Public Information: From Nosy Neighbors to
Cultural Evolution
E
´
tienne Danchin,
1
Luc-Alain Giraldeau,
2
Thomas J. Valone,
3
Richard H. Wagner
4
Psychologists, economists, and advertising moguls have long known that human
decision-making is strongly influenced by the behavior of others. A rapidly accumu-
lating body of evidence suggests that the same is true in animals. Individuals can use
information arising from cues inadvertently produced by the behavior of other
individuals with similar requirements. Many of these cues provide public information
about the quality of alternatives. The use of public information is taxonomically
widespread and can enhance fitness. Public information can lead to cultural evolu-
tion, which we suggest may then affect biological evolution.
A
nimals often face decisions such as
where to forage, with whom to mate, or
where to breed, each with different fit-
ness outcomes. To decide effectively, they need
information about the various alternatives. Un-
less conditions are constant, inheriting useful
information about the environment genetically
may be impossible, and so the acquisition of
information becomes beneficial.
There are two ways to acquire information
(Fig. 1): by using trial-and-error tactics to inter-
act with the physical environment (personal
information), or by monitoring others’ interac-
tions with the environment (social information).
Social information can be based on signals—
traits specifically designed by selection to con-
vey information. Alternatively, it can be based
on cues provided inadvertently by individuals
engaged in efficient performance of their activ-
ities (inadvertent social information, or ISI).
The social cues of ISI may indicate the location
of resources when other individuals with simi-
lar requirements for these resources are present
[social attraction (1)] or their behavior is ob-
served from a distance [i.e., local enhancement
(2)]. ISI may also involve public information
(PI) (3) about the quality of the resource when
it is revealed by the performance of other indi-
viduals that share similar environmental re-
quirements (4). Here we deal mostly with in-
stances of PI use.
The reliability of ISI for bystanders re-
sides in the fact that they are not intention-
ally produced; individuals providing them
are selected to perform as well as possible,
rather than to inform others. In particular,
PI provides rich and reliable information
about the quality of al-
ternatives (3, 4). The
benefits of using PI are
that it reduces the costs
associated with trial-
and-error learning and
provides additional in-
formation that can lead
to more accurate esti-
mates of environmental
parameters (5). The use
of ISI can thus vary
from situations where
the bystander parasit-
izes the information
(involving a cost to the
performer), to com-
mensalism (when the
bystander’s use of ISI
is neutral to the per-
former), to mutualism
(when both actors ben-
efit from the use of ISI
by the bystander).
The Diversity of
Public Information
Use
Foraging as public in-
formation. The idea that
animals may observe
others to get information
about resource quality
arose mostly in a forag-
ing context (6). For in-
stance, when Norway
rats (Rattus norvegicus)
face unfamiliar food,
they rely on ISI provid-
ed by the breath of com-
panions to decide on the appropriate prey to
eat (7 ). European starlings (Sturnus vulgaris;
Fig. 2A) and red crossbills (Loxia curviros-
tra) exploit hidden prey and must probe re-
peatedly to estimate the current quality of a
foraging patch. Both species observe their
flockmates’ probing success and use this as
PI to decide when to leave a patch in search
of another (8–10). Scrub jays (Aphelocoma
coerulescens; Fig. 2B) observe and remem-
ber the food caches of conspecifics and pilfer
them when given the opportunity (11). This
use of ISI could involve PI if the pilferer
also uses the information to estimate the
1
U.P.M.C. CNRS-UMR7625, Baˆt A–7e e´tage–Case 237,
7 quai Saint Bernard, 75252 Paris Ce´dex 05, France.
E-mail: edanchin@snv.jussieu.fr
2
Group de Recherche
en E
´
cologie Comportementale et Animale, De´parte-
ment des Sciences Biologiques, Universite´ du Que´bec
a` Montre´al, Case Postale 8888, Succursale Centre-
Ville, Montre´al, Que´bec H3C 3P8, Canada. E-mail:
giraldeau.luc-alain@uqam.ca
3
Department of Biology,
St. Louis University, St. Louis, MO 63103, USA. E-mail:
valone@slu.edu
4
Konrad Lorenz Institute, Austrian
Academy of Sciences, Savoyenstrasse 1a, A-1160 Vi-
enna, Austria. E-mail: r.wagner@klivv.oeaw.ac.at
Fig. 1. The various forms of nongenetically acquired information
(apart from parental effects). Information is anything that reduces
uncertainty. Personal information is acquired individually by interact-
ing with the physical environment. The interaction can generate both
private information (inaccessible to others) and nonprivate informa-
tion that produces social information (red arrow). A behavior can
convey information by design; it is then a signal that is produced by
selection. In many cases, however, social information is produced
inadvertently; it is then a cue, and we refer to it as inadvertent social
information (ISI). Topics covered in this review are in blue. ISI com-
prises cues that indicate the spatial location of resources (based on
the location of the information producers) and cues produced by the
performance of others, which is public information (PI). PI may play a
major role in cultural transmission and evolution. The arrow from the
cues box to the signals box indicates that signals directed to one party
may inadvertently be used by a third party. The use of that informa-
tion by others may create the selective pressures that transform ISI
into signals (34). Thus, PI may be viewed in some contexts as the
platform from which signals evolve.
REVIEW
www.sciencemag.org SCIENCE VOL 305 23 JULY 2004 487
quality of the caches. PI can also be ob-
tained heterospecifically; for example,
nine-spined sticklebacks (Pungitius pungi-
tius) use the feeding behavior of three-
spined sticklebacks (Gasterosteus aculea-
tus) at a poor and a rich patch to select the
most profitable patch to exploit (12).
Habitat copying: Breeding success as
public information. In attempting to repro-
duce, animals must first select an appropriate
place to breed, and PI may be used in the
appraisal of breeding site quality. In two lek-
king antelopes (Kobus kob thomasi and K.
leche kafuensis), for example, experimentally
transplanting soil from successful mating ter-
ritories to less successful ones showed that
females choose the mating territory according
to the odors of female urine, a cue correlated
with former local mating success (13). Like-
wise, birds such as kittiwakes (Rissa tridac-
tyla; Fig. 2C) prospecting for a new breeding
site copy the habitat choices of successful
rather than unsuccessful conspecifics (14). A
large-scale manipulation of the breeding
performance of collared flycatchers
(Ficedula albicollis) showed that local re-
productive success of conspecifics was one
of the cues used in the decision to disperse
to other breeding areas (15). Further exper-
imental studies of collared flycatchers have
suggested that prospectors are attracted to
the most successful sites as judged by
parental feeding activity (16, 17).
The occurrence of habitat copying im-
plies that animals prefer to settle close to
successful conspecifics in order to benefit
from the same favorable conditions (4, 18).
Modeling has shown that habitat copying
can lead to animal aggregation, measured
as significant departures from a null model
of dispersion (5). Once formed, these ag-
gregations can grow because of the Allee
effect (19) produced by PI use: Successful
individuals provide PI about the location of
high-quality habitat. In this context, colo-
nies and other social aggregations appear as
the by-product of habitat selection deci-
sions mediated by PI (18, 20, 21).
Mate-choice copying: Obtaining public
information by watching others mate. Female
mating decisions are often influenced by ex-
posure to the mating interactions of others,
such that mate-choice copying has now been
reported in several species of birds and fish
(22, 23). The mating interactions and deci-
sions of others are a source of PI that allows
an individual to assess more effectively the
quality of its potential mates (22). To ap-
praise the role of social information in mate
choice, it is necessary to separate the signals
deliberately produced by displaying males
from the cues that are inadvertently produced
by the mate choices of the copied females.
Females may choose mates entirely on the
basis of PI if their decisions are based on the
choices of other females that reveal male
attractiveness or quality. This use of PI can,
in some cases, even reverse their own former
choices (24 ). As expected, empirical data show
that females use PI and hence mate-copy when
choosing among potential mates of similar
quality and when lacking the ability to discrim-
inate (i.e., in situations where additional infor-
mation is required to reduce uncertainty) (23,
25). Furthermore, mating preferences influ-
enced by observed mating interactions could
persist over time (24 ). Mate-choice copying
was originally proposed as an explanation of
the marked skew in male mating success ob-
served in many promiscuous lekking species
(26). More broadly, conspecific copying by
both sexes has been suggested as a general
mechanism producing skews in the distribu-
tions of the reproductive commodities being
selected (21).
Eavesdropping: Watching the outcomes of
others’ interactions. Females can obtain infor-
mation about mate quality by observing male-
male interactions. Female birds, for instance,
“eavesdrop” (27) on song competitions be-
tween neighboring males and then seek and
obtain extra-pair fertilizations from the winning
singer (28, 29). When dominant territorial male
black-capped chickadees (Podecile atricapilla)
are defeated in playback-induced countersing-
ing contests against a simulated intruder, they
lose paternity more often than do those exposed
to the playback of a simulated submissive in-
truder (29). PI available through eavesdropping
therefore plays an important role in female as-
sessment of male quality.
Eavesdropping is also suggested by the be-
havior of female fighting fish (Betta splendens)
that mate preferentially with winners of male-
male contests (30, 31), whereas females that
have not seen fights show indifference (32).
Interestingly, the presence of a female audience
increased the fighting rates of males (33), which
suggests that male fights may provide both
signals and cues. Eavesdropping could there-
fore provide a circumstance under which cues
constituting PI can evolve into signals because
of the audience effect (34) (Fig. 1).
Flee-response and damage as public in-
formation about danger. Acquiring informa-
tion about dangers such as predators can be
risky. Not surprisingly, animals have evolved
the ability to detect the level of danger from
the use of cues that may unavoidably accom-
pany it. For instance, the general tendency to
copy flee-responses of an entire flock (or
herd) and to respond to fright or stress signs
of other animals clearly involves ISI and
perhaps even PI. When a predatory fish con-
sumes a prey, the damage inflicted to the
prey’s cells releases chemical substances that
provide PI concerning the ambient level of
predation danger. These so-called alarm sub-
stances have been experimentally demon-
strated in a large number of fishes (35). Even
plants may use this form of PI. Wild tobacco
plants (Nicotiana attenuata), for instance, ap-
parently obtain information from airborne
molecules released by damaged heterospe-
cific neighbors. Untouched tobacco plants
growing among clipped sagebrush (Artemisia
tridentate) neighbors produce more flowers
and seed-bearing capsules than do plants with
unclipped neighbors (36 ), because when
growing under high risk of herbivory they
have a shorter life expectancy and so prema-
turely divert more resources to reproduction
rather than growth.
AC
D
B
Fig. 2. Some of the animals involved in studies providing empirical evidence of the use of PI. (A)
A starling (Sturnus vulgaris; photo by T. J. Valone). (B) A scrub jay (Aphelocoma coerulescens; photo
by N. S. Clayton). (C) A kittiwake (Rissa tridactyla; photo by E. Danchin) and its chick. (D) A guppy
(Poecilia reticulata; photo by S. Nordell).
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23 JULY 2004 VOL 305 SCIENCE www.sciencemag.org488
Public Information and Cultural
Evolution
Cultural evolution. Many kinds of PI use are
akin to true imitation (37 ) and thus may trigger
the transmission of behavioral patterns among
individuals in a process akin to culture. We
define culture as the sum of traditions and
information that vary among groups; the trans-
mission of these differences across generations
rests on social interactions (imprinting, imita-
tion, learning, or teaching) that change the phe-
notype lastingly [definition derived from (24,
25, 38)]. Culture therefore consists of nonge-
netic, heritable differences among populations
(38, 39) and requires overlapping generations
that allow intergenerational transmission of
phenotypic traits.
A recent review (39) underlines the
striking similarities between cultural and
genetic transmissions (Table 1). In partic-
ular, most of the characteristics of evolu-
tion through natural selection (variation,
selective pressure, and heritability) are
shared by cultural selection. A key differ-
ence, however, is that acquired cultural
traits can be transmitted to the next gener-
ation [see (37, 39, 40) for a discussion].
Examples of nonhuman culture include
the song dialects of songbirds and ceta-
ceans (41, 42). Song dialects are by-
products of learning processes that lead to
geographic and group differences in the
details of the songs used by individuals
(41, 43, 44) that may persist outside the
breeding season (45). As expected of cul-
tural evolution, dialect characteristics can
change through time (46); in some cases,
such as in South Pacific sperm whales
(Physeter macrocephalus), dialect charac-
teristics appear linked to foraging success
(42). Moreover, in mountain white-
crowned sparrows (Zonotrichia leucophrys
oriantha), males singing a local dialect
have higher paternity, which suggests fe-
male preference for local dialects. The con-
sequence is that most of the population
variation at microsatellite loci that could
not be attributed to individuals was attrib-
utable to differences among, rather than
within, dialect regions (43). If the effect of
dialects on female mating preferences is
prevalent, then any two populations evolving
different dialects after a sufficiently long sep-
aration may ultimately become unable to in-
terbreed successfully (44), creating a cultur-
ally induced first step toward speciation.
Public information can trigger cultural
evolution. Like true imitation (37), PI can
contribute to the transmission of cultural
traits (24, 39). Examples are numerous.
Mate-choice copying implies the transmis-
sion of a phenotypic trait, a mating preference
based on the behavior of predecessors, that
provides information on the quality of alter-
native mates. Habitat copying, also based on
the publicly acquired information of site
quality, leads to long-lived, multigenerational
traditions of site use that can generate highly
skewed distributions of individuals (many in
one site, few in others) that can perhaps
provide a cultural explanation for the evolu-
tion of avian coloniality (18). The transmis-
sion of toolmaking and tool use (47, 48)
usually involves the performance of the indi-
vidual using the tool, and hence ISI, but
perhaps involves the use of PI if the success
level of the performer influences transmis-
sion. Finally, certain components of dialect
transmission may involve PI if the songs of
winning males are adopted more than those
of losers (eavesdropping), or if song reveals
something about male quality. Such possibil-
ities have not yet been explored.
Heritability, genes, and/or culture? The
widespread use of PI in animal decision-
making requires a reappraisal of the relative
contributions of culturally and genetically
transmitted traits to behavioral evolution. To
study this question, we must consider the
definition of heritability: the fraction of phe-
notypic variance (V
P
) that is transmitted,
which is V
A
/V
P
, where V
A
is additive genetic
variance. An implicit assumption in this def-
inition is that environmental variance (V
E
)
can be reduced to zero. V
E
can be divided into
three components:
V
E
⫽ V
DE
⫹ V
PE
⫹ V
AC
(1)
where V
DE
is the direct effect of environmen-
tal variation, V
PE
is nongenetic parental ef-
fects, and V
AC
is additive cultural inheritance.
Both V
AC
and V
PE
can lead to resemblance
between parent and offspring.
In practice, however, it may be difficult to
control for early parental effects. For exam-
ple, some birds place various quantities of
steroids and antibodies (49) in their eggs,
depending on local conditions. Some studies
(50, 51) claim that mate-choice preference is
heritable, implying a genetic transmission of
mating preferences. However, in most exper-
imental designs, young are raised together,
which allows for sexual imprinting. If this is
so, then mate preference could be transmitted
culturally rather than genetically. Part of the
estimated heritability, which is usually attrib-
uted to genetic additive variance, may in fact
represent parental and cultural variances
(V
PE
⫹ V
AC
). Thus, what is actually mea-
sured is (V
A
⫹ V
AC
⫹ V
PE
)/V
P
.Toour
knowledge, no estimation of heritability has
specifically controlled for the possibility of
either parental or cultural transmission of
preference. Variances and covariances are
traditionally interpreted as pure genetic heri-
tability (52), and even studies published in
behavioral journals interpret repeatability in
mate preferences as indicating genetic varia-
tion (51). Estimations of heritabilities should
therefore consider the potential effect of cul-
tural transmission, especially in studies of
demonstrably acquired behavior. This would
imply the rearing of young in isolation to
avoid any early imprinting.
Differences between genetic and cultural
evolution. The idea of a joint gene-culture ef-
fect on evolutionary processes is not new (53,
54). The differences between cultural and ge-
netic transmissions of traits (Table 1 and Fig. 3)
require contrasting evolutionary properties,
such that evolution in a population with both
genetic and cultural trait transmission differs
deeply from a population without any culture
(39). Cultural transmission can modify selec-
tion pressures (e.g., cultural transmission of
mate preference has the potential to change
sexual selection substantially). Nonrandom as-
sociations between genes and cultural traits can
affect the genetic response to selection. Culture
can spread rapidly, and hence can create strong
selection within a population, because cultural
traits can be transmitted vertically (from parent
to offspring), horizontally (among members of
Table 1. Similarities and differences between genetic and cultural transmission. Much as genes are
the unit of biological information (and thus of natural selection), memes are the unit of cultural
information (and thus of cultural selection). Genes are stored in DNA; memes may be stored in
nervous system or other tissues. Mechanisms of genetic transmission involve DNA duplication,
whereas mechanisms of cultural transmission are diverse and involve imitation, imprinting, and
learning, among others. Behavioral innovations are analogous to genetic mutation, and the
transmission mechanisms lead to heritability in both genetic and cultural systems. Heritability of
genetic traits may be lower than that of cultural traits such as language.
Genetic transmission Cultural transmission
Information unit (replicator) Gene Meme
Information vector DNA Behavior and central nervous system
Transmission mechanism DNA duplication Imitation, social facilitation,
imprinting, learning, teaching
Mutation Duplication errors;
pseudo-genes
Learning errors; innovation
Impact of most mutations Deleterious Unknown
Heritability Yes (low) Yes (moderate to high)
Transmission of acquired
characters
No Yes
Type of process Darwinian Lamarckian
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www.sciencemag.org SCIENCE VOL 305 23 JULY 2004 489
the same generation), and obliquely (from non-
parental members of the previous generation).
For instance, by diminishing within-group vari-
ation and increasing among-group variation,
cultural transmission and conformity to culture
can enhance the effect of selection among
groups relative to selection among individuals,
and can account for the spread of agricultural
practices (37, 39, 55).
Public information, genes, and culture. A
large number of male sexual ornaments are
thought to have arisen through Fisherian sex-
ual selection. Once female preference is fixed
in a population, the evolution of Fisherian
male ornaments can only move in the direc-
tion of greater exaggeration. Yet there is ev-
idence from phylogenetic analyses that the
evolution of exaggerated male traits can be
reversed: Ancestral species in which females
preferred bright males can give rise to daugh-
ter species in which females prefer drab
males (56). This result is puzzling because it
is difficult to explain how a mutant female
with a genetic preference for drab males
could invade a population where females pre-
fer bright males. However, experimental re-
sults obtained with guppies (Poecilia reticu-
lata; Fig. 2D) may provide an answer to this
puzzle. Female guppies appear to have a her-
itable noncultural preference for brightly col-
ored males (52). However, they can acquire a
preference for drab males, provided that they
observe other females mating preferentially
with such males for a sufficiently long period
of time (25). Mating preferences can thus be
reversed culturally through the use of PI.
A Fisherian interpretation for the evolution
of exaggerated male traits rests on the observa-
tion that when females mate with their preferred
kind of male, their offspring inherit both the
male’s exaggerated trait
and the female’s prefer-
ence (57). This joint in-
heritance of trait and
preference was interpret-
ed as implying that genes
that code for male traits
become linked to genes
that code for female pref-
erences. Genes, howev-
er, need not be invoked
at all, and the proper ex-
pression should be that
heritable male traits be-
come linked to heritable
female preference. For
instance, males’ territory
acquisition ability can be
influenced by the quality
of their natal territory.
When this is so, territory
quality can be inherited
without necessarily in-
volving any genetic trans-
mission, a process called
ecological inheritance (58). Similarly, as was
shown in guppies, female preference can be so-
cially acquired when species have overlapping
generations. An association can arise between an
ecologically inherited male ability to acquire ter-
ritories and a culturally inherited female mate
preference for males with such abilities.
An association between a genetic and a
culturally inherited trait is also possible. For
instance, territory acquisition ability can be
genetically inherited, whereas female prefer-
ence for this trait may be culturally acquired.
When this is assumed to be so, gene-culture
models reveal the existence of a parameter
equivalent to linkage disequilibrium between
genes that code for learning capacities and
cultural states (59), implying that links be-
tween genes and culture can be similar to
links among genes themselves. The reversion
of female preferences in some lineages (56)
may thus be explained by cultural inheritance
of mate preferences, with the cultural effect
arising from the use of PI.
Conclusions
PI is a widespread phenomenon that is
emerging as a potential unifying concept in
fields that involve decision-making processes
in which individuals can extract information
from others to assess resource quality. The
use of PI can enrich evolutionary models and
can have marked effects on evolutionary pre-
dictions. Future research should explore the
extent to which evolutionary scenarios are
affected by the use of PI.
A number of important questions about PI
still need to be explored. We know, for in-
stance, that PI use is not limited to cogni-
tively sophisticated organisms, because even
plants appear able to use it. However, it is
likely that an organism’s mechanisms for ac-
quiring PI and processing the information
may be associated to the extent to which PI
will influence its behavior.
Although information is often considered
as a highly valuable commodity, it is not
valuable in all circumstances. In some cases,
using PI may be incompatible with gathering
personal information, leading to a trade-off
between the two. The potential for such a
trade-off highlights the importance of ascer-
taining the relative value of public versus
personal information.
PI may be the major driving force in social
evolution, both as a selective agent for behav-
ioral adaptations and as a population-level pro-
cess that can change evolutionary dynamics, in
particular through its implications in cultural
evolution. Because evidence for the use of PI in
decision-making comes from very different
taxa, it suggests that cultural evolution may be
ancestral and perhaps more widespread than is
currently thought. A productive avenue of re-
search will be to investigate whether a number
of traits currently assumed to be genetically
transmitted could involve cultural processes.
Moreover, although much work has been de-
voted to exploring how biological evolution
affects culture, we suggest that evolutionary
biologists should also consider how cultural
evolution influences biological evolution (37).
A major issue will be to tease apart heritability
that results from the interaction of genes, ma-
ternal effects, and culture. PI may well provide
an effective tool for such studies.
In summary, the ability of individuals to
use PI unites a range of topics as diverse as
foraging, predation, mate choice, habitat
selection, and colony formation. The study
of PI, which is inadvertently produced, may
also enhance our understanding of the evo-
lution of signals and hence communication.
Finally, the public information framework
provides a useful approach for examining
the evolution of culture and its influence on
biological evolution.
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Habitat
Parental effects
Gene pool
Gene pool Meme pool = Culture
Learning Horizontal
Inadvertent
social
information
Oblique
Heritable information
Vertical
Meme pool
Private information
Generation n
Generation n + 1
Fig. 3. The role of PI and other forms of ISI in relation to genetic and
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R EVIEW
www.sciencemag.org SCIENCE VOL 305 23 JULY 2004 491
![Fig. 3. The role of PI and other forms of ISI in relation to genetic and cultural transmission. During development, individuals learn environmental types through maternal effects and imitation. Learning can involve private or social information. As a major source of information extracted from conspecifics, ISI and PI in particular lead to the emergence of culture. The effects of ISI and PI as selective agents for better learning and imitation feed back to the gene pool (hence to genetic evolution). Both genetic and cultural information are then transmitted to the next generation. An important difference between genetic and cultural transmission is the latter’s capacity to transmit traits both horizontally and obliquely. [Adapted from (58)]](/figures/fig-3-the-role-of-pi-and-other-forms-of-isi-in-relation-to-3cf88oxb.webp)