Costly signaling and the handicap principle in hunter-gatherer
research: A critical review
Duncan N. E. Stibbard-Hawkes
Department of Anthropology, Durham
University, Dawson Building, South Rd,
Durham, United Kingdom
Duncan N. E. Stibbard-Hawkes, Department of
Anthropology, Durham University, Dawson
Building, South Rd, Durham DH1 3LE, UK.
The Leakey Foundation, Grant/Award
Numbers: JEAG/056, RG75255
It has been argued that men's hunting in many forager groups is not, primarily, a means of family
provisioning but is a costly way of signaling otherwise cryptic qualities related to hunting ability.
Much literature concerning the signaling value of hunting draws links to Zahavi's handicap prin-
ciple and the costly signaling literature in zoology. However, although nominally grounded in the
same theoretical paradigm, these literatures have evolved separately. Here I review honest sig-
naling theory in both hunter-gatherer studies and zoology and highlight three issues with the
costly signaling literature in hunger-gather studies: (a) an overemphasis on the demonstration of
realized costs, which are neither necessary nor sufficient to diagnose costly signaling; (b) a lack
of clear predictions about what specific qualities hunting actually signals; and (c) an insufficient
focus on the broadcast effectiveness of hunting and its value as a heuristics for signal recipients.
Rather than signaling hunting prowess, hunting might instead facilitate reputation-building.
costly signaling, food sharing, Hamilton-Zuk, handicap principle, honest signaling, hunting
1.1 |Food redistribution, the sexual division of labor
and the puzzle of human hunting
The costly signaling or showoff hypothesis in anthropology has been
put forward as a solution to the proposed puzzles of human hunting
acquisition patterns. Hunting is a near-universal and often vital human
subsistence activity with a long evolutionary history. Hunting and
food sharing or redistribution of some form are universal to almost all
mobile forager societies.
Hunting with specialized weaponry dates
back at least 400,000 years
and butchery at least 2.6 million years
perhaps 3.39 MA.
It is highly plausible, based on models of
homology, that small to medium-bodied mammals were hunted by the
human/Pan last common ancestor.
Hunting has also been implicated
in the expansion of the human brain
and the evolution of human life-
history and capacity for social learning.
It is surprising, therefore, that
a general consensus on the ultimate adaptive functions of human
hunting has yet to be reached.
Many authors argue that hunting is primarily a subsistence activ-
ity through which hunters seek to provision themselves,
and their close kin.
Three patterns, frequently
observed among living and ethnographically documented forager
populations, however, have led others
to argue that direct self-
and family-provisioning is not the sole purpose of hunting.
Firstly, among many hunter-gatherer populations men and
women typically pursue different, often nonoverlapping sets of
Among most forager groups, including the Hadza,
Aché, San, Semang, Andamanese, Mbuti, Tiwi and many others,
men do the majority of hunting (Figure 1) and women gather the
majority of plant material. Even among groups like the Martu, where
women also hunt, men pursue larger game species than do women,
which are more widely shared and less reliably attained.
Secondly, many forager populations engage in regular and wide-
spread food sharing. Certain foods, especially those such as game spe-
cies that come in large packet sizes, may be shared or otherwise
redistributed widely beyond the household or nuclear family of the
individual who procured the food.
This phenomenon has been stud-
ied in detail among the Hadza, Aché, Tsimané, Hiwi, Mer Islanders,
Lamalera and! Kung (Ju/‘hoansi),
and is common in numerous
Thirdly, in many forager groups, it has been proposed that, after
accounting for food-redistribution, male resource acquisition patterns,
Abbreviations: MA, million years ago; RS, reproductive success.
Received: 14 February 2018 Revised: 6 November 2018 Accepted: 9 January 2019
Evolutionary Anthropology. 2019;1–14. wileyonlinelibrary.com/journal/evan © 2019 Wiley Periodicals, Inc. 1
and especially the targeting of big game, often appear energetically
suboptimal for familial provisioning,
‘settling for smaller foraging
incomes than time would allow’
and failing to maximize individual or
family resource acquisition rates in terms of net energy gathered per
Independent explanations have been proposed to account for
these patterns, each reviewed elsewhere. The fact that men more
often hunt than do women is viewed, by several authors,
consequence of the burdens of childcare in natural fertility (noncon-
traceptive) populations. From this perspective, the phenomenon is
framed as a sexual division of labor; a means of specializing in tasks
that either are or are not compatible with nursing, such that parents
may most efficiently provision their offspring.
have argued that the sharing or redis-
tribution of hunted quarry may act as a reciprocal insurance policy,
“storing meat in the bellies of... neighbors”
to buffer against short-
falls and lean periods, a behavior sometimes policed with third- or
This theory is widely supported,
although in populations where sufficient quantitative data are avail-
able, in no case could givers expect 100% of contributed food to be
It has also been proposed that food-redistribution might
be the consequence of “tolerated scrounging”or theft.
the tolerated scrounging model predicts that when an individual has a
large quantity of food, and so is sated, it becomes more worthwhile
for hungry neighbors to attempt to take that food than it is for the
owner to defend it.
Finally, it has been proposed that food redistri-
bution can be explained by inclusive fitness,
and people might pref-
erentially channel foods to close consanguineal relatives.
conversely, food is generally redistributed or shared out widely and
often indiscriminately with neighbors and, furthermore, forager camps
are often composed of individuals who are not closely related.
The notion that men target energetically sub-optimal resources
has been debated case by case. For instance, Hawkes
Aché men could, instead of hunting, more profitably spend their time
processing palm starch. Revised estimates of the caloric value of palm
starch show that male Aché foraging out of camp (including hunting)
gives a higher net energy gain than does palm processing.
Hawkes et al.
argued that, after food redistribution, an Aché
hunter's take-home caloric acquisition rate for foraging is still signifi-
cantly smaller than it is for palm starch processing. Similarly, Hawkes
have argued that, accounting for redistribution and shar-
ing, Hadza large game hunting is not a sensible means of maximizing
food acquisitions for oneself or one's nuclear family. Wood and Mar-
have criticized this claim, and have argued that Hadza men's
foraging decisions are not energetically sub-optimal and, moreover,
that food preferentially flows to consanguineal and affinal relatives of
the hunter. The debate is ongoing.
In sum, food redistribution, the sexual division of labor, and the
extent to which men target apparently energetically suboptimal
resources have each been framed as puzzles
; deviating from pat-
terns expected if hunters were seeking to most efficiently optimize
caloric intake for themselves and their families.
Each of these
phenomena has been either called into question
or accounted for
However, an alternative idea seeks to solve
each of these puzzles with a single, theoretically parsimonious frame-
work and sees men's hunting resource acquisition patterns as primar-
ily a means of showing off or honestly signaling qualities related to
1.2 |Showing off, costly signaling and the evolution
of Men's work
In 1985, Kaplan and Hill
found that Aché men who, on average,
brought back more meat, were more likely to be named as the fathers
of children with women who were not their primary partners.
Although the sample was small and, although Kaplan and Hill
clear that the relationship was not necessarily causal, they highlighted
the possibility that women may “attempt to pass on any genetic com-
ponent of hunting skill to their own sons by choosing good hunters as
mates.”In 1991 Hawkes
and Hawkes et al.
expanded upon this idea. They highlighted the fact that men appeared
to preferentially target those resources such as large game redistribu-
ted widely beyond the hunter's own nuclear family. They suggested
that the goal of men's hunting was to provide periodic bonanzas
which would advertise their skill as hunters to prospective female
partners (though see Reference 42), and might gain them favorable
treatment from neighbors, or play a role in male–male competi-
They called this theory the showoff hypothesis. They also
argued that showing off could parsimoniously account for the prepon-
derance of food-sharing and redistribution in the ethnographic litera-
ture, the sexual division of labor as well as the fact that men targeted
resources which appeared, in their view,
not a relatively optimal
means of nuclear family provisioning.
The showoff hypothesis provided a compelling alternative to the
idea that food-sharing and redistribution is a form of reciprocity. Reci-
procity, though still a popular explanation,
had already been
discussed comprehensively by 1991.
Hawkes and others
were critical of the reciprocity model for several reasons. They argued
that reciprocity entailed a collective action problem and that the recip-
ients of shared food would regularly benefit by cheating and shirking
their responsibilities to reciprocate.
Furthermore, they argued that
reciprocal food sharing required producers to control the distribution
FIGURE 1 A Hadza man whittles the shaft of a bow. Although Hadza
women may occasionally acquire small game, the majority of hunting,
including the preparation of bows, arrows and poisons, is done
by men [Color figure can be viewed at wileyonlinelibrary.com]
of the food they acquired, a fact not true for all forager groups.
argued that, in resource-limited environments, food is
inherently valuable. By targeting widely redistributed resources, there-
fore, hunters may attract favorable attention from potential mates,
rivals and allies
and/or signal their “hidden qualities”, skills or abili-
ties to other interested parties.
In this way, hunters may convert
food into reproductive success (RS) or more intangible benefits such
as alliances, status, or respect.
The showoff hypothesis also provided an explanation for the sex-
ual division of labor. Unlike the nuclear family provisioning model,
which stressed cooperation between sexes, the showoff hypothesis
framed sex-biased resource acquisition patterns as the consequence
of intersexual conflict.
argued that men and women
gain RS in fundamentally different ways because women pay a greater
energetic cost for reproduction than men and because men have a
higher potential reproductive rate than women. For this reason
argued that men are more likely to earn fitness from target-
ing widely redistributed resources than are women.
This view led to a third claim. Proponents of the showoff hypoth-
esis argued that men in forager groups targeted resources which,
when considered from the perspective of an individual or nuclear fam-
ily, were not optimal means of maximizing caloric intake either
food redistribution. In this way, Hawkes et al.
argued, food acquisition patterns bore high opportunity costs—
hunters could be seeking alternative resources which would be less
widely shared or otherwise redistributed. Bird
and Hawkes and
argued that these patterns of resource choice only made sense
if the goal of men's hunting was not to cooperate with their wives to
maximally provision their families but was, instead, to share food
In 2002 Hawkes and Bird
drew a direct comparison between
hunting and Zahavi's handicap principle. Zahavi
proposed that the
apparently wasteful traits or displays, often observed in nature, might
act as unfakeable honest advertisements of health, fitness, or other
heritable but otherwise cryptic characteristics. Hawkes and Bird
proposed that, due to the perceived costliness of men's food acquisition
BOX 1 HONEST, COSTLY OR HANDICAP SIGNALS: NOTES ON TERMINOLOGY
Various terms have been used to refer to systems of honest signaling. These can become confusing. To compound this problem, the
term costly signaling has had varying meanings. To provide clarity, I here provide a brief glossary of common terms:
The Handicap Principle Zahavi's original hypothesis. Describes the idea that organisms may advertise otherwise hidden characteris-
tics, relevant to other organisms, by investing in highly observable costly signals. As the name specifies, this model assumes that signals
necessarily involve a handicapping strategic realized cost, rather than just a potential cost.
Honest Signaling The term which is now preferred in much of the literature on the topic. Describes the idea that organisms may
advertise honestly otherwise hidden characteristics via correlated, observable signals, though does not necessitate that such signals
involve a cost to the signaller.
The Hamilton-Zuk Hypothesis Honest signaling where the signaled quality is specifically endo/ectoparasite resistance, usually
through bright colouration/pigmentation. Hamilton and Zuk
avoided the word handicap because females are not seeking handicaps,
but signals of health which cannot be bluffed.
Costly Signaling Although much classic literature used costly signaling synonymously with Zahavi's handicap principle, in more recent
costly signaling refers to the idea that signal honesty is maintained via a cost either realized or potential.
Such costs need
not necessarily be handicapping realized strategic costs.
Indices Maynard Smith and Harper
defined indices as “signals that are reliable because they cannot be faked,”and saw them as
distinct from signals involving a cost. Higham
has argued that indices, from a game-theoretical perspective, are costly signals where
the costs of cheating are infinite. Biernaskie et al.
have defined indices differently as signals “where physiological or developmental
mechanisms create a causal link between quality and signal size.”Biernaskie et al.
have argued, contrary to Maynard Smith and
that “the strength of a causal link between quality and the growth of a particular trait may indeed be adjusted by selection”
and can be modeled using a costly signaling framework. For a fuller discussion of this distinction, see Reference 67.
Alignment of Interest Signals Signals where both the receiver and the signaller benefit from the honesty of the signal
(e.g., communication between relatives) and so have aligning interests. Here there is no incentive for cheating and so no cost is required
to maintain the honesty of the signal.
The Showoff Hypothesis Hawkes
originally highlighted the fact that hunters, among many forager groups, pursued resources that are widely
redistributed and proposed that this might be a means of showing off to mates, allies and rivals. Earlier research on the showoff hypothesis
drew no explicit link between hunting/food redistribution and Zahavi's handicap principle.
Costly Signaling Since 2002,
this term is nearly always preferred in the human hunting literature. In the context of hunter-gatherer
studies, the model is effectively identical to the showoff hypothesis, although makes explicit the link to Zahavi and Grafen on strategi-
cally costly signals.
patterns, hunting may operate similarly and might signal “hunting prow-
ess.”This they referred to as costly signaling.
have sought to draw a distinction between the
showoff and costly signaling hypotheses of hunting, on the basis that
the former predicts only that hunters gain social attention and mating
while the latter is heavily influenced by Zahavi and sees
hunting as a signal of otherwise cryptic qualities, akin to animal signals
like peacocks' tails.
In fact there are few substantive differences
between the two and, to a certain extent, the latter has succeeded
the former. Both hypotheses provide pragmatically identical explana-
tions for food-sharing/redistribution and the sexual division of labor.
Both hypotheses make the same predictions about the relationship
between hunting success and lifetime RS. Furthermore, the terms are
often used interchangeably and proponents have, at various times,
advanced more than one of these views.
the costly signaling hypothesis is usually explicitly linked to the handi-
some early articles on the showoff hypothesis do
mention Zahavi's article in passing,
while some articles that use the
term costly signaling do not.
idea provided a ready-made theoretical framework by
which to analyze human hunting. It also well paralleled the showoff
hypothesis, to the extent that Bliege Bird and Smith
that “we find it remarkable that the rules that govern the (genetic)
evolution of signals such as peacocks’tails and gazelle stotting seem
to have such promise in explaining human signaling behavior which
varies independently of genetic change.”However, the costly signal-
ing framework (Box 1) has been subject to much discussion and fur-
ther scholarly work within the broader evolutionary sciences, not all
of which transitioned to the hunter-gatherer literature. To appreciate
this, it is useful to provide theoretical context for Zahavi's idea and
consider some of the ways in which the handicap principle and costly
signaling model have been developed further since 1975.
2|HANDICAPS AND THE HONEST
SIGNALING HYPOTHESIS IN ZOOLOGY
2.1 |Darwin, Fisher and the puzzle of the
The handicap principle was proposed by Zahavi
to solve a problem
highlighted by Darwin; Many species, such as peacocks (Figure 2), stag
beetles and birds of paradise are “provided with appendages which
appear to be no use... for the ordinary purposes of life.”
In the con-
text of ecological selection alone, the vivid colouration, horns, antlers
and exhausting mating displays of many species appear to represent
termed “a great waste of vital power”and may
increase vulnerability to predation. Darwin deduced that RS is related
not only to an organism's ability to survive in its environment but also
to reproduce with the opposite sex. Sex-specific weapons such as ant-
lers are of clear utility in intrasexual mate competition. Darwin argued
that those sex-specific characteristics not used in direct intrasexual
competition exist due to choice exerted by mates: individuals “by
selecting, during thousands of generations, the most melodious or
beautiful (mates), may produce a marked effect.”
Darwin's theory of sexual selection provides a powerful explana-
tion which, 160 years later, is almost universally accepted. Sexual
selection alone, however, does not explain why certain characteristics
are preferentially selected over others, nor the frequent occurrence of
costly, cumbersome and seemingly wasteful secondary sex character-
istics. The best explanation that Darwin could offer was that, just as
with humans, preferences may appear arbitrary or may fluctuate; the
choosy sex may be “capricious”in its assessment of beauty
must not judge the tastes of distinct species by a uniform standard.”
was the first to propose an explanation for the existence
of sexually selected traits that appear exaggerated and apparently
wasteful. He argued that exaggerated characteristics are caused by a
runaway process in which successive generations of mate choice
amplify not only trait size and intensity but also the strength of mate
preference. Characteristics that are “a fairly good index of natural
become hallmarks of mate choice. As aesthetic prefer-
ence is also heritable and, as individuals with preferences for certain
heritable characteristics tend to mate with individuals who display
those characteristics, heritable characteristics become linked to a heri-
table aesthetic taste for the same characteristics. This taste or prefer-
ence is amplified over successive generations, in turn causing the trait
itself to become increasingly exaggerated. This process eventually
reaches equilibrium when the competing forces of ecological and sex-
ual selection become balanced.
Fisher's runaway selection accounts for the apparent wasteful-
ness inherent to many costly traits and behaviors; removed from the
FIGURE 2 A wild peacock in Rajasthan, India. Its vibrant plumage and
large train play an important role in mate choice although appear to
be a hinderance in other contexts. Zahavi
proposed that such
ornaments act as handicaps, allowing individuals to demonstrate
otherwise hidden qualities [Color figure can be viewed at
context of sexual selection they are the nonadaptive, coincidental by-
products of a positive feedback loop in heritable mate preference.
However, runaway selection cannot account for apparently wasteful
traits and behaviors that appear in situations where characteristics
and preferences are inherited separately such as predator–prey inter-
actions or direct intra-sexual contest competition.
2.2 |Zahavi, Grafen, and the handicap principle
The handicap principle, variously known as costly or honest signaling
(though see Box 1 for disambiguation) gives another explanation for
the evolution of apparently costly or wasteful traits. Zahavi, in his
(1975) article Mate Selection - A Selection for a Handicap, proposed
that the wastefulness of seemingly costly traits is a functional and
adaptive means of revealing certain otherwise hidden qualities of the
signaller. Zahavi (1975) argued that, by being genuinely wasteful or
dangerous, costly displays are impossible to emulate without incurring
those risks or costs. By handicapping themselves, individuals in prime
condition with energy to spare may reliably signal qualities such as
vigor and vitality to prospective choosy mates, predators or rivals in a
way that other less fit or healthy conspecifics could not afford. The
cost of handicap signals, the hypothesis states, is adaptive as it makes
the signal difficult to fake. In doing so, costs reduce the prevalence of
cheaters and thus reduce the cost of attending to the signal for the
signal receiver. Zahavi
was the first to bring the idea to biology. The
use of costs to create signal honesty had been proposed 2 years ear-
lier in the economics literature,
but unlike Zahavi, Spence did not
propose that individuals must pay a high cost to give their own signal
in order for that signal to be honest.
When it was proposed in 1975, the handicap principle was met
In an early model, Maynard Smith
that “the handicap principle appears not to work.”Dawkins
that the theory could be applied to any trait or behavior which
seemed, prima facie, to be costly, wasteful or altruistic and commen-
ted that “If we observe an animal doing something really silly, like
standing on its head instead of running away from a lion, it may be
doing it in order to show off.”
In 1990, Grafen
modeled the handicap principle game-theoreti-
cally. This model was framed in the context of female-choice mate
selection, although Grafen generalized his results to other signaling
interactions such as between predators and prey or in intrasexual
competition. Grafen's model employed three variables: the first was
some male quality (q), which males could not alter and was hidden to
females but which, if they could observe it, would be selected for by
female mate choice. The second variable was advertising level (a),
which was observable to females. The variable qcould be converted
into awith the function A(q). Natural selection could alter the level of
advertisement for males of any given quality q. The third variable was
female preference pfor a. Grafen assumed that male fitness depends
on a,p, and q, and that female fitness is reduced by the discrepancies
between pand qacross all males in a population.
Grafen showed that handicapping signaling systems could exist in
evolutionary stable equilibrium where (a) signaling (a) is an honest
index of quality (q) for all signallers, (b) signals are costly at equilibrium
(i.e. all signallers pay a strategic cost in terms of ecological “viability”
when the competing forces of mate choice and ecological selection
become balanced), and (c) more intense signals are costlier for low
quality signallers than high quality signallers. Higher quality males sig-
naled more intensely at equilibrium than lower quality signallers in this
scenario because, although increases in advertising level give the same
increase in female preference (p) for all individuals, the marginal fit-
ness costs of increasing advertising level (a) were lower for higher
Grafen's model led to general acceptance of the handicap princi-
Zahavi's citation rate reached 50 per year within 4 years of Gra-
fen's articles, and accelerated thereafter.
Since 1990, variations on
the handicap principle, often citing Zahavi and Grafen, have been
invoked to account for a diversity of morphologies and behaviors in
numerous species from different orders, not limited to female prefer-
ence sexual selection but including predator–prey, parent-infant, and
intra-sexual signaling interactions.
Grafen interpreted his model as evidence for the handicap principle.
However, later authors, employing models similar to Grafen's (see Refer-
ences 64,65), showed that to ensure a reliable correlation between signal
it was not necessary that signallers paid realized strategic
costs at equilibrium that guaranteed the honesty of signals—there only
needed to be a potential cost for deviating from honest equilibrium.
An equilibrium is reached for a particular signaller when an
increase in advertisement level is more costly in terms of ecological
viability than any additional fitness gained through influencing
receiver behavior. So long as the equilibrium for signallers of all levels
of quality is stable, and advertising levels for all individuals are differ-
entiated and correspond to the quality being advertised, then signals
maintain their honesty. Strategic
signallers pay high realized strategic costs at equilibrium, is only one
such mechanism included under the umbrella of costly signaling. Pun-
ishment of cheaters, where individuals are punished for signaling dis-
honestly, is an alternative mechanism where, although it is costly for
signallers to deviate from an honest equilibrium, signallers need not
pay any realized strategic costs (Box 2). Indices, that is, signals which
are reliable because they are impossible to fake (Boxes 1 and 2), may
also provide a mechanism by which signal honesty is guaranteed with-
out associated strategic costs, although this framing of the index con-
cept has been criticized (see Reference 67).
For this reason, Számadó,
that costly signaling and the handicap principle are not one and the
same (Box 1). Handicap signaling sensu Zahavi
predicts that signal-
lers must necessarily pay a realized strategic cost, while costly signal-
ing is any system by which signal honesty is maintained at equilibrium
through costs incurred for signaling dishonestly by deviating from that
equilibrium (potential costs), though which need not involve realized
strategic costs. This distinction, and the associated logic, is important
when considering how scholars might recognize and identify costly
signals in their empirical research.
2.3 |Recognizing and researching honest and costly
Honest signaling theory and the handicap principle, “has become one
of the most enduring and well known of all theories in... behavioral
Despite this, many authors
have argued that much
of the literature on signaling among animals and humans does not pro-
vide evidence sufficient to demonstrate that traits and behaviors do
indeed act as honest signals. In fact, conclusive evidence may be diffi-
cult to find. However, there are several conditions which researchers
may look for. The first is that:
A) Signals affect probabilistically the behavior of a signal recipient.
A signal is defined by Maynard Smith and Harper (2003) as “any
act or structure which alters the behavior of other organisms, which
evolved because of that effect, and which is effective because the
receiver's response has also evolved.”This definition specifies acts
and structures “evolved”at the exclusion of socially learned behaviors
though to sensibly broaden the definition, “appeared”may be
substituted for “evolved.”This definition is useful because, unlike
some other definitions (see Reference 70), it makes no claims about
the information content of the signal, nor the proximate mechanisms
by which receivers perceive and respond to signals.
To show that a trait or behavior fits this definition one must show
that such traits or behaviors affect probabilistically the behavior of a
signal recipient. In the case of sexually selected signals, one must dem-
onstrate that the intensity of a signal is related to the probability of
mating. In the case of predator/prey interactions, one must demon-
strate that signaling intensity decreases the likelihood of pursuit.
This condition may be demonstrated via experimental manipula-
tion, as has been neatly done with widowbirds, Euplectes spp..
Correlational data may also be sufficient to demonstrate this condi-
tion, as is often seen in the anthropological literature.
tal manipulation may allow researchers to conclude more confidently
that a signal affects the behavior of a recipient than does correlational
research, although experimental research is less often possible due to
the difficulties, ethical and practical, of manipulating the intensity of
signals. Showing that traits affect the behavior of recipients does not,
BOX 2 DEEP CROAKS: DO HONEST SIGNALS NECESSARILY INVOLVE REALIZED COSTS?
Zahavi and Zahavi
stated that reliable signals must entail a realized cost to the signaller which serves to guarantee the honesty of the
signal, hence the name handicap signaling (Box 1). Maynard Smith and Harper
termed these strategic costs. There are, however, many
mechanisms by which honest signals need not involve strategic costs and need involve only low or negligible realized cost.
For example, strategic costs are not necessary where signaller and receiver have aligned interests and there is no benefit to cheating
(e.g., a parent and a lost infant both benefit from being reunited
Furthermore Maynard Smith and Harper
draw a distinction between indices—‘signals that are reliable because they cannot be
faked’—and handicaps—“signals that are reliable because they are costly to produce.”For example, among European toads, Bufo bufo,
vocalization (croak) depth reliably indicates body size.
Body size is, in turn, reliably correlated with fighting ability. Other toads use
croak depth in their assessment of fighting ability. Here croak depth also acts as an honest signal. Croak depth (signal intensity),
although it entails the efficacy cost of growing vocal cords, does not require any extra strategic investment in sound-producing appara-
tus. It is an acoustic byproduct of body size, that Maynard Smith and Harper
argue, poses no additional strategic cost yet is impossible
to fake (Although contra see
Biernaskie et al.
have criticized this distinction, and have argued that signals such as toad's body sizes, which are dependent on
highly conserved developmental or physiological mechanisms such as the insulin/insulin-like signaling (ILS) pathway in growth, might
not be statically constrained by condition nor, hypothetically, impossible to fake. For example an individual toad could, hypothetically,
increase growth by diverting resources away from other important physiological processes—although individuals in poor condition may
pay a prohibitively high marginal cost to do so. In this way, they argue, many proposed indices can still be modeled in a costly signaling
framework. Importantly, however, depending on the particular system, this process still need not necessarily involve realized strategic
costs (handicaps) and instead need only require a “disproportionate production cost of faking a dishonest signal”for “low-quality individ-
uals”Biernaskie et al.
Finally, costs can be borne by individuals who do not signal honestly through changes in receiver behavior. Individuals who give a
false signal may, for example, be subject to punishment.
This has been demonstrated empirically via manipulation of status badges in
article wasps (Polistes dominulus), house sparrows (Passer domesticus) and great tits (Parus major),
although the validity of the evidence
Additionally, traits and behaviors involving realized costs can appear without signaling. To give just one example, when a bird
invests time and energy into incubating the eggs and feeding the chicks of a brood parasite such as a cuckoo or cowbird, it pays a real-
ized cost not because it is signaling, but because it cannot discriminate between its own and another's offspring.
It is clear, then, that although certain animal signals might involve a realized strategic costs, apparent costs are neither necessary
nor sufficient conditions of honest signaling. Costly signals can involve potential, rather than actual costs. Apparent realized costs can
appear in nonsignaling contexts. Further, even in signaling contexts, it is impossible to empirically distinguish between strategic costs
and efficacy costs.
Evidence for apparent realized costs associated with a particular trait or behavior therefore, does not, itself, provide
positive evidence for either costly signaling or handicap signaling.
however, allow us to distinguish between signals—those traits or
behaviors that have evolved or appeared because of the effect they
have on a recipient—and cues—those traits that affect the behavior of
a recipient but have not appeared because of that effect.
Another necessary condition of honest signals, and a central
assumption of Grafen’s
model is that:
B) Signals are reliably correlated with a signaled quality which is oth-
erwise cryptic or difficult to observe.
To demonstrate this one must show “a good correlation between
the signalling trait and the trait being signalled”.
This condition is often difficult to demonstrate empirically.
Although many traits and behaviors appear to act as signals, the cryp-
tic trait being signaled is often hard to measure or observe. To com-
pound this difficulty, the signaled trait may not be fixed or stable
(e.g. nutrition), may relate to external factors that vary spatially
(e.g. parasite resistance), or may only be measurable at certain points
during the lifespan (e.g. resistance to developmental stress). Further-
more, where there are trade-offs between signal intensity and under-
lying condition, no correlation may be observed in cross-sectional
studies and without experimental manipulation of signal intensity. In
some cases authors may not even propose a specific signaled trait.
Nonetheless, in many cases signal intensity is demonstrably corre-
lated with a signaled quality. For example, Møller and de Lope,
experimentally shortening the tail feathers of barn swallows, Hirundo
rustica, showed that those with longer tails (higher signal intensity)
were better able to survive and forage once their tails were artificially
shortened than were those with naturally shorter tails. Using correla-
tional data, FitzGibbon and Fanshawe
showed that those Thomson's
gazelle which stotted—jumped high into the air—more often outran
predators. If it can be shown that traits or behaviors reliably affect the
behavior of a signal recipient and are also correlated with a signaled
quality, a strong case can be made that such traits act as honest sig-
nals, although it is again difficult from this evidence alone to distin-
guish signals from cues.
There are several further considerations. As mentioned previ-
ously, Zahavi and Zahavi
have argued that “to be reliable, signals
have to be costly.”If this claim is true, it must be demonstrated that:
C) Signals have an associated strategic cost.
This condition is often cited in the literature on honest signaling in
humans and much of the debate about human hunting as costly signal-
ing has centered around whether men's hunting acquisition patterns
are inherently costly when accounting for food redistribution.
However, while certain animal signals do appear to impose a cost,
as argued by Számadó
and put well by Biernaskie et al.
tenance of honesty does not require a realized cost paid by honest
signallers, as in Zahavi's view of the handicap principle, but rather a
potential cost for dishonesty”(see Box 2). The demonstration of cost
itself may be sufficient to distinguish between strategic signals, which
involve a realized strategic cost, and other types of costly signaling
where costs are paid by potential deviations from an honest equilib-
rium. However, even this endeavor is complicated by the fact that it is
impossible to empirically distinguish between strategic realized costs
(involved in maintaining as signal's honesty) and realized efficacy costs
(involved only in ensuring the signal reaches its recipient).
tantly, although questions might be raised by the fact that a certain
trait or behavior appears, prima facie, to probabilistically impose a
realized fitness cost on the organism, this fact alone is neither neces-
sary nor sufficient evidence of costly signaling. Instead, as suggested by
Lachmann et al.
Bergstrom et al.
and restated by
it might be more enlightening to force individuals to exhibit
signals of increased intensity and sustain out of equilibrium costs.
Here, however, such experimental research may be neither ethical nor
There are two further related considerations, less often discussed:
D) Signals, even those involving strategic costs, must be efficacious
means of broadcasting information to signal recipients.
E) Efficacy costs should be as low as possible to the signaller.
Signals benefit both the receiver and the signaller by being con-
spicuous and easy to read. This is because, if a signal is not a quick,
reliable and effective means of broadcasting information to a signal
recipient, then the benefit of attending to that signal is diminished. In
turn, if the signal is ignored by the receiver, there is no benefit to the
signaller in signaling. This selects for signals that are conspicuous and
take little time and energy for the recipient to interpret.
Producing signals most likely to reach their target may involve an
to the signaller, which does not increase the signal's
honesty or reliability and is, thus, not a handicap in the Zahavian
sense. Efficacy costs have received less attention than strategic costs
because, in practice, there is no universally reliable methodology for
distinguishing between the two.
However, as Higham et al.
argued, “there is a need to incorporate more elements of signal effi-
cacy into existing frameworks and theory.”Furthermore, selection
should be expected to minimize efficacy costs, while maximizing signal
3|THE STATE OF THE EVIDENCE FOR
HUMAN HUNTING AS A COSTLY SIGNAL
3.1 |Where are we today? The current status of the
costly signaling hypothesis in hunter-gatherer studies
The costly signaling explanation of human hunting is not universally
has questioned why, if hunting is a form of compe-
tition, men state a preference for living in the same camp as better
hunters. Wood and Marlowe
have questioned the assumption
that Hadza food acquisition patterns are calorically suboptimal or
costly. Furthermore, Gurven and Hill
have argued that costly signal-
ing alone is inconsistent with the fact that men in forager groups,
rather than being entirely motivated by showing off to others, are
often directly involved in provisioning and childcare. They have
argued that there are multiple pathways by which men's foraging
Despite these concerns, the costly signaling model has been widely
cited and highly influential. It is regularly referenced in recent work on
human hunting, foraging and food sharing/redistribution
familiar to most evolutionary anthropologists. There is also much posi-
tive evidence for the costly signaling hypothesis, predominantly of two
types. Much research links hunting reputation and hunting success to
measures of mate choice and RS.
There is also a body of literature
highlighting the fact that, among many forager groups, men acquire
resources that are more widely redistributed beyond a hunter's nuclear
family than those acquired by women
and therefore appear to
represent a cost.
Men's hunting acquisition patterns appear to meet some, but not all
of the necessary conditions of honest signaling outlined in Section 2.3.
Here I outline the state of the evidence for hunting as a costly signal,
and highlight three issues which require further consideration.
3.2 |Strength of the evidence for hunting as a
3.2.1 |Hunting and mate choice: An effect on the signal
Hunting is often positively related to measures of RS and better
hunters may have more or younger mates.
If human hunting is a
costly signal this may fulfill the requirement that receivers (in this case
prospective partners) attend and respond to the signal. This is not true
of all populations, however.
Furthermore, costly signaling of hunt-
ing skill is not the only possible explanation for this pattern. Better
hunters might make more desirable partners simply because they bet-
ter provide for their families although Hawkes et al.
this argument on the grounds that food is too widely shared to pro-
vide any advantage to the family of the procurer.
It is also possible that hunting success is related to measures of
RS due to a confounding variable. For example, strength might con-
tribute independently to hunting success
Furthermore, and more importantly, demonstrating an effect on
receivers is insufficient to distinguish whether hunting acts as a signal
or a cue.
3.2.2 |What does hunting actually signal?
It has not yet been demonstrated that human hunting reputation is
correlated with a signaled quality that is otherwise cryptic. In humans,
this quality is unknown and proponents of the costly signaling hypoth-
esis of human hunting
generally do not specify what otherwise
cryptic qualities hunting effort may serve to make clear. Sometimes
specific qualities are proposed, although these differ between publica-
tions. Bliege Bird and Smith
suggest that these qualities might be
“skill and cognitive ability”or perhaps “physical vigor.”Elsewhere the
same authors propose “strength, skill, esoteric knowledge, or leader-
“vigor, intelligence, economic productivity, and/or
and “ethological knowledge, visual acuity
These claims remain largely untested. Some recent
work has found a relationship between hunting reputation and upper
although upper body strength may not be otherwise
cryptic as it can be assessed visually.
found that Hadza hunting reputation predicted several hunting
skills including aim, upper body strength, and an ability to recognize
the vocalizations of prey species, albeit with a degree of noise, dis-
agreement and error. If hunting is indeed an honest signal, more work
must be done to show it is correlated with an otherwise cryptic but
adaptively relevant quality. Importantly, if the signaling value of hunt-
ing is ever to be fruitfully investigated, specific, operational, testable
predictions must be provided.
3.2.3 |Cost is not sufficient: An overemphasis on costs
A convincing argument may be made that human hunting is costly
(i.e. energetically sub-optimal), especially when food-redistribution is
considered. Certain authors argue that, among many forager popula-
tions, hunters target resources that may be redistributed at opportu-
nity cost to themselves and their families
(Figure 3). Evidence that
men target more difficult to attain and more widely redistributed
foods comes from numerous populations.
the Mer islanders, there is some evidence that hunting is less costly
for better hunters,
although in this case age is used as an imperfect
proximate measure of hunting skill.
However, others have argued that, due to either reciprocal sharing
or errors in the assessment of resource acquisition patterns,
ing does not universally entail a cost. Wood and Marlowe
FIGURE 3 The carcass of a lesser kudu, recently killed by a Hadza
hunter and then dismembered and brought back to a central place by
the hunter and his campmates. Large game meat may be redistributed
at several stages, including at the site of the kill, upon returning to
camp, and after cooking. Credit to Colin Groves for identification
[Color figure can be viewed at wileyonlinelibrary.com]
argued that Hadza hunting is not costly or sub-optimal because (a) small
game are frequently pursued, (b) a producer's household can expect a
larger proportion of all hunting returns, large game and small, than might
other campmates, and (c) small and large game appear to be similarly
widely shared. Contrary to the predictions of Hawkes et al.
argued, in a situation where game of all sizes are widely shared, large
game may not be a sub-optimal resource. In response, Hawkes et al.
highlighted several potential problems with Wood and Marlowe's
methods, namely that Wood and Marlowe
had defined households too
broadly, had incorrectly classified skinsaschoicecutsofmeat,artificially
inflating the proportion of each carcass kept by a producer's household,
and had used only the weights of meat brought back to camp, rather
than whole carcass weights. In turn Wood and Marlowe
Hawkes et al.'s calculations and demonstrated that men spent a compa-
rable period of time directly pursuing small and large game, spent the
majority of foraging time walking in search of any animal, small or large,
and pursued most small game that they encountered. Neither the debate
nor the proper interpretation of these data have been resolved to the
satisfaction of all parties.
The costliness of hunting acquisition patterns and food-
redistribution is however, largely moot. Strategic costs (handicaps) are
neither necessary nor sufficient for honest signaling.
ples of honest signaling involve little realized cost to the signaller
(Box 2). Realized costs at equilibrium which serve to guarantee the
honesty of the signal distinguish strategic signals
other forms of signaling where costs are paid when deviating from
equilibrium (Box 2). However, the demonstration of realized cost
alone is not sufficient to demonstrate that a trait or behavior acts as a
signal nor, if the trait does act as a signal, to distinguish strategic cost
from efficacy cost. This point has been made repeatedly outside of
the hunter-gatherer literature,
although within hunter-gatherer
studies authors have
to focus on demonstrating
that men's resource acquisition patterns are suboptimal and that men
prioritize foods that go mostly to others rather than their own house-
Critically, although these patterns might be reasonably inter-
preted as evidence against the family provisioning model, such studies
provide no positive support for the notion that hunting acts as a costly
3.2.4 |Signal efficacy revisited: Human hunting is a poor
Signals must be a reliable way of broadcasting to potential signal
recipients. They must be conspicuous and must act as good heuristics.
In the zoological literature this is known as the efficacy of a signal
and in the anthropological literature as broadcast effectiveness.
ponents of the costly signaling hypothesis
argue that the inherent
value of meat in resource-limited environments makes hunting an
especially conspicuous signal of hunting prowess; by targeting widely
redistributed foods, hunters attract large audiences.
This argument is ostensibly compelling and is consistent with the
fact that meat is valuable and, in many groups, shared widely. How-
ever, closer inspection casts doubt on the assumption that hunting
and the targeting of widely redistributed foods is a relatively effective
way of broadcasting information about the hunter's abilities. For an
honest signal of hunting ability to work, a person's perceived hunting
reputation must be reliably correlated with his actual skill at finding
and killing wild animals.
There are several reasons why, among for-
ager groups, this may not always be the case. Firstly, among some
groups such as the Hadza, men generally hunt alone with no
and so campmates seldom observe hunting skills in action.
Furthermore, among the Hadza, men may eat a significant proportion
of the food they acquire alone out of camp, including small (though
not large) game.
Given inter-individual variation in the amount of
small game eaten, this means that there is not a 1:1 correspondence
between their actual success at killing wild animals and the amount of
meat they return with. This obfuscates true hunting skill. In some
instances, such as torch fishing on Ifaluk atoll
hunting is done in the
presence of an audience of onlookers. This does allow individuals to
observe hunting skills in action, though such cases are in the minority.
In other instances such as Meriam turtle hunting,
together cooperatively as a group and hunters may observe one
another, although the skills and contributions of particular individuals
are still obscured to those not participating.
In addition, individual hunting incomes in many environments are
subject to high daily variance. Hadza hunters, for example, procure
large game on between 1% and 3% of days.
The “!Kung, Aché, and
Hiwi, targeting smaller game, make kills 27%, 50%, and 44% of the
and kill large game less often than do the
The consequence of such variability in success is that, to
accurately estimate the true mean hunting success rate of, for exam-
ple, a !Kung hunter with a ± 20% degree of accuracy, ~600 days of
observation are required.
And lower daily success rates necessitate
even more observation days. Put simply, without almost 2 years or
more living in the same or an immediately proximate camp, from for-
aging returns alone, it is difficult to tell whether the hunter providing
you with meat is a good hunter, or simply a bad hunter who got lucky.
Collecting enough observation days is unlikely for most individuals,
especially given that, among many foragers, camp composition regu-
larly changes. From receiver perspective, this renders hunting return
rate an inefficient metric for assessing true hunting skill.
Furthermore, for the hunter, efficacy costs, those costs involved
in producing the signal, but which do not increase the reliability of sig-
nal content (i.e. hunting skill) appear untenably high. If he wants to sig-
nal a specific ability such as aim, for example, why does a Hadza man
spend a mean of 6.3 hr a day, alone, out of camp, where he cannot be
hunting a resource that will, after more than 2 years, pro-
vide some noisy indication of skill with a bow and arrow,
could stay in camp and shoot arrows at a target instead? A similar
argument could be made for strength, eyesight, ecological knowl-
or almost any other specific aspect of hunting ability that a
hunter might want to broadcast. This example may appear facile, but
is exactly how many animal signals operate. Handicapping somatic
traits such as peacocks tails, when fanned out, are instantly readable
to conspecifics, while gazelle stotting displays take less than a minute
to perform. In fact, with the exception of Arabian babblers, whose sta-
tus as honest signallers has been disputed,
most examples of honest
signaling from the zoological literature, independent of species life-
span and almost universally, are conspicuous, short in duration and
take a form and modality
that serves to maximize efficacy. Hunting
may generally not be a similarly efficacious means of transmitting
information about qualities related to hunting prowess.
4|GENEROSITY SIGNALING AND
4.1 |Generosity, stinginess, and reputation: An
alternative to showing off hunting skill
Beyond the fact that hunting should show-off some aspect of “hunt-
it is unclear what specific hidden attribute it might
serve to signal. Although men's hunting acquisition patterns may, after
food redistribution, represent an opportunity cost to the hunter and
the demonstration of such costs does not provide posi-
tive evidence that hunting acts as a signal. Furthermore, for several
reasons, sharing or targeting widely redistributed meat is not a wholly
effective and reliable means of signaling information about ones skill
as a hunter
and does not, as other animal signals do, operate as a
quick and efficacious heuristic for signal recipients in assessing ele-
ments of hunting prowess.
An alternative suggestion is that the redistribution of hunted
meat may play a role in signaling a hunter's pro-sociality,
ment to public interest”
or intention “to cooperate, share gener-
In other words hunting foods which are widely
redistributed might facilitate the maintenance of reputation for gener-
osity and pro-sociality.
Reputation, put simply, is “knowledge of an [individual]‘s typical
behavior based on that [individual]‘s past behavior”.
an unrivaled capacity to remember and assimilate large amounts of
information about numerous other individuals over long periods of
time. The human capacity for sophisticated language
humans, unlike most nonhuman animals, can communicate detailed
knowledge about others to conspecifics (indirect reputation). Individ-
uals may, through acts of cooperation, build reputations among both
the individuals with whom they cooperate and third parties either
through direct observation or indirect communication (e.g., gossip).
Having a positive image positively influences later interactions with
third parties, while having a negative image may do the opposite. This
idea, often called image scoring has been modeled, game theoretically
with some success, and may go some way toward maintaining a sys-
tem of indirect reciprocity.
This framework is still consistent with the idea that hunting might
act as a signal. Image scoring and reputation models are still built
around the assumption that cooperation (e.g., food-sharing) signals
information about an individual's willingness to cooperate to other
interested parties. Furthermore, reputation-based models are not dis-
similar from Hawkes'
proposition that individuals who share more
should make more valuable social partners. Critically, however, the
show off and costly signaling hypotheses in hunter-gatherer studies
have been largely built on the assumption that hunters signal some
aspect of their “hunting prowess.”
The reputation maintenance
model, instead, predicts that individuals signal generosity and willing-
ness to share or garner widely redistributed resources. Furthermore, it
differs in three important assumptions all of which appear more con-
sistent with patterns observed in the literature.
First, the anthropological literature on hunting as a handicap tra-
ditionally predicts that it serves to advertise some hidden quality(s)
related to hunting skill.
Under the reputation maintenance model,
this is not the case and the signal and the signaled quality are one and
the same; by targeting widely redistributed food, for example, hunters
demonstrate only that they are willing to provide food for the group.
In this respect, hunting may act more as an index than as a Zahavian
handicap (although see Boxes 1 and 2 and associated references for a
disambiguation and discussion of this term).
Second, the handicap signaling model of hunting predicts that the
opportunity costs of sharing or targeting widely redistributed
resources serve to guarantee the honesty of the signal.
viduals in better condition, who are better able to afford strategic
costs, should pay higher costs and signal more intensely.
In the con-
text of hunting, this means that better hunters should be better able
to bear the costs of procuring more widely redistributed food items.
By contrast, under the reputation model, sharing is only necessary
insofar as a positive reputation can be maintained and predicts that
hunters should take any opportunity to keep food for themselves so
long as it does not damage their reputation for generosity. In other
words, food sharing is only necessary to “keep up appearances.”The
cost, in this case, comes from the reputational penalties incurred when
individuals are caught keeping food for themselves, or are perceived
not to be contributing. In this way, reputation-based signaling models
only need involve potential costs, and not realized strategic costs
(handicaps). This prediction is consistent with the fact that Hadza men
eat much food, including honey and small game, alone out of camp.
is further consistent with numerous anecdotal accounts of foragers
attempting to hide food and other items undetected.
Third, proponents of the costly signaling hypothesis of human
hunting argue that “hunting is an arena of male competition”.
hunting truly were a form of male-male competition individuals should
be expected to signal in order to outcompete potential rivals. Under a
reputation maintenance/generosity signaling model, however, people
are not in direct competition with other individuals and should,
instead, seek out those reputed to be more generous or to bring back
more food. This is consistent with the fact that, in a series of inter-
views, almost all adult men among the Hadza and Aché reported that
they would rather live in camps with better hunters because they
would get more food.
If hunting is a form of male-male competition,
hunters might be expected to avoid better rivals who acquire more
Under the reputation/generosity signaling model, how-
ever, those with good reputations should be sought out because they
make valuable social partners.
The above arguments are based upon the proposition that having
a positive reputation is beneficial. This proposition may be reversed.
Many of the arguments concerning the evolution and maintenance of
cooperation and food redistribution/sharing state that such systems
are maintained through the punishment of defectors and nonrecipro-
Reputation damage may provide a feasible mechanism for
such punishment. A negative reputation may be harmful, minimizing
later opportunities for cooperation and mutual support. In the words
“once language evolved, the fear of being called stingy
could motivate human sharing, as it does even nowadays.”If this propo-
sition is correct, individuals may be able to punish noncooperators—for
example those who do not target widely redistributed resources, or
who attempt to keep food for themselves—by damaging their reputa-
tions. Importantly, while forms of corporal punishment are costly, and
incur a risk of harm to the punisher, word of mouth attacks on a per-
son's reputation are virtually cost-free. They can be indirect, without
the knowledge of the person being punished and, thus, without the risk
Though this discussion so far has been broadly theoretical, there
are a wealth of empirical accounts from hunter-gatherer groups of
people responding to perceived stinginess with reputational attacks.
For example in a sample of everyday conversation topics among the !
Kung, more than 60% related to food or complaints about people's
lack of generosity.
Furthermore, refusing to share food among the
Batek is met with resentment from other camp members.
tern is familiar to Hadza researchers also and Marlowe
arguments and bickering will often center around food redistribution
and that people share food for fear of being labeled stingy. It is also
notable that many aspects of human psychology—the emotions of
pride, regret, shame, guilt, embarrassment and contrition which appear
in some form universal
—provide proximate mechanisms for the
maintenance of a positive reputation.
4.2 |Empirical evidence
The importance of reputation maintenance is not a new idea.
has already highlighted the impact of language on collective
action problems; and reputation was incorporated into a recent model
of the evolution of human cooperation.
modeled systems of reputation and have shown that analysis in terms
of reputation damage can, theoretically, solve collective action prob-
lems. Reputation scores also appear to foster cooperation when incor-
porated into empirical economic experiments.
signaling/reputation maintenance model would go some way toward
reconciling the separate literatures concerning image scoring and
Furthermore, despite a wealth of theoretical work, with only few
little empirical research has been done to assess the
benefits of having a positive reputation (for generosity) and the disad-
vantages of a negative reputation (for stinginess) in hunter-gatherer
groups. This is, in part, because reputation is multifaceted and difficult
to quantify. Furthermore, the advantages and disadvantages of having
a positive and negative reputation may be only intermittently
observed, and it may be difficult to establish causality. There are some
hints, however. The oft reported fact that better hunters have higher
is consistent with the idea that positive reputations are benefi-
cial, as are reports that better hunters make more desirable camp-
In one of the few studies to examine reputation directly, Lyle
showed that those with reputations for generosity
among a Peruvian farming/herding community had lower household
morbidity and received more help with subsistence. In another, Bliege
Bird and Power
showed that, among the Martu, pro-social individ-
uals have a larger number of cooperation partners. It is further notable
that many Hadza view nonreciprocators negatively.
recent literature on social capital, relational wealth and social network
may provide some good evidence for the benefits
of a positive reputation for pro-sociality.
Overall, more research should be done on the selective conse-
quences of positive and negative reputations for generosity. This could
take the form of interviews or correlational studies or follow the
methods set out by Lyle and Smith,
or could look directly at network
position and relational wealth (see Reference 106). For the time being,
however, reputation maintenance is a compelling solution to the prob-
lem of food redistribution and one that, although it still fits into a costly
signaling framework sensu lato (Box 1) is arguably more consistent with
the empirical evidence than explanations invoking Zahavi's handicap
principle specifically. The importance of managing one's reputation
is something that readers will almost certainly be familiar with. It
has previously been sidelined in the academic discourse on food
sharing/redistribution in hunter gatherer groups and, in Smith's
words “evolutionists interested in Homo sapiens have much to explore
at the intersection of cooperation and communication.”
The extent of human cooperation is, as many have noted, idiosyn-
cratic and puzzling.
Hunting and food-sharing among hunter-
gatherer groups provides a microcosm of this phenomenon. Food-
sharing and redistribution, the sexual division of labor, and the fact
that men appear often to target potentially energetically sub-optimal
resources are complex phenomena and difficult to account for within
a self-interested framework. For this reason, to some evolutionary
anthropologists, the idea that hunting might signal some cryptic
aspect of hunting skill is greatly appealing. It addresses the puzzle of
food redistribution and the sexual division of labor parsimoniously.
Furthermore, it is consistent with the fact that more well-reputed
hunters in numerous groups appear to have greater RS.
ally, it draws directly from the handicap principle which, along with
other forms of costly signaling,
has been of utility in explaining the
existence of superficially wasteful or costly traits and behaviors
observed elsewhere in nature.
However, the theoretical appeal and simplicity of this explanation
may belie its faults. It is yet possible that hunting does act as a
handicapping signal in the Zahavian sense, although more work must
be done to show what otherwise cryptic hunting-skill related trait(/s)
hunting serves to make clear. Furthermore, it is important to establish
why, if it is a signal of hunting prowess, human hunting takes a consid-
erably greater investment of time to interpret by the signal recipient
relative to most other proposed examples of signaling from nonhuman
animals. Finally, because realized cost alone is not a necessary condi-
tion of honest signaling (Box 2), discussions of the costly signaling
hypothesis should not take evidence that hunting is costly and ener-
getically sub-optimal (see References 27,32) as positive evidence that
hunting acts as a strategic costly signal.
An alternative hypothesis, also involving a signaling mechanism,
but more consistent with the forager literature, is that hunting signals
generosity or pro-sociality and acts as a means of reputation mainte-
nance. Instead of paying strategic costs to signal cryptic, heritable
aspects of hunting ability, men's acquisition patterns might instead
signal altruism, prosociality and a willingness to cooperate. Indeed,
although the focus of much traditional costly signaling literature has
been hunting prowess, these articles have also often mentioned the
potential of hunting to signal generosity
and garner cooperation
an idea brought to the fore in recent work by Bliege Bird
In models of reputation, food-sharing and redistribution still signal
generosity. In this respect, reputation maintenance still fits into a
broader costly signaling framework (sensu Reference 69). However, by
moving away from Zahavi's model and the associated idea that
hunters pay realized strategic costs to signal cryptic aspects of hunting
prowess, and by focussing on the roles that language and reputation
play in the maintenance of human cooperation, we may find a more
fruitful alternative paradigm for anthropological research.
Thanks to Frank Marlowe and Robert Attenborough for the advice
and support they have given in formulating these ideas. Thanks also
to Jo Setchell, Jamie Tehrani, Sarah Elton, and Trevor Hawkes for their
comments and advice. Finally, many thanks to James Higham and
three other reviewers for their feedback and suggestions.
Duncan N. E. Stibbard-Hawkes https://orcid.org/0000-0002-6719-
 Kelly RL. 2013. The lifeways of hunter-gatherers: The foraging spec-
trum, 3rd ed. Cambridge: Cambridge University Press.
 Thieme H. 1997. Lower Palaeolithic hunting spears from Germany.
 Domínguez-Rodrigo M, Pickering TR, Semaw S, Rogers MJ. 2005.
Cutmarked bones from Pliocene archaeological sites at Gona, Afar,
Ethiopia: Implications for the function of the world's oldest stone
tools. J Hum Evol 48(2):109–121.
 McPherron SP, Alemseged Z, Marean CW, et al. 2010. Evidence for
stone-tool-assisted consumption of animal tissues before 3.39 mil-
lion years ago at Dikika, Ethiopia. Nature 466(7308):857–860.
 Wrangham RW. 1987. The significance of African apes for recon-
structing human social evolution. In: Kinzey WG, editor. The evolu-
tion of human behavior: Primate models, 1st ed. New York: State
University of New York Press. p 51–71.
 Aiello LC, Wheeler P. 1995. The expensive-tissue hypothesis: The
brain and the digestive system in human and primate evolution. Curr
 Kaplan H, Gurven M, Winking J. 2007. An evolutionary theory of
human life span: Embodied capital and the human adaptive complex.
In: Bengtson VL, Gans D, Putney NM, Silverstein M, editors. Hand-
book of theories of aging, 2nd ed. New York: Springer. p 39–61.
 Berbesque JC, Wood BM, Crittenden AN, Mabulla A, Marlowe FW.
2016. Eat first, share later: Hadza hunter-gatherer men consume
more while foraging than in central places. Evol Hum Behav 37
 Marlowe FW. 2001. Male contribution to diet and female reproduc-
tive success among foragers. Curr Anthropol 42(5):755–760.
 Wood BM, Marlowe FW. 2014. Toward a reality-based understand-
ing of Hadza Men's work. Hum Nat 25(4):620–630.
 Kaplan H, Gurven M. 2004. The natural history of human food sharing
and cooperation: A review and a new multi-individual approach to the
negotiation of norms. In: Gintis H, Bowles S, EF RB, editors. Moral
sentiments and material interests: The foundations of cooperation in
economic life Cambridge, Massachusetts: MIT Press pp. 75–114.
 Hawkes K. 1991. Showing off: Tests of an hypothesis about Men's
foraging goals. Ethol Sociobiol 12(1):29–54.
 Hawkes K, Bird RB. 2002. Showing off, handicap signaling, and the
evolution of Men's work. Evol Anthropol 11:58–67.
 Bliege Bird R. 2007. Fishing and the sexual division of labor among
the Meriam. Am Anthropol 109(3):442–451.
 Marlowe FW. 2007. Hunting and gathering: The human sexual divi-
sion of foraging labor. Cross-Cult Res 41(2):170–195.
 Bliege Bird R, Bird DW. 2008. Why women hunt: Risk and contem-
porary foraging in a Western Desert aboriginal community. Curr
 Codding BF, Bird RB, Bird DW. 2011. Provisioning offspring and
others: Risk-energy trade-offs and gender differences in hunter-
gatherer foraging strategies. Proc R Soc B Biol Sci 278(1717):
 Gurven M, Hill K. 2009. Why do men hunt? Curr Anthropol 50(1):
 Gurven M. 2004. To give and to give not: The behavioral ecology of
human food transfers. Behav Brain Sci 27:543–583.
 Kaplan H, Hill K. 1985. Hunting ability and reproductive success
among male ache foragers: Preliminary results. Curr Anthropol 26
 Cashdan EA. 1985. Coping with risk: Reciprocity among the
Basarwa of northern Botswana. Man 20(3):454–474.
 Wiessner P. 2002. Hunting, healing, and hxaro exchange: A long-
term perspective on !Kung (Ju/‘hoansi) large-game hunting. Evol
Hum Behav 23(6):407–436.
 Bird DW, Bliege Bird R. 2002. Risk and reciprocity in Meriam food
sharing. Evol Hum Behav 23(4):297–321.
 Marlowe FW. 2010. The Hadza: Hunter-gatherers of Tanzania, Los
Angeles: University of California Press.
 Nolin DA. 2012. Food-sharing networks in Lamalera, Indonesia: Sta-
tus, sharing, and signaling. Evol Hum Behav 33(4):334–345.
 Blurton Jones NG. 2016. Demography and evolutionary ecology of
Hadza hunter-gatherers, Cambridge: Cambridge University Press.
 Hawkes K, O'Connell JF, Blurton Jones NG. 2014. More lessons
from the Hadza about Men's work. Hum Nat 25(4):596–619.
 Washburn S, Lancaster C. 1968. The evolution of hunting. In:
Lee RB, DeVore I, editors. Man the hunter, 2nd ed. Chicago: Aldine.
 Bird R. 1999. Cooperation and conflict: The behavioral ecology of
the sexual division of labor. Evol Anthropol 8(2):65–75.
 Winterhalder B. 2001. The behavioural ecology of hunter-gatherers.
In: Panter-Brick C, Layton RH, Rowley-Conwy P, editors. Hunter-
gatherers: An interdisciplinary perspective, Cambridge: Cambridge
University Press. p 12–38.
 Layton R, O'Hara S. Human social evolution: A comparison of
hunter-gatherer and chimpanzee social organization. Proc British
 Hawkes K, O'Connell JF, Coxworth JE. 2010. Family provisioning is
not the only reason men hunt. Curr Anthropol 51(2):259–264.
 Gintis H, Smith E, Bowles S. 2001. Costly signaling and cooperation.
J Theor Biol 213(2):103–119.
 Fehr E, Gächter S. 2002. Altruistic punishment in humans. Nature
 Blurton Jones NG. 1984. A selfish origin for human food sharing:
Tolerated theft. Ethol Sociobiol 5(1):1–3.
 Winterhalder B. 1996. A marginal model of tolerated theft. Ethol
 Hamilton WD. 1964. The Genetical evolution of social behaviour.
J Theor Biol 7(1):1–16.
 Wood BM, Marlowe FW. 2013. Household and kin provisioning by
hadza men. Hum Nat 24(3):280–317.
 Hill KR, Walker RS, Bozicevi
c M, et al. 2011. Co-residence patterns
in hunter-gatherer societies show unique human social structure.
Science (New York, NY) 331(6022):1286–1289.
 Dyble M, Salali GD, Chaudhary N, et al. 2015. Sex equality can
explain the unique social structure of hunter-gatherer bands. Sci-
 Hawkes K, O'Connell JF, Blurton Jones NG. Hunting income pat-
terns among the Hadza: Big game, common goods, foraging goals
and the evolution of the human diet. Philos Royal Soc B: Biol Sci
1991;334(1270):243–250; discussion 250–251.
 Hawkes K, O'Connell JF, Blurton Jones NG. 2001. Hunting and
nuclear families: Some lessons from the Hadza about Men's work.
Curr Anthropol 42(5):681–709.
 Hawkes K, O'Connell JF, Blurton Jones NG. 2001. Hadza meat shar-
ing. Evol Hum Behav 22:113–142.
 Hawkes K. Hunting and th e evolution of egalitarian societies:
Lessons from the Hadza. In: Diehl M, editor. Hierarchies in action,
1 ed. No. 27, Illinois: Center for Archaeological Investigations;
 Gurven M, Jaeggi AV. 2015. Food sharing. In: Buchmann RAS, C M,
editors. Emerging trends in the social and behavioral sciences: An
interdisciplinary, searchable, and linkable resource, 1st ed. Hoboken,
New Jersey: Wiley. p 1–12.
 Kaplan H, Hill K, Cadeliña R. 1985. Food sharing among ache foragers:
Tests of explanatory hypothesis. Curr Anthropol 26(2):223–233.
 Hawkes K. 1992. Sharing and collective action. In: Smith EA,
Winterhalder B, editors. Evolutionary ecology and human behavior,
1st ed. London: Aldine Transaction. p 269–300.
 Hawkes K, Altman J, Beckerman S, et al. 1993. Why gatherers work
an ancient version of the problem of public goods [and comments
and reply]. Curr Anthropol 34:341–361.
 Hawkes K. 2001. Is meat the Hunter's property? Big game, owner-
ship, and explanations. In: Stanford CB, Bunn HT, editors. Meat-
eating and human evolution, 1st ed. Oxford: Oxford University
Press. p 219–236.
 Hawkes K. 1996. Foraging differences between men and women:
Behavioral ecology of the sexual division of labour. In: Shennan S,
Steele J, editors. The archaeology of human ancestry: Power, sex
and tradition, 1st ed. London: Routledge. p 283–298.
 Zahavi A. 1975. Mate selection—A selection for a handicap. J Theor
 Gurven M, von Rueden C. 2006. Hunting, social status and biologi-
cal fitness. Soc Biol 53(1–2):81–99.
 Bliege Bird R, Smith EA. 2005. Signaling theory, strategic interaction,
and symbolic capital. Curr Anthropol 46(2):221–248.
 Grafen A. 1990. Biological signals as handicaps. J Theor Biol 144(4):
 Darwin C. 1871. The descent of man, and selection in relation to
sex, 1st ed. London: John Murray.
 Darwin C. 1859. On the origin of species, 1st ed. London: John
 Fisher RA. 1915. The evolution of sexual preference. Eugen Rev 7
 Spence M. Job market signaling. Q J Econ 1973;87(3):355.
 Dawkins R. 1976. The selfish gene, 1st ed. Oxford: Oxford Univer-
 Maynard Smith J. 1976. Sexual selection and the handicap principle.
J Theor Biol 57(1):239–242.
 Dawkins R. 2006. The selfish gene: 30th anniversary edition, 3rd
ed. Oxford: Oxford University Press.
 Maynard Smith J, Harper D. Animal Signals. 1 ed. Oxford: Oxford
University Press; 2003.
 Grose J. 2011. Modelling and the fall and rise of the handicap princi-
ple. Biol Philos 26(5):677–696.
 Lachmann M, Szamado S, Bergstrom CT. Cost and conflict in
animal signals and human language. Proc Natl Acad Sci 2001;98
 Getty T. 2006. Sexually selected signals are not similar to sports
handicaps. Trends Ecol Evol 21(2):83–88.
 Zahavi A, Zahavi A. 1997. The handicap principle: A missing piece of
Darwin's puzzle, 1st ed. Oxford: Oxford University Press.
 Biernaskie JM, Grafen A, Perry JC. The evolution of index signals to
avoid the cost of dishonesty. Proc R Soc B Biol Sci 2014;281(1790):
 Számadó S. 2011. The cost of honesty and the fallacy of the handi-
cap principle. Anim Behav 81(1):3–10.
 Higham JP. 2014. How does honest costly signaling work? Behav
 Rendall D, Owren MJ, Ryan MJ. 2009. What do animal signals
mean? Anim Behav 78(2):233–240.
 Pryke SR, Andersson S. 2002. A generalized female bias for long tails
in a short-tailed widowbird. Proc R Soc B Biol Sci 269(1505):
 Andersson S. 1992. Female preference for long tails in lekking Jack-
son's widowbirds: Experimental evidence. Anim Behav 43(3):
 Smith EA. 2004. Why do good hunters have higher reproductive
success? Hum Nat 15(4):343–364.
 Gurven M, Kaplan H, Gutierrez M. 2006. How long does it take to
become a proficient hunter? Implications for the evolution of
extended development and long life span. J Hum Evol 51(5):
 Power EA. 2017. Discerning devotion: Testing the signaling theory
of religion. Evol Hum Behav 38(1):82–91.
 Møller AP, de Lope F. Differential costs of a secondary sexual char-
acter: An experimental test of the handicap principle. Evolution
 FitzGibbon CD, Fanshawe JH. 1988. Stotting in Thomson's
gazelles: An honest signal of condition. Behav Ecol Sociobiol 23(2):
 Bergstrom CT, Szamado S, Lachmann M. Separating equilibria in
continuous signalling games. Philos Trans Royal Soc B: Biol
 Maynard Smith J, Harper D. 1995. Animal signals: Models and ter-
minology. J Theor Biol 177(3):305–311.
 Higham JP, Pfefferle D, Heistermann M, Maestripieri D, Stevens M.
2013. Signaling in multiple modalities in male rhesus macaques: Sex
skin coloration and barks in relation to androgen levels, social status,
and mating behavior. Behav Ecol Sociobiol 67(9):1457–1469.
 Wood BM. 2006. Prestige or provisioning? A test of foraging goals
among the Hadza. Curr Anthropol 47(2):383–387.
 Kraft TS, Venkataraman VV, Tacey I. 2018. Foraging performance,
Prosociality, and kin presence do not predict lifetime reproductive
success in Batek. Hum Nat 1–27.
 Apicella CL. 2014. Upper-body strength predicts hunting reputation
and reproductive success in Hadza hunter-gatherers. Evol Hum
 Stibbard-Hawkes DNE, Attenborough RD, Marlowe FW. 2018. A
noisy signal: To what extent are Hadza hunting reputations predic-
tive of actual hunting skills? Evol Hum Behav 39(6):639–651.
 Smith EA, Bliege Bird R, Bird DW. 2003. The benefits of costly sig-
naling: Meriam turtle hunters. Behav Ecol 14(1):116–126.
 Smith EA, Bliege Bird R. 2005. Costly signaling and cooperative
behavior. In: Gintis H, Bowles S, Boyd R, Fehr E, editors. Moral sen-
timents and material interests: On the foundations of cooperation in
economic life, Cambridge: MIT Press. p 115–148.
 Sell A, Cosmides L, Tooby J, Sznycer D, Von Rueden C, Gurven M.
2009. Human adaptations for the visual assessment of strength and
fighting ability from the body and face. Proc R Soc B Biol Sci 276
 Bliege Bird R, Smith E, Bird DW. 2001. The hunting handicap: Costly
signaling in human foraging strategies. Behav Ecol Sociobiol 50
 Fraser B. 2012. Costly signalling theories: Beyond the handicap prin-
ciple. Biol Philos 27(2):263–278.
 Hawkes K, O'Connell J, Blurton Jones N. 2018. Hunter-gatherer
studies and human evolution: A very selective review. Am J Phys
 Sosis R. 2000. Costly signaling and torch fishing on Ifaluk atoll. Evol
Hum Behav 21(4):223–244.
 Hill K, Hurtado AM. 2009. Cooperative breeding in south American
hunter-gatherers. Proc R Soc B Biol Sci 276(1674):3863–3870.
 Wright J, Berg E, De Kort SR, Khazin V, Maklakov AA. 2001. Coop-
erative sentinel behaviour in the Arabian babbler. Anim Behav 62(5):
 Bliege Bird R, Power EA. 2015. Prosocial signaling and cooperation
among Martu hunters. Evol Hum Behav 36(5):389–397.
 Bird RB, Scelza B, Bird DW, Smith EA. 2012. The hierarchy of virtue:
Mutualism, altruism and signaling in Martu women's cooperative
hunting. Evol Hum Behav 33(1):64–78.
 Russell YI, Call J, Dunbar RIM. An ‘indirect reputation’experiment in
four great ape species. In: Congress of the European Federation for
Primatology. Göttingen, Germany: European Federation for Prima-
 Smith EA. 2010. Communication and collective action: Language and
the evolution of human cooperation. Evol Hum Behav 31(4):231–245.
 Nowak MA, Sigmund K. 2005. Evolution of indirect reciprocity.
 Peterson N. 1993. Demand sharing: Reciprocity and the pressure
for generosity among foragers. Am Anthropol 95(4):860–874.
 Endicott K. 1988. Property, power, and conflict among the Batek of
Malaysia.In: Ingold T, Riches D, Woodburn J, editors.Hunters and gath-
erers2: Property, Power,and ideology, 1sted. Oxford: Berg. p 110–127.
 Ekman P. 1992. Are there basic emotions? Psychol Rev 99(3):
 Tomasello M, Melis AP, Tennie C, Wyman E, Herrmann E. 2012.
Two key steps in the evolution of human cooperation. Curr Anthro-
 dos Santos M, Rankin DJ, Wedekind C. The evolution of punish-
ment through reputation. Proc R Soc B Biol Sci 2011;278(1704):
 Lyle HF, Smith EA. 2014. The reputational and social network bene-
fits of prosociality in an Andean community. Proc Natl Acad Sci U S
 Apicella CL, Marlowe FW, Fowler JH, Christakis NA, 2012. Social
networks and cooperation in hunter-gatherers. Nature, 481(7382),
 Chaudhary N, Salali GD, Thompson J, Rey A, Gerbault P,
Stevenson EGJ, Dyble M, E. Page A, Smith D, Mace R, Vinicius L,
Migliano AB Competition for cooperation: Variability, benefits and
heritability of relational wealth in hunter-gatherers. Sci Rep 2016;6
 Bshary R, Raihani NJ. 2017. Helping in humans and other animals: A
fruitful interdisciplinary dialogue. Proc R Soc B Biol Sci 284(1863):
 Hamilton WD, Zuk M. 1982. Heritable true fitness and bright birds:
A role for parasites? Science 218(4570):384–387.
 Davies NB, Halliday TR. 1978. Deep croaks and fighting assessment
in toads Bufo bufo. Nature 274:683–685.
 Searcy WA, Nowicki S. 2005. Krebs JR, Clutton-Brock T, editors. The
evolution of animal communication: Reliability and deception in signal-
ing systems, 1st ed. Princeton, New Jersy: Princeton University Press.
 Tibbetts EA, Izzo A. 2010. Social punishment of dishonest signalers
caused by mismatch between signal and behavior. Curr Biol 20(18):
DUNCAN STIBBARD-HAWKES received his BA and PhD in biological
anthropology from the University of Cambridge. He conducted his
PhD research with the Hadza in Northern Tanzania, where he exam-
ined hunting reputation and the costly signalling hypothesis. He cur-
rently lectures in evolutionary anthropology at Durham University.
How to cite this article: Stibbard-Hawkes DNE. Costly signal-
ing and the handicap principle in hunter-gatherer research: A
critical review. Evolutionary Anthropology. 2019;1–14. https://