Psychedelics, Sociality, and Human Evolution

Abstract

Our hominin ancestors inevitably encountered and likely ingested psychedelic mushrooms throughout their evolutionary history. This assertion is supported by current understanding of: early hominins’ paleodiet and paleoecology; primate phylogeny of mycophagical and self-medicative behaviors; and the biogeography of psilocybin-containing fungi. These lines of evidence indicate mushrooms (including bioactive species) have been a relevant resource since the Pliocene, when hominins intensified exploitation of forest floor foods. Psilocybin and similar psychedelics that primarily target the serotonin 2A receptor subtype stimulate an active coping strategy response that may provide an enhanced capacity for adaptive changes through a flexible and associative mode of cognition. Such psychedelics also alter emotional processing, self-regulation, and social behavior, often having enduring effects on individual and group well-being and sociality. A homeostatic and drug instrumentalization perspective suggests that incidental inclusion of psychedelics in the diet of hominins, and their eventual addition to rituals and institutions of early humans could have conferred selective advantages. Hominin evolution occurred in an ever-changing, and at times quickly changing, environmental landscape and entailed advancement into a socio-cognitive niche, i.e., the development of a socially interdependent lifeway based on reasoning, cooperative communication, and social learning. In this context, psychedelics’ effects in enhancing sociality, imagination, eloquence, and suggestibility may have increased adaptability and fitness. We present interdisciplinary evidence for a model of psychedelic instrumentalization focused on four interrelated instrumentalization goals: management of psychological distress and treatment of health problems; enhanced social interaction and interpersonal relations; facilitation of collective ritual and religious activities; and enhanced group decision-making. The socio-cognitive niche was simultaneously a selection pressure and an adaptive response, and was partially constructed by hominins through their activities and their choices. Therefore, the evolutionary scenario put forward suggests that integration of psilocybin into ancient diet, communal practice, and proto-religious activity may have enhanced hominin response to the socio-cognitive niche, while also aiding in its creation. In particular, the interpersonal and prosocial effects of psilocybin may have mediated the expansion of social bonding mechanisms such as laughter, music, storytelling, and religion, imposing a systematic bias on the selective environment that favored selection for prosociality in our lineage.

Full text

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 1
HYPOTHESIS AND THEORY
published: 29 September 2021
doi: 10.3389/fpsyg.2021.729425
Edited by:
Antonio Benítez-Burraco,
Seville University, Spain
Reviewed by:
Kyle Summers,
East Carolina University, United States
Bernard Crespi,
Simon Fraser University, Canada
Danilo De Gregorio,
Vita-Salute San Raffaele University,
Italy
*Correspondence:
José Manuel Rodríguez Arce
jose.rodriguezarce@ucr.ac.cr
Specialty section:
This article was submitted to
Personality and Social Psychology,
a section of the journal
Frontiers in Psychology
Received: 23 June 2021
Accepted: 06 September 2021
Published: 29 September 2021
Citation:
Rodríguez Arce JM and
Winkelman MJ (2021) Psychedelics,
Sociality, and Human Evolution.
Front. Psychol. 12:729425.
doi: 10.3389/fpsyg.2021.729425
Psychedelics, Sociality, and Human
Evolution
José Manuel Rodríguez Arce1*and Michael James Winkelman2
1Evolutionary Anthropologist, Independent Researcher, San José, Costa Rica, 2School of Human Evolution and Social
Change, Arizona State University, Tempe, AZ, United States
Our hominin ancestors inevitably encountered and likely ingested psychedelic
mushrooms throughout their evolutionary history. This assertion is supported by current
understanding of: early hominins’ paleodiet and paleoecology; primate phylogeny of
mycophagical and self-medicative behaviors; and the biogeography of psilocybin-
containing fungi. These lines of evidence indicate mushrooms (including bioactive
species) have been a relevant resource since the Pliocene, when hominins intensified
exploitation of forest floor foods. Psilocybin and similar psychedelics that primarily target
the serotonin 2A receptor subtype stimulate an active coping strategy response that may
provide an enhanced capacity for adaptive changes through a flexible and associative
mode of cognition. Such psychedelics also alter emotional processing, self-regulation,
and social behavior, often having enduring effects on individual and group well-
being and sociality. A homeostatic and drug instrumentalization perspective suggests
that incidental inclusion of psychedelics in the diet of hominins, and their eventual
addition to rituals and institutions of early humans could have conferred selective
advantages. Hominin evolution occurred in an ever-changing, and at times quickly
changing, environmental landscape and entailed advancement into a socio-cognitive
niche, i.e., the development of a socially interdependent lifeway based on reasoning,
cooperative communication, and social learning. In this context, psychedelics’ effects
in enhancing sociality, imagination, eloquence, and suggestibility may have increased
adaptability and fitness. We present interdisciplinary evidence for a model of psychedelic
instrumentalization focused on four interrelated instrumentalization goals: management
of psychological distress and treatment of health problems; enhanced social interaction
and interpersonal relations; facilitation of collective ritual and religious activities; and
enhanced group decision-making. The socio-cognitive niche was simultaneously a
selection pressure and an adaptive response, and was partially constructed by hominins
through their activities and their choices. Therefore, the evolutionary scenario put
forward suggests that integration of psilocybin into ancient diet, communal practice,
and proto-religious activity may have enhanced hominin response to the socio-cognitive
niche, while also aiding in its creation. In particular, the interpersonal and prosocial
effects of psilocybin may have mediated the expansion of social bonding mechanisms
such as laughter, music, storytelling, and religion, imposing a systematic bias on the
selective environment that favored selection for prosociality in our lineage.
Keywords: drug instrumentalization, evolution of religion, hominin evolution, niche-construction theory, sociality,
socio-cognitive niche, psilocybin, psychedelics
Frontiers in Psychology | www.frontiersin.org 1September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 2
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
INTRODUCTION
Early hominins were omnivores that relied substantially on forest
floor foods, including mushrooms (Sayers and Lovejoy, 2014).
The presence of mycophagy and self-medication among both
primates (Huffman, 1997;Hanson et al., 2003) and Paleolithic
humans (Hardy et al., 2013;O’Regan et al., 2016) suggests
hominins also incorporated fungi with bioactive properties in
their diet. It is likely that psychedelic mushrooms from the
genus Psilocybe were ingested by our ancestors since the Pliocene
(beginning 5.3 million years ago [mya]), when semi-arboreal
hominins intensified foraging activity on the ground (see White
et al., 2009). Exposures to psychedelic fungi by australopithecines
and early Homo during the Pleistocene (beginning 2.5 mya)
are implied by their presence in African grasslands (Guzmán
et al., 2014), especially growing on dung of ungulates [an
important target of hominin scavenging and hunting for millions
of years (Domínguez-Rodrigo and Pickering, 2003)]. Moreover,
psilocybin-containing mushrooms are found on all continents
(except Antarctica) and across most ecological zones (Guzmán
et al., 1998;Guzmán, 2005;Froese et al., 2016), and thrive
on landscapes affected by anthropic activities [e.g., woodland
clearings and grazing pastures (Stamets, 1996)], indicating their
widespread availability as Homo spread across Africa, into
Eurasia, and eventually across the globe (see Antón et al., 2014)1.
Typical psychedelics such as psilocybin and lysergic acid
diethylamide (LSD) modify fundamental brain processes that
normally serve to constrain neural systems central to perception,
emotion, cognition, and sense of self (Swanson, 2018). It is
well established that such effects are generated primarily by
the interaction of these substances with the serotonin (5-
hydroxytryptamine; 5-HT) system, binding the 5-HT2A receptor
as partial agonists (Nichols, 2016). Psychedelic stimulation of 5-
HT2A receptors increases excitability of neocortical pyramidal
neurons, augmenting extracellular glutamate release in the
prefrontal cortex, and thereby disrupting cortical rhythmicity
and large-scale brain networks (Carhart-Harris et al., 2014;
Varley et al., 2020;Vollenweider and Preller, 2020). This
alteration of distributed neural processes manifests as increased
synaptic plasticity and entropy, as well as reduced integrity of
discrete brain networks (e.g., functional disintegration of the
default-mode network [DMN]) and reduced segregation between
networks (e.g., increased functional connectivity between the
DMN and dorsal attention network) (De Gregorio et al.,
2018;Preller et al., 2019, 2020;Madsen et al., 2021). Such
changes in brain activity and connectivity lead to a flexible,
functionally more connected brain during the psychedelic state
(Petri et al., 2014;Tagliazucchi et al., 2016;Mason et al., 2020).
Further important mechanisms of action of psychedelics involve
reduced thalamic filtering of interoceptive and exteroceptive
1We focus on psilocybin mushrooms as likely candidates for early psychedelic
consumption in our lineage for the reasons enumerated here and because
they require no preparation whatsoever, being bioactive in their natural state.
Psychedelic plants in general were also ubiquitous and, in some instances, readily
available (though certain plants required further processing to extract psychoactive
secondary compounds) (Rätsch, 2005;Wink and van Wyk, 2008;Pennacchio et al.,
2010;Alrashedy and Molina, 2016).
information, which sustains an increased information flow to
particular areas of the cortex (Vollenweider and Preller, 2020);
and sensory bottom-up overflow and relaxed high-level priors
(e.g., models related to self or social identity) as formulated by
the relaxed beliefs under psychedelics (REBUS) model (Carhart-
Harris and Friston, 2019; for further contextualization see
Noorani and Alderson-Day, 2020).
The present paper suggests that these and other
psychopharmacological properties of psilocybin could have
had direct effects on the adaptation of early humans to their
environment by enhancing their ability to live in highly social
cooperative communities and participate in collaborative
activities with shared goals and intentions. This human niche
expanded the core of hominin sociality through collective
intentionality, hyper cooperation, cultural transmission and
innovation, teaching, and more recently, language (Boyd et al.,
2011;Sterelny, 2012;Gamble et al., 2014;Tomasello, 2014).
The emergence of these distinctively human capabilities occurs
across our evolutionary history and involved a pattern of
socio-cognitive niche construction predicated on a cumulative
and ratcheting culture alongside substantive neurological and
behavioral plasticity (Iriki and Taoka, 2012;Whiten and Erdal,
2012;Fuentes, 2015). In this context, psilocybin may have
been harnessed to increase adaptability and fitness through
its capacity to modulate the 5-HT2A receptor mediated active
coping strategy (Carhart-Harris and Nutt, 2017), which provides
elevated cortical plasticity, enhanced rate of associative learning,
and elevated capacity to mediate psychological transformation
(Brouwer and Carhart-Harris, 2021).
Our model emphasizes effects of incidental ingestion
of psilocybin-containing mushrooms as an environmental
factor affecting hominin populations across millions of
years of evolution. Eventually, psychedelic consumption
was institutionalized in many pre-modern human societies in
ritual activities focused on healing, divination (i.e., for obtaining
otherwise inaccessible information), and socialization (e.g., in
initiations) (Dobkin de Ríos, 1984;Furst, 1990;Schultes et al.,
2001;Rätsch, 2005;Quirce et al., 2010;Leptourgos et al., 2020).
In many instances, only male shamans ingested psychedelics
(Harner, 1973). But in some cases they were also consumed by
the general population (e.g., among the Huichol of Mexico, the
híkuri cactus, Lophophora williamsii, is used by men, women,
and children: Myerhoff, 1974). Hunters and gatherers likely
learned about hallucinogenic plants as part of their detailed
environmental knowledge (see e.g., Veile, 2018), and smaller
scale societies placed high cultural value on the personal
revelations produced (Boyer, 2019), which is attested to in the
recurring mythological roles ascribed to the these mind-altering
materials (Guerra-Doce, 2014, 2015).
Given the robust alterations of perception and consciousness
produced by psychedelics and their medicinal and religious
importance in some traditional cultures, it has been hypothesized
that their ingestion influenced human evolution. McKenna
(1992) proposed that psilocybin’s effects stimulating visual
acuity, sexual activity, and ecstatic/visionary experiences
influenced hominins’ foraging, sensitivity to community, as
well as religious and spiritual concerns. He also argued the
Frontiers in Psychology | www.frontiersin.org 2September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 3
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
presence of psychedelics in the early human diet drove the rapid
reorganization of the brain’s information-processing capacities
by catalyzing the emergence of self-reflective consciousness
and language. These hypotheses about human origins have
received little attention and thus still need to be examined
further. Moreover, they require additional development so that
they can be empirically tested (e.g., using cross-cultural research
methods and experimental approaches). The aim of this paper is
to contribute to this task by formulating an evolutionary model
of the adaptive utilization of psychedelics that properly integrates
current anthropological and neuropsychopharmacological
knowledge on these substances with the human evolutionary
behavioral sciences.
We recognize that a simplistic version of McKenna’s account
of human evolution implying that psilocybin use by itself
led inevitably to the emergence of the unique cognitive,
communicative, and cooperative patterns characteristic of
modern human populations is most certainly false. Hominin
entry into the socio-cognitive niche cannot be explained in
terms of a single causal factor, a critical adaptive breakthrough
(e.g., bipedality, tool-use, cooking, or even psychedelic use),
but instead through positive feedback loops among various
aspects of hominin life, an adaptive complex involving novel or
greatly exaggerated features of our lineage (Sterelny, 2012). From
this multifactorial and coevolutionary viewpoint, we propose
psychedelics acted as an enabling factor in human adaptation
and evolution. This means psychedelic use may have established
positive feedback loops with core features of the evolving
hominin lifeway, in part generating the coevolving dynamic that
came to structure human evolution. This proposal is based on two
premises:
(a) Psychedelics are serotonin analogs that preferentially
activate the 5-HT2A receptor subtype (Nichols, 2016),
and thereby have effective medicinal applications in
the treatment of stress-related conditions (Vollenweider
and Preller, 2020) and significantly modulate aspects of
creativity (Girn et al., 2020) and sociality (Preller and
Vollenweider, 2019) that could have enhanced adaptability
and fitness, especially in a knowledge-using, socially
interdependent lifeway; and
(b) Psychedelic use can amplify symbolic behavior and a
predisposition for collective rituals and synchronicity (e.g.,
by stimulating deployment of rhythmic, hermeneutical,
and rhetorical activity to endure, make sense of, and
communicate ecstatic and visionary experiences; Doyle,
2011) that could have transformed the social environment,
and thus local selection pressures, through cultural
niche construction.
While we are definitely not proposing that psychedelics
are the “missing link” in hominin evolution, we do propose
that the dietary incorporation of psilocybin would have
enhanced the survival and reproductive prospects of our
ancestors through its incidental effects on adaptive stress-coping
and enhancement of socio-cognitive dynamics. Moreover, the
integration of psilocybin into ancient diet, communal practice,
and proto-religious activity could have sustained feedback loops
in which increases in social cognition and symbolic behavior
engendered by psychedelic use selected for yet further increases
in such capacities by increasing the richness and complexity of
the social and semiotic environment. Psychedelics thus may have
helped hominins both create and respond to a socio-cognitive
niche, as hypothesized in Figure 1.
This article presents evidence for this claim. First, the
main characteristics of the human socio-cognitive niche
are described. Then, we examine interdisciplinary evidence
supporting the hypotheses that psychedelic ingestion has deep
hominin roots and that psilocybin instrumentalization conferred
adaptive benefits and contributed to the human evolutionary
trajectory involving advancement into a socio-cognitive niche
(Barrett et al., 2007;Whiten and Erdal, 2012). The model of
adaptive utilization of psychedelics presented is informed
by a homeostatic perspective (Forbey et al., 2009) and the
drug instrumentalization paradigm (Müller and Schumann,
2011) to explain potential selective advantages bestowed
by psychedelics to hominins. The model also incorporates
niche-construction (Laland et al., 2016) and gene-culture
coevolutionary (Richerson et al., 2010) processes to specify how
dietary and societal incorporation of psychedelics may have
become evolutionarily significant by imposing a systematic bias
on the selective environment that supported development of a
socio-cognitive niche. The interpersonal and prosocial effects of
psychedelics could have mediated expansion of social bonding
mechanisms such as laughter, singing, dancing, storytelling,
and religion that, in turn, accelerated the rate at which key
biological components of social cognition and religiosity
spread in our lineage.
THE HUMAN SOCIO-COGNITIVE NICHE
Modern humans have complex languages, sophisticated
technology, intricate stores of cultural knowledge and beliefs,
and an advanced theory of mind (Richerson and Christiansen,
2013;Tomasello, 2014). Early hominins may have lacked these
traits (Silk, 2007), but specific selection pressures led to their
acquisition in the Homo lineage (Schwartz and Tattersall,
2015). To explain this constellation of zoologically unusual
features it has been argued that we evolved to specialize in
the cognitive niche (Tooby and Devore, 1987;Cosmides and
Tooby, 2001;Barrett et al., 2007;Pinker, 2010;Bertolotti
and Magnani, 2017). A niche is the structural, temporal, and
social context in which a species exists, defining its mode
of adaptation (Fuentes, 2015). Therefore, the concept of the
“cognitive niche” implies that it is mainly by thinking that
humans succeed in adapting to a wider range of environments
than other animals (Boyd et al., 2011). From this viewpoint,
“improvisational intelligence” was selected in our lineage because
the costs required to sustain it were outweighed by the benefits
of the numerous solutions such intelligence could generate
(Morgan, 2016).
Crucially, however, the human niche is not only about
being smart: this way of life also has a cooperative core that
Frontiers in Psychology | www.frontiersin.org 3September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 4
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
FIGURE 1 | A model of psychedelics instrumentalization by early humans, and of the evolutionary consequences of its intergenerational recurrence. The left side
represents the process of instrumentalization, which can occur repeatedly across the life-span of a generation of hominins. The right side represents the process of
niche-construction supporting gene-culture coevolution across generations as populations construct and bequeath transformed ecological and social environments
that exercise selective influences on following generations (Odling-Smee et al., 2003). The left side of the diagram portrays potential selective advantages conferred
by psychedelic use under the socio-ecological conditions in which our ancestors evolved. The right side illustrates the process of selective feedback through which
psychedelic instrumentalization could have enhanced the creation and evolution of the human socio-cognitive niche. The four colored boxes on the left represent the
major aspects of the emerging human adaptive complex that created the socio-cognitive niche; these involve skills and processes potentially amplified by
psychedelic instrumentalization, with the two-directional arrows between the boxes representing the interconnectedness of these competence realms that coevolved
in creating our unique adaptation mode. The emergence and persistence of this adaptive complex across human evolution permitted the progressive construction of
socially modified environments (represented by the green box at the right side of the diagram) that in turn selected for enhancements in the same underlying human
propensities and capabilities (represented by arrows with a plus [+] sign) that sustained the socio-cognitive niche.
nurtures a “deep social mind,” a way of thinking characterized
by profound mental intermingling and group-mindedness
(Whiten and Erdal, 2012). This novel form of socially infused
thinking (Tomasello, 2014) entails unique cognitive skills
and motivations for collaborating and communicating with
others, such as an altruistic and egalitarian orientation and
the capacity to mindread in order to enhance interpersonal
coordination (Bernhard et al., 2006;Fehr et al., 2008;Heyes
and Frith, 2014). Functioning in this socio-cognitive niche
thus required not just intelligence and technological know-
how, but more importantly the capacity for cooperation
among non-kin and social learning, eventually mediated by
Frontiers in Psychology | www.frontiersin.org 4September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 5
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
language (Barrett et al., 2007;Whiten and Erdal, 2012). Equipped
with this suit of adaptations to richly cooperative social lives
(Sterelny, 2014), humans expanded across the globe, successfully
adapting to a diverse range of habitats (Antón et al., 2014).
We became a ‘generalist specialist,’ not only occupying and
utilizing a diversity of environments, but also specializing
in our adaptation to some of these environmental extremes
(Roberts and Stewart, 2018).
Current understanding of the cognitive niche emphasizes that
humans’ uniquely developed ability to learn from others was
absolutely vital for their ecological success because it enabled
the gradual accumulation of information and technologies across
generations and the development of well-adapted bodies of
local knowledge and complex social arrangements beyond the
individual capacity to invent alone (Boyd et al., 2011;Richerson
and Christiansen, 2013;Sterelny, 2014). Therefore, as has
been cogently argued by Boyd et al. (2011) and Whiten and
Erdal (2012), and empirically shown by Morgan (2016), the
cognitive niche is eminently a social and cultural niche. We
adapt not through intelligence alone but primarily through the
skills, values, ideas, information, and expected modes of social
interaction acquired from others in distinctively prosocial and
culturally scaffolded milieus. The expansion of sociality and inter-
generational cultural learning in our lineage was thus crucial for
the reliable preservation of various types of expertise and the
expansion of cognitive capital via cumulative cultural evolution
(Sterelny, 2012, 2014).
The human socio-cognitive (or cultural) niche is
simultaneously selection pressure and adaptive response
(Downey and Lende, 2012). It was built and reshaped by
hominins, who consequently modified the evolutionary
pressures acting on them, on their descendants, and on unrelated
populations sharing the same landscape (Laland and O’Brien,
2011). The various aspects of social cognition and behavior of
the cognitive niche are dynamic components that established
reinforcing relationships among themselves (e.g., mindreading
and culture create, and in turn, are sustained through sociality),
embodying an interconnected, adaptive complex that sustains
our unique survival mode (Whiten and Erdal, 2012). Hence, the
emergence of Homo was characterized by an auto-catalytic niche
construction process; an iterative dynamic whereby increasing
cognition, dietary quality, and cooperative behavior resulted in
lowered extrinsic mortality risk and favored changes in brain
size, body composition, life-history parameters, and behavioral
and communicative complexity (Kaplan et al., 2000;Antón and
Snodgrass, 2012;Fuentes, 2015).
The socio-cognitive niche theory invokes the undeniable
practical advantages of increased cognition, sociality,
communication, and social learning in order to explain the
evolution of human uniqueness. Our model and the supporting
evidence reviewed below suggest that the instrumentalization
of psilocybin could have enhanced performance on each
of these interrelated competence domains (see left side of
Figure 1), potentially increasing the adaptability and fitness of
our ancestors. The psychedelic instrumentalization model also
proposes that psilocybin consumption had niche-constructing
effects that imposed a systematic bias toward a socio-cognitive
niche across the human evolutionary trajectory (see right side of
Figure 1).
ANCIENT HOMININ DIETS AND THE
ECOLOGY OF
PSILOCYBIN-CONTAINING FUNGI
Hominin encounters with macroscopic fungi growing on the
soil surface must constitute a very ancient and continual
phenomenon that demanded behavioral adaptations. Fungi are
widely distributed across ecozones and comprise not only
valuable foods and medicines, but also highly toxic and even
quickly fatal substances. Sporocarps (fungal fruitbodies) are
much more abundant in the forest understory than in the middle
and upper canopies where most primate species tend to live
(Hanson et al., 2003). Once our hominin ancestors habitually
foraged on the floors of forests and in meadows, especially
in tropical areas, they recurrently encountered mushrooms.
By necessity, they experimented with mycophagy and found
out which species could be safely eaten as food or carefully
exploited as medicine. Likewise, when psilocybin containing
fungi were consumed in large enough quantities they caused
dramatic alterations in perception and consciousness, drawing
attention to their properties and their positive and negative effects
on well-being. As a consequence, memories (and eventually
cultural traditions) were formed regarding the identification of
these species and the resulting effects of their ingestion. As
has been hypothesized for non-human primate self-medicative
behaviors (see Huffman, 1997), traditions of medicinal use of
psychedelic mushrooms may have started as a result of ill, hungry
hominins trying new foods during periods of extreme food
scarcity, and upon recovery, associating their improved health
with the new dietary item. Subsequently, local enhancement (i.e.,
naïve individuals having their attention drawn to species used by
others) and social learning could have played a role in spreading
the behavior though the group.
While incontrovertible direct evidence of psychedelic
mushroom ingestion by ancient humans (e.g., dental calculus
containing psilocybin mushroom tissue or spores) is lacking,
there is direct evidence of the ingestion of edible mushrooms
(O’Regan et al., 2016) and medicinal plants (Hardy et al.,
2013) derived from analysis of dental calculus recovered from
remains of humans from the Upper Paleolithic. There are 22
primate species known to eat fungi (Hanson et al., 2003), and
African great apes, in particular, are known to ingest a variety
of non-nutritional plants to “treat” homeostatic challenges
[e.g., to aid in the control of intestinal parasites and/or provide
relief from related gastrointestinal upset (Huffman, 1997)]. It
thus seems highly unlikely that our hominin ancestors ignored
the widespread coprophilic species of psilocybin containing
mushrooms conspicuously growing on ungulates’ dung (e.g., the
pantropical Psilocybe cubensis), especially since Plio-Pleistocene
hominin activities of scavenging, hunting, and eventually
domestication of bovines placed this psychedelic within the
sphere of daily activities (see van Ginneken et al., 2017 for
evidence and discussion regarding the similarity of migration
Frontiers in Psychology | www.frontiersin.org 5September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 6
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
routes of early bovines and early hominins and its implications
for understanding our ancestors’ pan-African dispersal). As will
be shown below, the likelihood of intentional and repeated use
of psilocybin is supported by its low toxicity and by its close
resemblance to the neurotransmitter serotonin, which opened
up the possibility for its exploitation as a “treatment” for a
significant homeostatic challenge recurrent in a socio-cognitive
niche – serotonin depletion.
TRADITIONAL PSILOCYBIN
MUSHROOM INGESTION AND THE
ANTIQUITY OF RITUAL PSYCHEDELIC
USE
Frost (2017) reviews reports from Mesoamerican transegalitarian
agricultural societies during the early contact period with the
Spanish, illustrating a range of uses for psilocybin mushrooms
that involve healing, spiritual, ritual, social, festive, and divinatory
practices, some still reported in the 20th century (e.g., Estrada,
1989) among the Mazatecs of Oaxaca in southern Mexico. The
Nahua, for instance, used these fungi in the rituals performed
by Mexica (Aztec) clergy, and on a local, personal level through
the assistance of medicinal/divinatory aid of ticitls (shamanistic
healers). In the context of the official religious system, psychedelic
mushroom consumption characterized notions of hospitality and
ostentatiousness amongst the Mexica elite, and involved intricate
ritual performances that included call and response, chanting,
and dancing, as described in Hernando de Alvarado Tezozómoc’s
Crónica Mexicana (written circa 1598) (Frost, 2017). Modern-
day Mazatecs employ psilocybin mushrooms mainly to find lost
items, discover hidden truths, or diagnose an ailment in the
context of nocturnal rituals in which it is common for both
healer and client/patient to consume the mushrooms (Estrada,
1989). This ceremony involves whistling, humming, chanting,
singing, percussive artistry, ventriloquism, and dancing. To our
knowledge, there are no documented foraging societies that use
psilocybin fungi. This may be due, in part, to the fact that
mushrooms grow mainly during the rainy season, a particularly
difficult time for ethnographers to accompany the already
challenging nomadic lifestyle of foragers. Possible evidence of the
use of psilocybin-containing mushrooms among early Neolithic
farming and herding communities may be present in rock
carvings and paintings [e.g., in Africa (Samorini, 2020) and Spain
(Akers et al., 2011), also see Winkelman (2019a) for review].
The utilization of psilocybin mushrooms or other psychedelic
plants is documented in the ethnographic and historical
literature from all cultural regions of the globe except the
Insular Pacific (see Table 1 for examples). It is likely that
psychedelics have been used ritually for millennia, and that
this behavior has deep hominin roots. Evidence regarding
the evolution of human hepatic enzymes suggests significant
selection pressures were exerted on hominin populations by
frequently encountered environmental chemicals, including
fungal and vegetal secondary metabolites that act as stimulants,
narcotics, and hallucinogens (Sullivan and Hagen, 2002;
Sullivan et al., 2008). Drug consumption is not an evolutionary
novelty; rather, ancient and recent exposures resulted in evolved
countermeasures to tolerate them to some degree and safely
metabolize them. Evidence of humans’ relationships with
psychedelics during more recent times (the Holocene) is found
in the archeological and paleoethnobotanical record (Guerra-
Doce, 2015;Fitzpatrick, 2018;Miller et al., 2019;Samorini,
2019;Robinson et al., 2020). While the presence of psychoactive
plant remains in archeological contexts does not establish their
use as drugs, it is highly probable in many instances given
known ethnographic analogies, artifactual associations, and
iconographic interpretations (Guerra-Doce, 2014;Winkelman,
2019a;Domnauer, 2020).
HOMEOSTASIS OF INGESTIVE
BEHAVIORS AND THE DRUG
INSTRUMENTALIZATION PARADIGM
Natural landscapes are a diverse combination of plant species that
are literally nutrition centers and pharmacies with a wide range of
primary (nutrient) and secondary (pharmaceutical) compounds
TABLE 1 | Selected societies from all over the world that employ psychedelics acting on the serotonergic system.
Region Subregion Culture Species employed Common
name
Main psychoactive
principles
References
Africa West Africa Fang Tabernanthe iboga eboka ibogaine, ibogamine Rätsch (2005)
Africa Eastern Africa Maasai Acacia nilotica olkiloriti dimethyltryptamine (DMT),
tetrahydroharman
Sobiecki (2002)
Middle East Middle East Iran Peganum harmala haoma harmine, harman Flattery and Schwartz (1989)
Asia East Asia Chinese Gymnopilus junonius xiàojùn psilocybin, psilocin Zhang and Greatrex (1987)
Europe Southeastern Europe Greeks Claviceps spp. kykeon ergometrine, ergotamine Samorini (2019)
North America Arctic and Subarctic Ojibwa Lophophora williamsii peyote mescaline, pellotine Barnouw (1950)
Middle America and
the Caribbean
Central Mexico Mazatec Psilocybe spp. ndi xi tjo psilocybin, psilocin Estrada (1989)
South America Amazon and Orinoco Tukano Banisteriopsis caapi+
Diplopterys cabrerana
yagé harmine, harmaline +DMT Jackson (1983)
South America Southern South
America
Mataco Anadenanthera
colubrina var. cebil
cebil DMT, 5-MeO-DMT Dijour (1933)
Frontiers in Psychology | www.frontiersin.org 6September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 7
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
vital to the health of plants and herbivores (Villalba and
Provenza, 2007). Animals generally avoid secondary metabolites
(which typically have negative physiological and behavioral
consequences following their ingestion) while selecting nutrient-
rich foods. However, a homeostatic perspective suggests that
dietary selection is not guided simply by avoidance of plant
secondary metabolites, but, in some cases, by their selection
to ameliorate other challenges (Forbey et al., 2009). From
this view, food selection is a quest for substances (whether
nutrients or drugs) that provide homeostatic utility for the
organism (Villalba and Provenza, 2007). Hence, potentially
toxic secondary metabolites in fungi and plants might be
actively selected by animals to achieve homeostasis. Evidence
shows animals exploit the biological activity of secondary
metabolites to mitigate the costs of infection by parasites, enhance
reproduction, moderate thermoregulation, avoid predation, and
increase alertness (Rodríguez and Wrangham, 1993;Huffman,
1997;Forbey et al., 2009).
Similarly, drug instrumentalization theory proposes that
non-addictive drug use can be explained in functional terms
as a purposeful adaptive process. It proposes humans and
many animal species seek and consume psychoactive substances
because the subsequent effects on mental states can be utilized
to improve performance of goal directed behaviors (Müller
and Schumann, 2011;Müller, 2020). From this viewpoint,
repeated, non-addictive drug use should be modeled as a two-
step process: (1) the seeking and consumption of a psychoactive
drug in order to change the present mental state into a
previously learned mental state, which then allows for (2)
better performance of other, previously established behaviors and
enhanced goal achievement (Müller and Schumann, 2011). Some
instrumentalization goals proposed by the researchers include:
improved social interaction; improved cognitive performance
and counteracting fatigue; facilitated recovery and coping
with psychological stress; and facilitation of spiritual and
religious activities.
According to the homeostatic perspective, the probability
of secondary metabolite exploitation is determined by the
relative difference between the cost of a challenge and the
toxicity of the secondary metabolite in question; the ultimate
“goal” for the animal being to regulate homeostasis, achieving
a balance between minimizing the cost of a challenge and
minimizing toxicity (Forbey et al., 2009). We review next
substantial evidence that psilocybin possesses very low toxicity
and generates very few and unimportant negative side effects.
This quality, in combination with the relatively high costs of
the challenge it could potentially ameliorate (i.e., serotonin
depletion) and the adaptive behaviors it could facilitate
(discussed afterward), made psilocybin a prime candidate for
instrumentalization in our lineage.
TOXICITY OF PSILOCYBIN AND
ASSOCIATED COSTS
Hagen et al. (2013) propose that plant neurotoxins currently
used as drugs illustrate the necessity of their characterizations
in terms of acute drug toxicity because of their fitness costs;
however, the situation of psychedelics is dramatically different.
Although there is a general public perception that psychedelics
are dangerous, from a physiologic viewpoint they are one of
the safest classes of central nervous system drugs (Nichols,
2016). Psilocybin, in particular, is exceptionally harmless. This is
reflected by its high therapeutic index, 641, which is indicative
of very low toxicity (Tylš et al., 2014). van Amsterdam et al.’s
(2011) review of literature on psilocybin risks found that in
spite of moderate acute toxicity, psilocybin has low chronic
toxicity and negligible public health risk. Other public health
assessments have similarly concluded that psilocybin mushrooms
are the safest of all common recreational drugs (Gable, 2004;Nutt
et al., 2010;Studerus et al., 2011). Moreover, psilocybin is not
neurotoxic, its lethal to psychoactive dose ratio is estimated at
1000:1, it has little or no potential for creating dependence, and
there is no evidence of long-term cognitive impairment (Johnson
et al., 2008;Tylš et al., 2016).
Even though some adverse physical effects may occur
during psychedelic action, most commonly dizziness, nausea,
drowsiness, paraesthesia, blurred vision, and dilated pupils, they
are relatively unimpressive even at doses yielding powerful
psychological effects (Johnson et al., 2008). Higher doses are more
likely to cause anxiety or fear due to feelings of ego dissolution
or lack of control (Johnson and Griffiths, 2017), as well as
paranoid and delusional thinking (Carhart-Harris et al., 2016b),
but even exceptional overdoses don’t lead to enduring harms
(Haden and Woods, 2020). Side effects such as derealization,
depersonalization, long lasting unpleasant experiences (bad
trips), and psychotic reactions can also occur (Strassman, 1984);
however, psychological interventions are mostly sufficient and
the risk of prolonged psychosis (lasting longer than 48 h) in
otherwise healthy subjects after a single dose of psilocybin is
rare; and in most cases, prolonged negative effects are associated
with personality predispositions (Johnson et al., 2008). A large
population study of 130,000 adults in the United States found
no link between the use of psychedelics and suicidal behavior or
mental health problems (Johansen and Krebs, 2015). Typically,
when psychedelics are administered in a supportive, controlled
environment (ritual or clinical setting) no severe acute or chronic
adverse effects occur, and no overdose deaths have been reported
after ingestion of typical doses of LSD, psilocybin, or mescaline
(Nichols, 2016).
The notable potential cost of psychedelic ingestion involves
the loss of cognitive structuring, opening the possibility for errors
in judgment, false perceptions, distortions, and illusions that
could undermine an individual’s capacity for alertness, strategic
thinking, and decision-making. This specific cost (excessively
“relaxed beliefs”; see Carhart-Harris and Friston, 2019), coupled
with the rapid onset of mental tolerance and lack of hedonic
reward (craving or withdrawal) help explain why psychedelic
use is normally episodic and not compulsive, with chronic use
being relatively unusual (Nichols, 2004, 2010). The ontologically
shocking effects of psychedelics and their meaning-enhancing
properties is likely why their use commonly occurs in engineered
social contexts (e.g., in intense and immersive shared experiences
consisting of multimodal performances of music, ritual, and
Frontiers in Psychology | www.frontiersin.org 7September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 8
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
dance: Sterelny, 2018;Winkelman, 2021c; also see St John,
2006). These factors of set (i.e., intentions, mood state, and
expectations) and setting (i.e., context of ingestion, involving
all sensory modes, social environment, and the set of those
present) provide for protection of the psyche and integration
of the experience (Dobkin de Ríos, 1984;Hartogsohn, 2016;
Lifshitz et al., 2018). It seems human ancestors learned to employ
psychedelics in specific contexts and in conjunction with certain
“protective” behaviors that allowed them to minimize and endure
negative effects (costs) and maximize and counter exploit certain
qualities to maintain homeostasis and manage the challenges
of group living.
PSYCHEDELIC SELF-MEDICATION AS A
“TREATMENT” FOR SEROTONIN
DEPLETION
From a homeostatic perspective, increased fitness can potentially
result from consumption of psychoactive plants containing
compounds that chemically resemble endogenous signaling
molecules, especially when internal signaling functions are
compromised [e.g., due to deficiencies in dietary precursors
in marginal environments (Sullivan and Hagen, 2015)]. Our
proposal is that the incidental ingestion of psilocybin and
other psychedelic secondary metabolites that have very low
toxicity and structurally resemble the neurotransmitter serotonin
(5-hydroxytryptamine; 5-HT) provided a “treatment” for 5-
HT depletion, a costly challenge likely recurring throughout
advancement into a socio-cognitive niche (see e.g., Young and
Leyton, 2002;Wood et al., 2006). Consequent to this self-
medicative behavior was the development of cultural traditions of
psilocybin use to ritually and symbolically exploit its salutogenic,
sociality expanding, and cognitive enhancing effects (see below).
Hominin evolution occurred in settings of strong climatic
and environmental variability (Potts, 2013) and involved
an increasing interdependence and reliance on intelligence,
cooperation, and learning from others (Sterelny, 2012). This
dynamic inevitably placed a higher strain on the serotonergic
system given its involvement in facilitating stress relief and
mental flexibility (Carhart-Harris and Nutt, 2017;Nilsson et al.,
2019) by regulating perception, cognitive function, mood,
memory, and social behavior (Berger et al., 2009;Friedman, 2018;
Tricklebank and Daly, 2019).
Humans cannot produce the amino acid tryptophan,
precursor in the biosynthesis of 5-HT, and must obtain it
through their diet (Friedman, 2018). Given early hominins’
diets low reliance on tryptophan-rich foods such as seeds, nuts,
red meat, and fish (Hublin and Richards, 2009;Ungar and
Sponheimer, 2011) they certainly faced deficits of this essential
amino acid with the potential to perturb homeostasis through
lowered levels of 5-HT. Under such circumstances, tryptamine
psychedelics (e.g., DMT, psilocybin) could have provided an ideal
substitute for a fundamental bioactive compound that is hard
for the body to produce, effectively mimicking 5-HT’s structure
and function (Nichols, 2016). Self-medication with psilocybin
mushrooms would have ameliorated the costs associated with
impairment of serotonergic neural signaling, involving depressed
mood (Jenkins et al., 2016), increased stress vulnerability (Sachs
et al., 2015), and cognitive inflexibility (Kanen et al., 2020).
5-Hydroxytryptamine moderates anxiety and stress, promotes
patience and coping, and under conditions of increased
environmental volatility, opens a window of plasticity for greater
adaptation (Branchi, 2011;Miyazaki et al., 2012;Carhart-
Harris and Nutt, 2017). Therefore, the brain displays two
different serotonin-mediated responses to adversity: a default
response involving a passive coping strategy (i.e., tolerating a
source of stress) mediated by 5-HT1A receptor signaling; and
an active coping strategy that provides an enhanced capacity
for change that is mediated by 5-HT2A receptor signaling
(Carhart-Harris and Nutt, 2017). Interestingly, serotonergic
psychedelics preferentially engage the 5-HT2A receptor signaling
pathway, functionally modulating its activity (Nichols, 2016;
Carhart-Harris and Nutt, 2017). Psilocybin thus stimulates
a system that evolved to mediate rapid and deep learning
when faced with environmental demands for change (Brouwer
and Carhart-Harris, 2021). From the homeostatic and drug
instrumentalization perspective developed here, this capacity
of serotonin-mimicking psychedelics to enable a hyper-plastic
state that can aid psychological transformation when (actual or
perceived) environmental pressures demand it (Brouwer and
Carhart-Harris, 2021) helps explain why ritualized psychedelic
consumption became central to group healing, decision-making,
management of ecological relations, and creation of individual
and social identity in many premodern societies (Rätsch, 2005;
Guerra-Doce, 2014, 2015;Kennedy, 2014).
The negative impact of 5-HT depletion on fitness likely
increased as hominization ensued given an escalating dependence
on cognitive skills for an intensively cooperative and collective
life (Dunbar, 2014;Gamble et al., 2014). Under these conditions
of demands for functioning in a socio-cognitive niche, higher-
order executive tasks such as social learning, working memory,
and behavioral flexibility became increasingly important; this
generated an increased demand for sufficient levels of 5-HT
to modulate the function of the prefrontal cortex, on which
these skills critically depend (see Puig and Gulledge, 2011).
Considering the costly nature of 5-HT production, its key role in
hominin adaptive brain function and behavior, and the increasing
selection pressures for sophisticated social cognition skills for
participation in the socio-cognitive niche, it is reasonable –
perhaps inevitable – that early hominins actively pursued
available exogenous chemical analogs of 5-HT.
Importantly, as meat became a more pervasive item in later
hominins’ diet, it is likely that tryptophan deficits were less
common since it is present in high quantities in most protein-
based foods (Friedman, 2018). This means that if psychedelics
were initially used among hominins and archaic human species to
“treat” 5-HT depletion, reliance on this self-medicative behavior
may have become less important as our human ancestors’ diet
progressively included seeds and nuts, as well as larger quantities
of meat from large animals and fish. Thus, while psychedelics may
have entered hominin evolution via their role as a “treatment”
for 5-HT depletion, once full “migration” into a socio-cognitive
niche was complete (which involved establishment of a foraging
Frontiers in Psychology | www.frontiersin.org 8September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 9
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
strategy extended to large mammalian prey) their ingestion
was likely sustained because of the additional adaptive benefits
their ritual and symbolic instrumentalization could confer to
humans properly (see below). In other words, while tryptophan
deficiency was likely no longer an issue among hunter-gatherer
societies or prehistoric horticultural/agricultural societies, the
premium placed on cognitive and social functions by the socio-
cognitive niche meant there was still a place for counter exploiting
psychedelics’ effects in our lineage.
PSYCHEDELIC INSTRUMENTALIZATION
IN THE HUMAN SOCIO-COGNITIVE
NICHE
Entry into the socio-cognitive niche involved increasing
cognition, sociality, communication, and social learning.
Figure 1 summarizes a model of how these major aspects of the
emerging human adaptive complex were potentially enhanced
by incidental psychedelic ingestion and periodic psychedelic
instrumentalization. The model suggests psilocybin would have
amplified the requisite capacities for increasingly complex social
interaction and a suite of cognitive abilities supportive of the
socio-cognitive niche, including aspects of creativity, non-verbal
and linguistic expression, and suggestibility (left side of Figure 1).
These effects could have facilitated general problem solving,
cooperative foraging, ritual healing, conventional representation
and symbolization (including myth and identity formation),
and enculturation practices (e.g., rites of passage). The following
sections integrate current understanding of the socio-cognitive
niche with recent psychedelic research (mainly controlled
experimental studies in humans, both in clinical populations
and healthy volunteers) to illustrate how psychedelics could
have been adaptively employed by our ancestors. We focus
on four interrelated psychedelic instrumentalization goals:
management of psychological distress and treatment of health
problems; improved social interaction and interpersonal
relations; facilitation of collective ritual and religious activities;
and enhanced group decision-making.
Management of Psychological Distress
and Treatment of Health Problems
Foraging is not a safe activity; it leads to significant mortality and
morbidity. Even cooperative hunting, for example, is accident
prone, attacks by wounded animals being paramount (Klein,
1999). Human ancestors suffered from infectious pathogens
(e.g., bacteria, viruses, parasites) and social stress management
imposed pressure on their time budget as group size increased
(Gamble et al., 2014). We suggest under these conditions of
disease and stress, psychedelic use could have improved stress
management, healing, and well-being. Psychedelics can facilitate
adaptive stress coping via upregulation of 5-HT2A receptor
functioning (Carhart-Harris and Nutt, 2017), bringing about
a “pivotal mental state” characterized by an enhanced rate
of associative learning and the potential for the mediation
of stress through psychological or cognitive transformations
(Brouwer and Carhart-Harris, 2021). These effects in enhancing
active coping strategies illustrate a core aspect of psilocybin’s
potential contributions to hominin adaptability and fitness.
Psychedelic abatement of psychological distress can aid
in the treatment of mental illness. In contemporary clinical
contexts, psychedelics have effective psychiatric applications,
particularly in the treatment of stress-related disorders (dos
Santos et al., 2016;Garcia-Romeu et al., 2016;Carhart-Harris
and Goodwin, 2017;Johnson and Griffiths, 2017;Goldberg et al.,
2020a;Luoma et al., 2020;Reiff et al., 2020;Vollenweider and
Preller, 2020;Carhart-Harris et al., 2021;De Gregorio et al.,
2021a;Inserra et al., 2021). Winkelman and Sessa’s (2019)
edited volume contains reviews of clinical evidence showing
the therapeutic effectiveness of psychedelics in the treatment of
various health conditions, including anxiety, trauma, treatment-
resistant depression, as well as personality, inflammatory, and
autoimmune conditions (also see Szabo, 2019;Thompson and
Szabo, 2020). The immersive experiences engendered by high
doses of psychedelics are often attributed deep personal meaning,
and a growing body of theoretical and empirical work shows
they can have persisting beneficial effects on well-being and
psychosocial functioning (Kuypers et al., 2016;Sweat et al.,
2016;Bouso et al., 2018;Haijen et al., 2018;Carhart-Harris and
Friston, 2019;Kuypers, 2019;Mason et al., 2019, 2021;Preller
and Vollenweider, 2019;Barrett et al., 2020;Girn et al., 2020;
Goldberg et al., 2020b;Yaden and Griffiths, 2020). There are also
hints that lifetime psychedelic use is associated with markers of
physical health (self-reported overall health, body mass index,
and heart condition and/or cancer in the past 12 months:
Simonsson et al., 2021).
Most pre-modern societies considered illness to be caused
by supernatural and spiritual agents (Schultes et al., 2001;
Rätsch, 2005); psychedelics can contribute to cures because
they produce spiritual experiences and a sense of control
over preternatural realms (Dobkin de Ríos, 1984;Furst, 1990;
Winkelman, 2010). Many shamanistic healing traditions use
psychedelics to facilitate an experience of contact between the
ritual specialist and supernatural beings/realms, inducing visions
that provide knowledge about the causes of the condition
afflicting the patient and proper treatment, or allowing healers to
confront and combat a disease through symbolic battles with its
cause (Rivier and Lindgren, 1972;Harner, 1973;Dobkin de Ríos,
1984;Ferreira Júnior et al., 2015).
Psychedelics’ imagery-inducing (de Araujo et al., 2012),
meaning-enhancing (Hartogsohn, 2018), and contextual effects
(Carhart-Harris et al., 2018b) can play an important role
in boosting imagination, the placebo effect, and hypnotic
suggestibility, thereby favoring salutogenesis through
psychoendoneuroimmunological processes (Ray, 2004).
Psychosocial healing is a component of human cooperation
that comprises empathy, mirroring, emotional contagion, self-
regulation, and mentalizing; it also recruits symbolic processes
requiring shared meanings of symbols (Kohrt et al., 2020).
Thus, besides the psychedelic substance, other ritual elements
(e.g., cultural expectations, mimetic enactments, verbal displays,
songs, and dances) also serve an important function in enabling
healing (Winkelman, 2008, 2019b, 2021a,c;Uthaug et al., 2021).
Frontiers in Psychology | www.frontiersin.org 9September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 10
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
The fact that psychedelics induce an experience of well-being
may have favored learning of their use by humans (Johns,
1990). Rodriguez et al. (1982) suggest hallucinogenic plants
were initially used for the treatment of diseases due to their
antiparasitic properties. As argued by Ferreira Júnior et al. (2015),
the overlap between medicinal and hallucinogenic uses may
indicate that the initial consumption of a plant for medicinal
purposes lead to the discovery of its use as a hallucinogen. This is
consistent with our view that psychedelics were initially ingested
because they could provide homeostatic utility.
Improved Social Interaction and
Interpersonal Relations
Humans, like all primates, are intensely social. The human
niche encompasses face-to-face interactions within social groups,
interactions among social groups, and complex social dynamics
at both group and larger community levels (Fuentes, 2015).
Human ancestors faced the adaptive problem of maintaining the
cohesion of large social groups in the face of the centrifugal
forces created by the stresses of group living. Primates solve this
problem by developing intense forms of commitment to each
other through close physical proximity and the use of touch (e.g.,
licking and other social grooming behaviors [Dunbar, 2010]).
Hominins evolved larger group sizes (100–200 individuals)
by developing indirect ways (i.e., without physical contact)
of triggering endorphin activation that produces community
bonding (Dunbar, 2014;Gamble et al., 2014). In sequential order,
these extended grooming behaviors involved laughter (a form of
chorusing), singing (without words), dancing, storytelling, and
more recently, religion – activities that stimulate the endogenous
opioid mechanisms that enhance the sense of being bonded with
others involved (Pearce et al., 2015;Tarr et al., 2015;Dunbar et al.,
2016;Charles et al., 2020). The enhanced emotional ties provided
human groups with a higher degree of cohesiveness and stability
through time, enhancing various forms of cooperation.
We propose that in this context, psychedelics’ effects were
harnessed to modulate the strength and quality of social bonds.
Ingestion of psilocybin induces euphoria, involuntary grinning,
uncontrollable laughter, giddiness, playfulness, and exuberance
(Preller and Vollenweider, 2016); it also enhances engagement
with music (Kaelen et al., 2018) and eloquence (Doyle, 2011).
This means psilocybin ingestion would have amplified sociality
long before the emergence of religious rituals. Once archaic
humans developed religious and spiritual concerns (see following
section on Facilitation of collective ritual and religious activities),
psilocybin would have become even more useful given its
intrinsic ability to produce mystical-type experiences involving
the dissolution of self-boundaries and a sense of unity with
others (Griffiths et al., 2006, 2011). Therefore, psychedelic use
increased participation in the emerging niche in which sociality
enhancing experiences such as playing and laughing, singing
and dancing, fantasizing and telling stories, and participating in
religious rituals became commonplace activities. Collective use
of psychedelics may have thus enriched social life and bolstered
hermeneutical and rhetorical activity, enhancing management of
group tension (through emotional catharsis) and strengthening
social bonds (by triggering the endorphin system), ultimately
facilitating complex sociality and communication in the ever-
larger human groups.
Recent studies show that psychedelics can modify a range
of social behaviors and cognitive processes, having pro-social
effects (Table 2; also see Preller and Vollenweider (2019) for
a recent review of experimental and controlled studies in
humans). Psilocybin has been shown to modulate different
objective measures of social cognition; most importantly, it
increases empathy for positive emotions (Pokorny et al., 2017)
and reduces recognition and processing of negative emotional
faces (Schmidt et al., 2013), which facilitates social approach
behaviors and thus social interaction (Preller and Vollenweider,
2019). Psilocybin also increases altruistic behavior: employing
the Ultimatum Game, Gabay et al. (2018) found that it reduced
costly punishment by increasing the participants’ concern for
the outcome of interacting partners. Furthermore, psilocybin
shifts emotional biases away from negative toward positive
stimuli (Kraehenmann et al., 2016), and a single high-dose
experience can engender measurable and long-lasting changes in
socially oriented aspects of personality, such as increases in the
dimensions of Openness and Extraversion (MacLean et al., 2011;
Bouso et al., 2018;Erritzoe et al., 2018).
The unusually high level of intragroup tolerance and
cooperative communication of modern humans is explained
by selection for prosociality (or against aggression), a process
that has been described as self-domestication (Benítez-Burraco
et al., 2020). Selection likely modulated tolerance with increased
brain 5-HT levels (Hare, 2017;Raghanti et al., 2018), which is
consistent with the scenario developed here in which serotonergic
psychedelics provided homeostatic utility by substituting for
5-HT under circumstances in which endogenous biosynthesis
and thus signaling functions were compromised. Changes in
social cognition also relied on decreases in emotional reactivity
supported by shifts in the hormonal and subcortical profiles (e.g.,
amygdala reactivity) linked to temperament, which then allowed
cognitive skills to be expressed in new social situations (e.g., in
teaching contexts) (Hare and Tomasello, 2005;Hare, 2017). It
is thus noteworthy that a single dose of psilocybin decreases
amygdala reactivity to negative stimuli and increases positive
mood state (Kraehenmann et al., 2016; also see Rocha et al.,
2019). Such shifts in affect and the neural correlates of affective
processing can endure for several weeks beyond acute drug effects
(Barrett et al., 2020). This suggests that psychedelics increased
social tolerance and cohesion by inducing socially desirable
mood changes from reduced neural responses to negative stimuli
(Kometer et al., 2012;Mueller et al., 2017;Barrett et al., 2020;
Vollenweider and Preller, 2020).
Recent work with rodents has unveiled a mechanism of
action potentially underlying the prosocial effects of psychedelics.
De Gregorio et al. (2021b) have demonstrated that repeated
administration of low doses of LSD in mice enhances
social interaction by potentiating 5-HT2A and AMPA receptor
neurotransmission in the medial prefrontal cortex via an
increasing phosphorylation of the mTORC1 (a protein involved
in the modulation of social behavior). Moreover, psilocybin
has been found to increase striatal dopamine concentrations
Frontiers in Psychology | www.frontiersin.org 10 September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 11
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
TABLE 2 | Evidence for enhanced social and interpersonal capacities during and after psychedelic exposure.
Potentially adaptive
effect
Study Summary of results Subject population Total number
of subjects
Enhanced social
approach behaviors
and social interaction
Kometer et al. (2012);
Dolder et al. (2016);
Pokorny et al. (2017)
↑positive mood states, ↓recognition of negative facial expression,
and ↑behavior toward positive relative to negative cues
LSD ↑happiness, trust, closeness to others, emotional empathy,
and sociality
↑explicit and implicit emotional empathy
Healthy subjects
Healthy subjects
Healthy subjects
17 (6 females)
40 (20 females)
33 (15 females)
Enhanced social
connectedness
Watts et al. (2017) ↓disconnection (from self, others, and the outside world), ↓
avoidance of difficult emotions and memories, and ↑acceptance
Patients with
treatment-resistant depression
20 (6 females)
Enhanced emotional
self-control and
tolerance
Barrett et al. (2020) ↓negative mood, ↑positive mood, and ↓amygdala response to
negative affective stimuli; reflecting ↑top-down control of
emotionally conflicting information
Healthy subjects 12 (7 females)
Enhanced prosocial
attitudes/behaviors and
healthy psychological
functioning
Griffiths et al. (2018) Positive changes on longitudinal measures of interpersonal
closeness, gratitude, life meaning/purpose, forgiveness, and
altruistic behavior
Healthy subjects 75 (45 females)
Positive personality
changes
MacLean et al. (2011);
Erritzoe et al. (2018);
Netzband et al. (2020)
↑Openness (sustained 1 year after the session)
↓Neuroticism and ↑Extraversion (sustained at 3-month follow-up)
Ayahuasca ↑agreeableness and ↓neuroticism (sustained in a
6-month follow up)
Healthy subjects
Patients with
treatment-resistant depression
Patients with depression,
anxiety, or post-traumatic
stress disorder
52 (30 females)
20 (6 females)
24 (9 females)
In all studies, psilocybin was the substance administered, unless otherwise stated.
↑, increased; ↓, decreased.
in humans, a mechanism partly underlying euphoria and
depersonalization phenomena (Vollenweider et al., 1999). Striatal
dopamine promotes social living and increases reward emanating
from social interactions (Rilling and Sanfey, 2011). The human
striatum exhibits a unique neurochemical profile involving
high dopamine levels, consistent with humans’ distinctive
ultrasociality (Raghanti et al., 2018). This suggests psilocybin
instrumentalization could have favored a dopamine-dominated
striatum personality style, which is associated with enhanced
sensitivity to social cues that promote social conformity,
empathy, and altruism (see Raghanti et al., 2018).
Facilitation of Collective Ritual and
Religious Activities
Rituals are socially stipulated, conventional behaviors that are
critical for group social interaction; they also drive cultural
transmission within and between generations (Legare and
Nielsen, 2020). Rituals are very diverse and complex, but often
involve synchronic movement, causally opaque action, and both
euphoric and dysphoric arousal (Whitehouse and Lanman, 2014;
Boyer and Liénard, 2020). Ritualized behaviors in the animal
kingdom have the basic function of enhancing coordination
and cooperation (Winkelman, 2009, 2019b,c). In humans, they
also have other social, psychological, and instrumental functions
involving, for instance, signaling commitment to others, binding
group members together, and reducing individual and collective
anxiety (Boyer and Liénard, 2020;Legare and Nielsen, 2020;
Nielsen et al., 2020). In traditional cultures, rituals often have
goals related to survival and reproductive success such as curing
an illness, harming a rival, or ensuring success in hunting
(Rossano, 2020). They are particularly crucial during times
of transition, risk, and uncertainty in the human lifespan
(Legare and Nielsen, 2020).
Religion comprises symbolically and emotionally laden beliefs
and practices (e.g., rituals) regarding superhuman powers, and
the institutions that maintain and transmit such beliefs and
practices (Bulbulia et al., 2013). A wealth of ethnographic and
experimental evidence suggests that religions forge solidarity
and cooperation through various mechanisms and at different
levels of social complexity (Katz, 1984;Boehm, 1993;Winkelman,
2013b, 2021b;Norenzayan et al., 2016;Skoggard et al.,
2020). Early religious forms developed in the context of
intense and immersive experiences of music, ritual, and dance
(Dunbar, 2017, 2020), likely in combination with psychedelics
(Sterelny, 2018;Winkelman, 2019b,c, 2021a,c) and other mind-
altering techniques (Rossano, 2007, 2009). Dunbar (2017, 2020)
suggests these shamanic type religions based on trance-dancing
evolved sometime between the appearance of archaic humans
(i.e., Heidelbergensians) around 500,000 years ago and the
appearance of anatomically modern humans (Homo sapiens)
around 200,000 years ago as one of a series of behaviors that
humans developed to enhance social bonding by triggering the
endorphin system.
Foragers mainly utilize psychedelics in shamanic rituals
(Harner, 1973;Dobkin de Ríos, 1984;Winkelman, 2010, 2013a)
indicating a key aspect of psychedelic instrumentalization was
incorporation into prosocial contexts involving synchronic
activities (e.g., ritual, drumming, dancing, and singing) that
were the precursors to shamanism (Winkelman, 2011a,b, 2019b,
2021c). The prosocial and interpersonal effects of psychedelics
(see Table 2) likely supported the “collective effervescence” (sensu
Durkheim, 1995) and the sense of “communitas” (sensu
Turner, 1969) during our ancestors’ rituals, religious ceremonies,
Frontiers in Psychology | www.frontiersin.org 11 September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 12
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
and secular celebrations, thus aiding activities that allowed
individuals to reaffirm their common identity and their
connectedness within the social order. Recent work by Kettner
et al. (2021) lends support to this hypothesis, showing that
communitas – an intense sense of togetherness and shared
humanity – mediates enduring increases in psychological well-
being and social connectedness following psychedelic use in
ceremonial retreats.
Since pre-modern societies typically conceptualized
psychedelics as entheogens [i.e., as gateways to a spiritual
or religious experience and/or communication with the
spirit worlds (Winkelman and Hoffman, 2015)] that provide
sacred knowledge and power, they have to be understood as a
source of inspiration of primordial magico-religious impulses.
Importantly, controlled studies show that psychedelics reliably
produce mystical-type experiences involving self-loss and a sense
of awe and connectedness (Griffiths et al., 2006, 2011, 2018),
as well as a range of anomalous experiences (e.g., synaesthesia,
out-of-body and near-death experiences, entity encounters; see
Luke, 2020; also Strassman, 2001;Winkelman, 2018) that are
commonly interpreted as spiritual interactions in pre-modern
cultures. Psilocybin occasioned mystical experiences produce
enduring beneficial changes, such as trait-level increases in
prosocial attitudes and behaviors (Griffiths et al., 2018) and in
the personality domain of Openness (MacLean et al., 2011).
Moreover, both psychedelic mystical experiences and entity
encounters have profound and sometimes lasting effects on
beliefs and worldviews (Griffiths et al., 2011, 2019;Davis et al.,
2020;Lutkajtis, 2020).
Generally, in traditional smaller scale societies psychedelics
are employed in socially oriented settings including healing
rituals, rites of passage, initiation into secret societies and cults,
and multi-group gatherings (Dobkin de Ríos, 1984;Rätsch, 2005).
In these contexts, psychedelic use is carefully programmed and
orchestrated by the ritual specialists to produce experiences of a
confirmatory nature (Noorani and Alderson-Day, 2020), in the
sense that they reinforce a set of socially situated expectations
established before entering the altered state (e.g., that a cure
will be effected through shamanistic magical intervention, or
that initiatic contact with the ancestors will be achieved).
Cross-culturally, ritual specialists leverage collective, socially
bonding mythic narratives and coordinated, mixed modality
performances of entrained ritual or dance to provide structuring
during ego-dissolution and to evoke culturally expected visions
through expressive dimensions of ritual (Dobkin de Ríos, 1984;
Winkelman, 2002, 2015, 2021c;Rodríguez and Quirce, 2012).
Thus, for instance, among the Tukano from the Colombian
Amazon, psychedelic yagé (Banisteriopsis caapi +Diplopterys
cabrerana) is administered during the Yuruparí dance rites, an
ancestor ceremony for initiation of young men into adult male
society (Hugh-Jones, 1979;Jackson, 1983). This intense, self-
defining experience involves dancing that is interspersed with
periods during which tobacco, coca, manioc beer, and yagé are
consumed and myths are chanted in unison. During this ritual,
young boys are supposed to enter into controlled and voluntary
contact with the beginning and source of life, the (other-)world
of myth, in order to gain visionary knowledge by assuming the
identity of the He People or first ancestors (Reichel-Dolmatoff,
1971;Hugh-Jones, 1979).
Traditional enculturation rituals such as the one just described
involve a “socialization of hallucinations” that involves the
education of attention, the categorization of perceptions, and the
shaping of emotions and expectations (Dupuis, 2021). Crucially,
as argued by Dupuis (2021: 10), “Insofar as psychedelics are
able to produce perceptions whose phenomenological content
is strongly influenced by culture, their noetic property may
enhance the significance and attribution of the reality of
cultural worldviews as metaphysical, ontological, or supernatural
claims. . . these two properties make hallucinogenic substances
powerful potential vectors of cultural transmission.”
Current neuroscientific understanding of the effects of
psychedelics suggests they can potentially facilitate ritual
activities aimed at socialization and enculturation (such as rites
of passage and initiation cults). Brain action of psychedelics
involves a temporal dampening effect on activity and integrity
of the default-mode network (DMN) that decreases top-
down inhibition, liberating sensory and cognitive bottom-up
information flow, thereby increasing the richness of subjective
experience (Carhart-Harris et al., 2012, 2014;Carhart-Harris and
Friston, 2019). DMN roles in self and social cognition (Spreng
and Andrews-Hanna, 2015;Fingelkurts et al., 2020) are also
compromised, with an inhibition or reduction of personhood
and agency that leads to enhanced cognitive flexibility and
emotional lability (Carhart-Harris and Nutt, 2017;Carhart-
Harris and Friston, 2019). In this liminal state, suggestibility,
sensitivity to context, and imagery are all heightened (Carhart-
Harris et al., 2015, 2018b;Kometer and Vollenweider, 2016).
Moreover, this “pivotal mental state” (Brouwer and Carhart-
Harris, 2021) involves a generalized malleability, in the form of
enhanced synaptogenesis and neural plasticity (Ly et al., 2018),
as well as low-level learning and extinction learning (Carhart-
Harris and Nutt, 2017) that can further aid self-actualization
and self-editing. This destabilizing process is contained within
ritual to create new meaning, mediate identity formation, and
facilitate the programming of the individual into cult beliefs and
cultural patterns.
Enhanced Group Decision-Making
Hominins developed an egalitarian political system in which
interdependence and the availability of lethal weapons (e.g.,
wooden spears and lithic points) made possible group control
of leaders; consequently, group success came to depend greatly
on the ability of leaders to persuade (Gintis et al., 2015).
Undermining the ability of dominants to exploit others helped
our ancestors replace hierarchical social dominance with a
more equitable sociopolitical structure based on knowledge,
conflict resolution, generosity, and status leveling mechanisms
(Boehm, 1993). According to Gintis et al. (2015), the heightened
social value of nonauthoritarian leadership entailed enhanced
fitness for such leadership traits as the ability to form and
influence coalitions and intelligence. This emerging sociopolitical
system thus selected for increased cognitive and linguistic ability,
which enhanced prosocial leadership skills. In this context, non-
authoritarian, charismatic leaders such as shamans and other
Frontiers in Psychology | www.frontiersin.org 12 September 2021 | Volume 12 | Article 729425

fpsyg-12-729425 September 27, 2021 Time: 12:27 # 13
Rodríguez Arce and Winkelman Psychedelics, Sociality, and Human Evolution
leaders with supernatural abilities flourished, specializing in
palliating or preventing misfortune, providing prosocial services
based on knowledge and expertise related to ritual and medicinal
functions (Boyer, 2019;Garfield et al., 2020). This type of leaders
played an outsized role in numerous domains beyond healing,
particularly in group decision-making and problem-solving
contexts (e.g., conflict and intergroup mediation, guiding hunting
and group movement [Winkelman, 2010, 2013b, 2021a]).
Comparative ethnographic evidence reveals that one of the
main shamanistic uses of psychedelics is for divination, i.e., for
procuring otherwise unattainable information (Dobkin de Ríos,
1984;Schultes et al., 2001;Rätsch, 2005). Divination practices are
required for important collective decisions in many small-scale
societies (Boyer, 2020). Ingestion of a vision-inducing material is
a common method to gain privileged nonempirical knowledge
for decision-making (Sutton and Anderson, 2010). Psychedelic
supported divination is employed for purported communication
with ancestors or supernatural entities to solve diverse problems
and social quandaries, to diagnose and treat illnesses, to have
foreknowledge of the future, or to plan and organize subsistence-
related activities (e.g., making sure that a hunting expedition will
be successful) (Reichel-Dolmatoff, 1971;Dole, 1974;Myerhoff,
1974;Dobkin de Ríos, 1984;Furst, 1990;Ott, 1993). Therefore,
in smaller scale societies, psychedelic use is intimately linked
with strategizing and decision-making through its central role in
diagnostic, forecasting, and interventionist forms of divination.
Psychedelics can afford genuine epistemic benefits even if
there is no transcendent reality or all-knowing otherworldly
agents (Winkelman, 2013b;Letheby, 2019). Psychedelics can
offer new knowledge of old information, allowing appreciation
of already known (or otherwise knowable) facts in deep, vivid,
affectively and motivationally significant ways (Letheby, 2019).
These knowledge-gains seem to be supported by several related
psychedelic-enhanced mechanisms that include curious behavior,
explorative search, structure and fact-free learning, and insight
and perspective change (Carhart-Harris and Friston, 2019). Such
effects were likely useful for early humans under circumstances in
which immediate decisions had to be made and/or actions taken
promptly despite incomplete information. Our ancestors might
have been particularly drawn to the rapidly ensuing boost in
cognitive flexibility, imagination, and optimism, as well as to the
visual intensifications and complex imagery linked to intuitive
realizations that psychedelics can facilitate (see Table 3 for a
summary of behavioral and neuroimaging evidence of potentially
fitness-enhancing effects of psychedelics on cognition).
Psychedelics modulate aspects of creative thought, inducing
a hyper-associative, imagistic mode of thinking that operates
with little logical constraints and involves making connections
between relatively unrelated words and images (Girn et al.,
2020). Psychedelics thus augment semantic activation (Spitzer
et al., 1996;Family et al., 2016) and access to novel
mental representations (Baggott, 2015), spurring unconventional
associations and conceptual links that give rise to unusual
thoughts. In fact, naturalistic psilocybin use has been associated
with sub-acute enhancements in divergent thinking (Mason
et al., 2019) and creative problem-solving ability (Sweat
et al., 2016). Since reasoning about causally opaque events
TABLE 3 | Evidence for enhanced cognitive capacities during and after
psychedelic exposure.
Potentially
adaptive effect
Study Summary of results Total
number of
subjects
Enriched state of
consciousness
Lord et al.
(2019)
Psilocybin ↑the repertoire of
brain functional network states,
↑brain integration and neural
signal complexity
15 (5 females)
Enhanced
cognitive flexibility
Carhart-Harris
et al. (2016a)
LSD ↑cognitive flexibility and
optimism for up to 2 weeks
afterward
20 (4 females)
Heightened
creativity
Family et al.
(2016);
Sweat et al.
(2016);
Mason et al.
(2021)
LSD ↑indirect semantic
activation, facilitating retrieval of
distant associations
Naturalistic psychedelic use
associated with ↑creative
problem-solving ability
Acutely, psilocybin ↑ratings of
(spontaneous) creative insights
and ↓(deliberate) task-based
creativity. 7 days after
psilocybin, novel ideas ↑
10 (1 female)
68 (38
females)
60 (25
females)
Enhanced mental
imagery
de Araujo
et al. (2012)
Ayahuasca ↑the intensity of
recalled images to the same
level of natural image
10 (5 females)
Enhanced ability
to attribute
meaning/value
Studerus et al.
(2010)
Psilocybin alters the sense of
meaning in percepts, e.g.,
‘things around me had a new
strange meaning’
327 (140
females)
Enhanced
insightfulness and
self-awareness
Kometer et al.
(2015)
Psilocybin ↑retrieval and
reattribution of autobiographic
memories
50 (22
females)
All studies were performed with healthy volunteers.
↑, increased; ↓, decreased.
or outcomes – those lacking a known causal explanation – is
a pervasive feature of human cognition (Legare and Nielsen,
2020), it seems fitting that certain individuals (particularly
ritual leaders) in numerous cultures adopted psychedelics as
instruments for inspiration and envisioning, since they provide
a state of consciousness that can potentially facilitate creative
generation addressing knowledge gaps.
This psychedelic-induced ‘primary process thinking’
(Kraehenmann et al., 2017) involves an increased excitability
of the visual pathway (Kometer et al., 2013;Kometer and
Vollenweider, 2016;Timmermann et al., 2019) and engagement
of an intrinsic representational system also manifested in
phantasy, daydreaming, night-time dreaming, and mystical
visions (Horváth et al., 2017;Fox et al., 2018). This mode of
visual mentation that likely preceded our rational, language-
based consciousness supports information integration, decision
making processes through presentational symbolism (involving,
e.g., simulation of alternative mental scenarios), and learning
(Winkelman, 2010, 2017). For millions of years, this image-based
cognitive modality provided hominins with a meta-cognitive
system for representation of complex relations, problem-solving,
and strategic planning (Lohmar, 2010) despite it being less
analytically advanced than the (logical, rule-based, and reflective)
secondary process thinking (Carhart-Harris et al., 2014).
Frontiers in Psychology | www.frontiersin.org 13 September 2021 | Volume 12 | Article 729425