apparent: What is a plausible intermediate
stage in the evolution of alcoholism? How does one
progress from low-level consumption of ethanol in
wild fruits to full-fledged alcoholism?
Anthropologists have long recognized the importance of fermented foods in human nutrition. Practically every culture has developed unique and often
elaborate processes of fermentation (Battcock and

Azam-Ali, 1998). For example, in the Andean region


of South America chicha is traditionally made from
pulverized corn (Steinkraus, 1995). Corn meal is prepared by groups of older women, who thoroughly
chew it to produce an intermediate product, muko.
Amylase in their saliva converts starch to sugar in
muko, greatly increasing yeast activity and ethanol
production in the fermentation process that follows.
In an anthropological context, fermentation can be
viewed as controlled spoilage of food. Anaerobic conditions prevent the succession of microbes that would
otherwise completely oxidize the foodstuff. The microbes responsible for the later stages of food spoilage
generally cannot grow in alcoholic or acidic environments. Thus, by culturing the production of alcohols
and in many cases organic acids via limited exposure
to oxygen, the food is protected. Long before refrigeration and synthetic additives, fermentation was one
of the most important food preservation technologies
(Battcock and Azam-Ali, 1998).
Given the ancient and cosmopolitan reliance on fermented foods and the cultural inheritance of their use,
I suggest that humans may not have developed their
current attraction to ethanol via exposure to wild fruits.
Rather, they first encountered high concentrations of
ethanol through fermentation processes that were initially fostered for the purpose of food preservation. As
they discovered the inebriating qualities of some fermented foods, they focused attention on those fermentative processes, ultimately leading to the beer and
wine industries of today.
When viewed in this context, the questions that
structured much of this review can be seen as largely
irrelevant. It does not matter that ethanol concentrations in wild fruits are typically very low or that wild
frugivores seem to avoid fruits with the highest ethanol
content. Neither condition is necessary for exposure of
humans to physiologically meaningful amounts of ethanol. On one hand, Dudleys hypothesis dodges a bulletunsupported predictions are not damning. On the
other hand, an alternative but less satisfying explanation emerges for alcoholism in humans. Addiction to
ethanol may be analogous to addiction to caffeine, nicotine, heroin, or cocaine. All are secondary metabolites that humans have learned to concentrate and that
provide a desired physiological response. The response
is fortuitous, not adaptive. The principal difference between ethanol and most other addictive substances is
that ethanol is produced by fungi, not by plants. However, the evolutionary bases are similarthe adaptive
function of such compounds is likely rooted in competitive interactions with other organisms.
ACKNOWLEDGMENTS
I thank Robert Dudley and Michael Dickinson for
organizing the symposium, In Vino Veritas: The
Comparative Biology of Ethanol Consumption, and
in particular Robert Dudley for encouraging me to
ponder the relevance of the evolutionary triad to alcoholism. Thanks also to participants in the sympo-

EVOLUTIONARY ECOLOGY
sium for spirited discussion and to the National Science Foundation for funding.
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