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The evolutionary bases of social and moral emotions:
Dominance, submission, and true love
Ross Buck
University of Connecticut
Storrs, CT USA
Keywords
Acknowledgements
Paper to be presented at the
9th Sydney Symposium of Social Psychology
The evolution of the social mind:
Evolutionary psychology and social cognition
14-16th March 2006
In the first edition of Human Motivation and Emotion (1976; 1988a), this author
pondered the question of whether human nature is good or evil: whether in the “state of
nature” people lived together peacefully without leaders as imagined by Rousseau and
John Locke; or whether they were aggressively engaged in a constant “war of all against
all” as argued by Thomas Hobbes. My answer, after considering studies of exploratory
behavior and conformity/obedience, was that the central facts of human nature are in fact
powerful drives of curiosity directed toward the achievement of competence, and a great
susceptibility to social influence: “human beings are passionate creatures who are
powerfully oriented toward distant goals and strongly influenced by their fellows. From
these qualities come much that is good in humanity, and much that is evil” (Buck, 1976,
p. 413). Thirty years on, it is perhaps appropriate to revisit this conclusion in light of the
enormous advances made in the interim in the literatures in evolutionary theory and
affective neuroscience. This paper considers the deep evolutionary roots of motivation,
emotion, and communication; with the goal of examining the essential natures of
cooperation and competition from the viewpoint of developmental-interactionist (DI)
theory (Buck, 1985; 1999). I first consider the definition and evolution of
communication, with particular attention to the “selfish gene” view and its apparent
implication that genuine prosociality—“true love”—is impossible at the biological level.
I counter that an alternative “communicative gene” view implies that a biologically-based
capacity for genuine prosociality is not only possible but indeed is required to explain
basic facts of the role of communication in evolution. I then summarize recent evidence
that prosocial motivational-emotional systems are in fact clearly present in the structures
and chemicals of the brain, and suggest that in human beings powerful attachment
systems underlie systems of higher-level social and moral emotions that emerge naturally
and effortlessly from interaction over the course of development.
Genes, Communication, and Prosociality
The Evolution of Communication.
Symbolic, spontaneous, and pseudospontaneous communication. “Communication”
is here defined following E. O. Wilson (1975) as occurring “whenever the behavior of
one individual (the sender) influences the behavior of another (the receiver)…behavior
can be defined as communicative to the extent that it reduces uncertainty in the behavior
of another” (Buck, 1984, p. 4). In DI theory, human communication proceeds in two
simultaneous “streams:” one voluntary and symbolic, the other automatic and
spontaneous (Buck, 1988b, 1989, 1994; Buck & VanLear, 2002). Voluntary symbolic
communication is learned and culturally patterned, its elements are symbols which bear
an arbitrary relationship to the referent (for example, the word “tree” in English is
arbitrarily related to the object it represents), and its content consists of falsifiable
statements or propositions. A sender voluntarily encodes information into symbols,
which are transmitted to a receiver who, assuming the receiver has learned the symbols
and their rules for combination (vocabulary and grammar), can decode the message and
thereby come to know the information. Both sender and receiver must have learned a
similar language in order for symbolic communication to be successful.
In contrast, spontaneous communication is biologically structured in both its sending
and receiving aspects. An internal motivational/emotional state of the sender is
automatically and effortlessly expressed in an evolved display, which given attention is
picked up by the receiver and “known” directly via evolved preattunement as a
motivational/emotional response in the receiver. The display is not a symbol, but rather is
a sign of the internal motivational/emotional state. A sign bears a natural relationship to
the referent—it is an externally accessible aspect of the referent, as in smoke being a sign
of fire—so that if the sign is present the referent must be present by definition. Therefore
symbolic communication is not propositional in that by definition it cannot be false.
These two simultaneous streams of communication coexist in virtually every human
communicative exchange, although their relative importance will vary. In formal and
structured situations, such as a lecture, symbolic communication tends to dominate but
spontaneous communication plays a subsidiary albeit important role in conveying for
example the charisma of the speaker and enthusiasm of the audience. This domination of
symbolic communication is often aided by the architecture of the lecture room, with the
speaker elevated and facing the audience, and the audience oriented toward the speaker.
In a less structured seminar, the role of spontaneous communication is enhanced, often in
part by a face-to-face orientation of the seminar participants. In the “throes of passion,”
spontaneous communication comes to predominate: symbolic and rational considerations
are set aside in favor of strong emotions: love, ecstasy, rage, misery, terror.
The symbolic-spontaneous mix also varies with the intimacy of personal relationship
of sender and receiver. All else equal, symbolic communication predominates in formal
relationships where the actors do not know one another well, but as personal relationships
develop and become more intimate, the relative importance of spontaneous
communication tends to increase. The symbolic-spontaneous mix also varies over the
course of human development: the newborn is primarily a spontaneous communicator,
but as an infant grows into a toddler and comes to learn language, symbolic
communication becomes more and more important (Buck, 1982). Finally, the symbolicspontaneous mix varies along the evolutionary scale: as species increase in complexity,
relatively inflexible spontaneous communication systems interact progressively more
extensively with general-purpose symbolic communication systems, so that
communication becomes progressively more flexible. This progressive evolution of
increased behavioral plasticity has been termed anagenesis (Gottleib, 1984).
There is evidence that the individual has considerable “voluntary” control over the
display, in that it is possible for a sender to show motivational and emotional displays
that are not really present as internal states. Arthur VanLear and I termed this
“pseudospontaneous communication,” because while it is voluntary from the sender’s
point of view, it uses the display mechanism that can stimulate preattunements in the
receiver, so if the receiver is taken in it is as if it were a veridical display. A charismatic
sender, for example, can successfully “push the buttons” of an audience, and persuade by
manipulating others’ emotions (Buck & Van Lear, 2002). This voluntary expression of a
display was termed “voluntary expression formation” in analyses of brain mechanisms of
primate audiovocal communication by Jurgens (1979) and Ploog (1981). The question of
veridical versus manipulative displays is a fundamental issue in the evolution of
communication, as we shall see.
Classical ethology: communication and group selection. The classical analysis of the
evolution of communication stems from Charles Darwin’s theory of evolution, and
particularly Expression of the Emotions in Man and Animals (1872/1998). Darwin
suggested that emotional displays can have adaptive value in social animals because they
reveal inner states of the responder that are useful for social co-ordination, including for
example aggressive dominance, fearful submissiveness, and sexual readiness. This
implies that the inner state of the responder (sender) must be associated with external
expression, and that the receiver must be able to “pick up” the expression via sensory
cues: postures, facial expressions, pheromones. Darwin's thesis requires that sending and
receiving mechanisms co-evolve—evolve simultaneously with one another—for the
adaptive value of a system of communication to be realized. This analysis reflects the
features of spontaneous communication as defined previously.
Ethologists including Lorenz and Tinbergen agreed that the communication of certain
motivational-emotional states is adaptive (Hauser, 1986). Those individuals who show
evidence of that state in behavior will tend to be favored. Over the generations these
behaviors can become “ritualized” into expressive displays. Similar reasoning was
applied to the evolution of receiving mechanisms: individuals who respond appropriately
to these displays would tend to be favored, so that the perceptual systems of species
members can become “preattuned” to the pickup of these displays. In this way, displays
and preattunements coevolve as aspects of a system of spontaneous communication.
Some of Darwin’s successors advanced the notion that behaviors, including
communicative behaviors, evolve as group-level adaptations (Kreft, 2004a). It seemed
intuitively logical that successful groups would foster qualities in group members that
would support and sustain that success. For example, Dobzhansky (1937) suggested that
species maintain genetic diversity to cope with environmental change; Allee (1951) held
that dominance hierarchies function to minimize within-group conflict; and WynneEdwards (1962) maintained that individuals restrain from breeding to avoid population
die-offs.
The “selfish-gene” critique of group selection. In the 1960’s, such group-level
thinking was criticized as naïve, illogical, and unscientific. G. C. Williams (1966) argued
that the selection of individual-level benefits is more immediate and effective than the
selection of group-level benefits, and that group-level selection should only be invoked if
individual-level benefits have been ruled out (Kreft, 2004a; Redfield, 2002). The
classical view was further challenged when selection was interpreted as operating, not at
the level of the individual or group, but rather at the level of the gene (Hauser, 1996). In
The Extended Phenotype (1982), Richard Dawkins derided what he termed “sloppily
unconscious group-selectionism” (p. 6). He argued that the ultimate unit of evolutionary
selection is the active, germ-line replicator. A replicator is “anything in the universe of
which copies are made,” an active replicator is “any replicator whose nature has some
influence over its probability of being copied,” and a germ-line replicator is a “replicator
that is potentially the ancestor of an indefinitely long succession of descendent
replicators” (1982, p. 83). Dawkins argued that the only active replicator lasting across
evolutionary timescales is the gene, so that the “selfish gene” is the unit of selection, a
replicator motivated only to make copies of itself. Fitness was seen as based upon the
survival, not of the individual organism or the group, but rather upon inclusive fitness: the
survival of the genes.
Dawkins noted that, for some purposes, it is convenient to think of the effects of
replicators as being packaged together in discrete “vehicles” such as individual organisms
or groups, but such vehicles are not units of selection because their influence does not
extend over evolutionary timescales: “to the extent that active germ-line replicators
benefit from the survival of bodies in which they sit, we may expect to see adaptations
that can be interpreted as for bodily survival…To the extent that active germ-line
replicators benefit from the survival of bodies other than those in which they sit, we may
expect to see ‘altruism,’ parental care, etc. …But all of these adaptations will exist,
fundamentally, through differential replicator survival” (Dawkins, 1982, pp. 84-85.
Italics in the original). All in all, the critique of the naïve appeal of group-level selection
was devastating, and effectively “outlawed group-level thinking” in evolutionary biology
(Kreft, 2004a, p. 267).
Selfishness and communication. The “selfish gene” critique extended to the
understanding of communication as well, and specifically to the idea that accurate
communication is adaptive. Instead, it was argued that selection would actually operate
against those who show veridical displays that are predictive of their true inner states and
probable behaviors, and suggested that communication is actually a means by which one
animal exploits another: “a means by which one animal (the 'actor') exploits another
animal's (the 'reactor's') muscle power” (Krebs and Dawkins, 1984, pp. 380-381). Krebs
and Dawkins argued that displays evolve via selection for effective manipulation, defined
as the sender “actively changing the victim's (sic) behavior” (1984, p. 383).1 In this
regard, Dawkins and Krebs (1978) suggested an analogy between animal communication
and media advertising, where the object is persuasion rather than transfer of information.
This manipulative communication corresponds to pseudospontaneous communication as
defined previously, where the display does not in fact truly reflect an internal state but
rather is “put on” voluntarily by the sender, but it can activate the preattunements in the
receiver and therefore be emotionally compelling.
Krebs and Dawkins (1984) suggested that mind-reading on the part of the receiver-interpreting the actual internal state and predicting the behaviors of other animals--is the
counterpart to manipulation on the part of the sender. The sender's counter-response to
mind-reading may involve concealment (a poker-face) and active deception (simulating,
qualifying or falsifying one's display). The authors presented manipulation and mindreading as “intimately locked together in evolutionary arms races and feedback
loops…Mind-reading and manipulation coevolve, and signals are the result of this
coevolution” (Krebs and Dawkins, 1984, p. 389).
Multilevel selection theory. Sober and D. S. Wilson (1998; D. S. Wilson & Sober,
1994) suggested an alternative to the selfish gene position based upon the definition of
the unit of evolutionary selection. They suggested that evolution can take place at
multiple levels, including the gene, the individual organism, and the group. However, this
view was criticized by Dawkins (1994) because individuals and groups do not exist
across evolutionary timescales. He argued that individuals and groups are vehicles of
selection that are "not something fundamental" in evolution (Dawkins, 1994, p. 617), and
that although group selection is possible theoretically, it is not important in nature.
I use the terms "sender" and "receiver" in place of Krebs and Dawkins' (1984) "actor"
and "reactor."
1
Altruism.
Kin selection and reciprocal altruism. Altruism is defined as the sacrifice of one’s
own genetic fitness in favor of benefiting the genetic fitness of another. The phenomenon
of altruism poses a fundamental problem for evolutionary theory. Dawkins (1989) argued
that the “law of ruthless selfishness” governing the selection of genes implies that true
altruism is impossible: “Be warned that if you wish, as I do, to build a society in which
individuals cooperate generously and unselfishly towards a common good, you can
expect little help from biological nature. I am not advocating morality based on
evolution. Let us try to teach generosity and altruism, because we are born selfish (p. 3).”
Despite this, there are apparent examples of unselfish, cooperative, and even altruistic
behavior that must be taken into account. It is widely agreed that, under conditions of
kinship and/or reciprocity, mutually cooperative communication can foster the inclusive
fitness of the altruist, and therefore it can be favored by selection. In kin selection, one
helps genetically-related others, therefore indirectly preserving the genes shared with the
relative (Hamilton, 1963; 1964). In reciprocal altruism, one helps with expectation of
return (Trivers, 1971). Because such behavior fosters the survival of the altruist’s own
genes via inclusive fitness, such apparent altruism is actually selfish, and as such it does
not contradict the selfish gene hypothesis (Krebs and Dawkins, 1984). Evidence that
human beings sometimes appear to engage in altruistic behaviors despite considerations
of kinship and reciprocity being apparently absent has been answered by the argument
that humans are special because, as Dawkins noted, generosity and altruism can be
learned. For example, Rachlin (2002XX) argued that apparent altruism can be a
consequence of a learned commitment to an altruistic pattern of behavior.2 Such learning
must necessarily go against the naturally selfish tendencies of “biological nature.”
Quorum-sensing in bacteria. Recently, evidence relevant to the evolution of altruism
has come from an unexpected source: microbiology. In Animal Aggregations (1931), W.
C. Allee noted self-organizing activity in simple creatures, including bacteria. Bacteria
are prokaryotes—essentially bags of DNA—that lack the nuclei, mitochondria, and
organelles associated with the eukaryotic cells that make up all complex multicelled life.
Despite their relative simplicity, recent studies have discovered surprising complexity
and sophistication in the behavior of bacteria, including intra- and intercellular
communication resulting in behavior suggestive of intelligence and memory
(Hellingwerf, 2005), cooperation and altruism (Griffin, West, & Buckling, 2004; Kreft,
2004a, 2004b), and even “social intelligence” (Ben-Jacob, Becker, Shapira, and Levine,
2004). In addition, there is evidence that prokaryotes lived socially from the beginning.
The most ancient known organisms on Earth are fossilized colonies of cyanobacteria
termed stromatolites: stromatolites were abundant 3.5 billion years ago and exist today
living in suitable environments in Australia and Baja California (Olson, 1989). Today,
2
It is noteworthy that in his Behavioral and Brain Sciences paper "Altruism and
selfishness," Howard Rachlin used the word "choice" 80 times, while "emotion" did not
appear. In contrast, a paper in the same journal, "Empathy: Its ultimate and proximate
bases" by Stephanie D. Preston and Franz B. M. de Waal (2001), used "emotion" 139
times and "choice" once. Clearly, these articles represent fundamentally different ways of
looking at the phenomena of empathy and altruism, and each does not address the
positions of the other (Buck, 2002).
cyanobacteria are responsible for the pond scum that forms on stagnant water. In
stromatolites, these ancient, relatively uncomplicated creatures self-organize and selfconfigure to create a working community that recovers from damage, using systems of
communication that are not well understood.
Recent studies have elucidated mechanisms by which such bacterial social behavior is
coordinated. Many if not most species of bacteria exhibit quorum-sensing: mechanisms
for recruiting the mass production of molecules or engaging in other collective activities
beneficial to the bacteria. The bacteria are quiescent until a critical mass of individuals—
a “quorum” of millions or billions—has assembled, and they then produce the molecule
en mass in a useful concentration (Swift et al., 1996; Waters & Bassler, 2005).
It was thought until recently that quorum sensing was restricted to relatively few
species of bacteria, and served restricted functions. One well-described example is the
marine bioluminescent bacterium Vibrio fischeri. This bacterium lives freely in a
planktonic state, and also exists in symbiotic relationship with certain fish and squid (i.e.,
the Hawaiian squid Euprymna scolopes), causing luminescence that functions to attract
food and camouflage the squid in moonlight (Waters & Bassler, 2005). In the laboratory,
a growing colony of V. fischeri remains dark until a relatively high density of individuals
is achieved, at which point luminescence increases rapidly. This phenomenon is caused
by the action of signal molecules, which increase in concentration with an increasing
number of individuals. The signal molecule responsible for the activation of
luminescence in V. fischeri was identified in 1981, and the genetic system analyzed in
1983 (Eberhard et al., 1981; Engebrecht, Nealson, & Silverman, 1983). When the level of
signal molecules reaches a threshold, they enable proteins called LuxR to bind to specific
genes within the individual cells. A molecular apparatus “turned on” by the interaction
of LuxR and genes generates the light simultaneously in many individual bacteria
(Fuqua, Winans, & Greenberg, 1996; Greenberg, 1997; Schaefer et al., 1996; Waters &
Bassler, 2005).
One of the general problems of a system that works by cooperation is the presence of
cheaters who attempt to cash in on the benefits of the system without doing their part
(Travisano & Velicer, 2004). In the symbiotic relationship between V. fischeri and E.
scolopes, the bacteria receive rich nutrients that allow proliferation in exchange for the
benefit of giving light at the appropriate time to camouflage the squid. There are
individual bacteria, however, that potentially could bask in the benefits of the hospitality
of E. scolopes without incurring the metabolic costs of actually lighting up. If that
strategy were to succeed, the lights would soon go out. As it is, V. fischeri mutants who
are incapable of luminescence are outcompeted by their luminescent cousins in the squid
host: E. scolopes appears to possess a “policing” mechanism that distinguishes cells
incapable of luminescence and acts to eliminate cheaters (Waters & Bassler, 2005;
Visick, Foster, Doino, McFall-Nagai, & Ruby, 2000).
Interest in quorum-sensing within microbiology has exploded in the past decade: “the
number of known regulatory systems and the diversity of phenomena regulated are
growing dramatically, and it now appears that most bacteria possess at least one quorumsensing system” (Redfield, 2002, p. 365). While the functions of these systems are
extraordinarily diverse, the systems by which quorum-sensing is based are surprisingly
uniform. Quorum-sensing works by a bacterium’s release of an autoinducer molecule
into the environment. These constitute signals or displays, and typically involve amino
acids or peptides functioning as pheromones (Gallio, Sturgill, Rather, & Kylsten, 2002).
The bacterium also has the capacity to sense the concentration of this autoinducer in the
environment. If the concentration exceeds a threshold, the expression of genes within the
bacterium is altered, producing a variety of effects: motility, swarming, pigment
formation, etc. (Redfield, 2002). For example, quorum sensing is involved in some
bacterial infections, such that when a quorum is attained, the regulation of bacterial genes
is changed so that toxic “virulence factors” are produced. In cystic fibrosis, bacteria
produce a “biofilm” when they reach a certain concentration, a tough shell that protects
the bacteria from attack from the immune system of the victim and/or antibiotics. The
bacteria then can reproduce, produce toxins, and damage tissues in relative safety (Riedel
& Ebert, 2002). Biofilms have been characterized as “microbial societies with their own
defense and communication systems” (Costerton, Stewart, & Greenberg, 1999, p. 1322).
One feature of quorum sensing is that the bacteria may be quiescent—not activating a full
immune system response—until their number is sufficient to overwhelm the victim.3
Altruism and quorum-sensing. The production by a bacterium of an autoinducer, and
its responsiveness to the environmental concentration of the autoinducer, has all of the
qualities of spontaneous communication as defined previously. Both the display
(autoinducer production) and preattunement (responsiveness) are biologically-based, the
autoinducer is a sign of the referent (concentration of individuals), and the
communication is in no way intentional and is nonpropositional. The question whether
quorum-sensing in fact represents a system of communication to promote collective
action useful to the group is relevant to the question of cooperation and altruism in
evolutionary biology. In everyday language, altruism is typically related to a concern for
the welfare of others and the common good. In the context of evolutionary theory, these
are not considered: “Evolutionary altruism…does not require memory of past
interactions, recognition of individuals, sophisticated interactions or behavioral
repertoires, or direct interactions between individuals. It is therefore the simplest form of
altruism” (Kreft, 2004b, p. 2751).
In quorum-sensing, the concentration of autoinducer ordinarily exceeds threshold
only when the population of cells reaches a certain density, and the most widespread
interpretation of the quorum-sensing phenomenon is that it functions to sense population
density. Redfield (2002) has suggested that this interpretation of quorum-sensing is
incorrect for reasons that echo the selfish gene critique of group-level selection: “the
difficulty of maintaining genes for cooperative strategies in genetically mixed
populations makes this a notoriously weak and controversial mode of selection… (p.
365).” Furthermore, “those explanations that mesh well with our preconceptions are
often uncritically accepted while those that do not are scorned…perhaps because we are
social animals, we find the idea that bacteria have evolved communication and
The mechanism of quorum sensing is of great interest. If therapeutic agents can disrupt
bacterial communication, the virulence of the bacteria can be greatly reduced (Costerton,
et al., 1999; Foster, 2005). Moreover, because such treatments would target the
mechanism of communication—in effect disrupting the dyad-level communicative
relationship between bacteria rather than the bacteria as individuals—it would be less
likely to leave drug-resistant individuals behind to reproduce and eventually create strains
of drug-resistant bacteria (Buck & Ginsburg, 1991).
3
cooperation very appealing” (Redfield, 2002, p. 369). Redfield suggests that quorumsensing is actually a side effect of diffusion sensing: the ability to detect whether secreted
molecules move away from the cell.
Despite these objections, there is concrete evidence of individual sacrifice for group
benefit in microorganisms (Walters and Bassler, 2005). One example involves the slime
mold Dictyostelium discoideum. At one stage in its life cycle, slime molds exist as
unicellular amoebae feeding on bacteria. At this stage the amoebae exhibit positive
chemotaxis (attraction) vis a vis their prey and negative chemotaxis (repulsion) vis a vis
one another.4 The attractant is folic acid, an essential vitamin that the amoebae obtain
from ingesting bacteria. At the same time, the amoebae release an unidentified substance
that keeps other amoebae of the same species away: functioning to "aid dispersion of the
amoebae and therefore permit better utilization of the environment" (Lackie, 1986, p.
234). Thus this simple organism demonstrates a sort of "threat display" that may fulfill
functions analogous to those ascribed to territorial displays in more complex creatures
(Eibl-Eibesfeldt, 1975).
As bacteria in the environment are consumed, the amoebae begin to starve, the
negative chemotaxis to other amoebae ceases, and a positive chemotaxis begins. Within
4-6 hours, the individual amoebae begin to move toward aggregation centers, which
apparently contain those individuals whose positive chemotaxic systems were first
"turned on" by starvation. The chemical attractant responsible for aggregation is cyclic
adenosine monophosphate (cAMP), to which individual amoebae respond by themselves
releasing cAMP, thereby relaying the signal (Lackie, 1986). The initial phase involves
individual movement toward the center based upon perception of the dynamic gradient of
cAMP (interestingly, the amoebae do not respond to a static gradient of cAMP: Vicker,
Schill & Drescher, 1984). This phase is followed by a phase of streaming based upon
"nose to tail" contact following, facilitated by specialized contact sites which appear as
adhesion molecules now defining the front and rear of the individual amoebae (Gerisch et
al, 1975; 1980). It is noteworthy that competition between aggregation centers occurs,
based in part upon gradient interactions and in part apparently upon "dominance" by
older, more established, aggregation centers; although the mechanism of the latter is
unknown. It is also significant that, if mixed experimentally, individual amoebae of
different species aggregate independently (Lackie, 1986).
The aggregation center next forms a multi-celled slug, or grex, in which the cells are
derived from individual amoebae. The grex moves in a looping motion like an inchworm caterpillar. The size of the grex in D. discoideum ranges from 100,000 to 200,000
individual cells, so it must solve significant problems of coordination: as Lackie put it
"100,000 dissenting voices are scarcely a recipe for united action" (1986, p. 239). In fact,
the grex demonstrates coordinated responses to light, temperature, humidity, and oxygen.
The mechanism of coordination is not well understood, although gradients of cAMP
within the grex are involved, and lateral adhesions between individuals in addition to the
nose-to-tail joining may confer some mechanical coordination.
The grex moves from the domain of the individual amoebae in damp forest litter,
which is inappropriate for dispersal, up surface layers toward the light in a journey that
4
Chemotaxis is "the directed movement of a cell (or organism) in response to a chemical
substance in the environment" (Lackie, 1986, p. 220).
may take many days. The sensory analysis of the environment presumably takes place in
the front tip of the grex, and it is the cells in this area that become anchored and
"altruistically" die to form the cellulose stalk of a fruiting body (Strassmann, Zhu, &
Queller, 2000). The stalk formation is altruistic on the part of these individuals in the
technical evolutionary sense: they "surrender...personal genetic fitness for the
enhancement of personal genetic fitness in others" (E. O. Wilson, 1975, p. 106), or
behave "to increase another such entity's welfare at the expense of its own" (Dawkins,
1976, p. 4). Cells at the rear of the grex form a mass that climbs to the top of the stalk to
become individual spores, which are released into the environment. Given favorable
conditions, they germinate into individual amoebae, and begin the life cycle again.
In D. discoideum, the development of fruiting bodies is initiated by cAMP and
Differentiation-Inducing Factor (Town, Gross, & Kay, 1976; Town and Stanford, 1979).
In the soil-dwelling bacterium Myxococcus xanthus, a similar process involves quorum
sensing (Clarke, 1981; Losick & Kaiser, 1997; Shimkets, 1999). In both cases, “spore
development requires a large percentage of the population to undergo a lethal
differentiation event that leads to structures whose function is to promote spore
generation and dispersion” (Waters & Bassler, 2005, p. 336). These indeed appear to be
examples of altruism—in the technical evolutionary sense—at the microbial level: how
can this be reconciled with the powerful and compelling gene-selectionist account of
evolution?
The Communicative Gene Hypothesis.
Communication and the unit of selection. The issue of the possibility of "true"
altruism turns on the issue of the unit of selection: whether the unit of selection is the
individual gene as "selfish gene" proponents propose, or whether evolution can involve
the selection of units above the level of the individual gene. A possible solution is that
communicative relationships between genes can be replicators; units of selection in
evolution (Buck, 2002; Buck & Ginsburg, 1991; 1997a; 2000).
It is possible to retain a gene-selectionist position without a largely unexamined
accompanying assumption of genetic atomism: genes are selected in isolation from other
genes: "selection purely at the level of the individual gene" (Dawkins, 1989, pp. 84-85).
Buck & Ginsburg (1991) noted that genes do not function alone. Rather, genes function
in company with other genes, and more specifically, genes function by communicating
with other genes. This is not a controversial contention, but its implications regarding the
unit of selection have perhaps not been fully appreciated.
The genes that underlie a trait constitute the genotype, while the phenotype is the
expression of that trait in the qualities and behaviors of the individual organism that are
actually selected in the course of evolution. Genes are selected by proxy, via the
selection of the phenotype. In the case of communication, the phenotype subject to
selection is functional communication accuracy, the accuracy of gene A sending and gene
B receiving (Ca  b). If individuals who communicate effectively have a greater chance
of survival, the sending accuracy of gene A to gene B and the receiving ability of gene B
from gene A will be selected simultaneously. So, genes associated with a sending
mechanism (for example controlling a bacterium’s release of an autoinducer molecule)
and a receiving mechanism (controlling the capacity to sense the concentration of this
autoinducer) must co-evolve. This is not “selection at the level of the individual gene,”
but rather it is selection at the level of the communicative relationship of genes A and B,
and the result is the display-preattunement relationship characteristic of spontaneous
communication.
The elements of communication. A critical postulate of the communicative gene
view is that in any system of interacting elements, communication involves both
individual elements and the unique relationship between those elements relative to other
elements. Thus, Ca  b accuracy depends in part on the individual abilities of gene A to
send (Sa) and gene B to receive (Rb), but it also depends in part upon the unique ability
of gene A to send to gene B relative to other genes (Ua  b). Similarly, the reciprocal
ability of gene B to send to gene A depends in part on the ability of gene B to send (Sb)
and gene A to receive (Ra), and in part to the unique ability of gene B to send to gene A
relative to other genes (Ub  a).
This breakdown of communication into sending effects, receiving effects, and unique
relationship effects is a feature of the Social relations Model (SRM: Warner, Kenny, &
Stoto, 19XX; Kenny, 1994). This defines the following as making up communication
between genes A and B:
1. Ca  b = (Sa + Rb + [Ua  b] + error)
2. Cb  a = (Sb + Ra + [Ub  a] + error)
These terms can be measured or estimated via round-robin designs in which
communication between A and B are assessed in company with their communication vis a
vis other elements (e.g., C, D, E, etc.). The SRM allows the analysis of the proportion of
variance in total communication accuracy due to individual sending and receiving
accuracies, and that due to the unique relationship between the individual elements plus
error, which can be estimated in designs incorporating repeated measures.
To recapitulate, communication accuracy (Ca  b) is the phenotype, the trait selected
by evolution. The SRM shows that Ca  b reflects not only the individual sending
accuracy of A and receiving ability of B, but the unique relationship of A and B as well.
This unique relationship (Ua  b) is an aspect of the genotype which is selected by proxy
via the selection of the phenotype Ca  b. Studies using the SRM have consistently
found that a substantial portion of variance if communication accuracy—up to 50% or
more—is due to the unique relationship between individuals as opposed to individual
sending and receiving abilities (Sabatelli, Buck & Kenny, 1986, Kenny, 1994).
Although the SRM was developed in the context of social psychology, the point
regarding communication—that both individual and dyad-level components make up
observed communication accuracy—is general, applying to any system of
communicating elements including genes. It is possible in principle to measure the
interaction between specific genes using the equivalent of a round-robin design: that is,
controlling for their interactions with other genes, and therefore assessing unique
relationship effects.
Implications for altruism: Relationships as replicators. This analysis suggests that the
genotype (the replicator) includes potentially measurable relationship factors; that
communicative relationships can be replicators in Dawkins’s (1982) sense.
Communicative relationships arguably meet the criteria for being active germ-line
replicators. A replicator is anything of which copies are made; an active replicator
influences the probability of being copied; a germ-line replicator is an ancestor of
descendant replicators; and replicators exist across evolutionary time scales.
Communicative relationships (Ua  b) and (Ub  a) can be copied via the selection of
the phenotype Ca  b and Cb  a; the nature of (Ua  b) and (Ub  a) can influence
the probability of being copied; and these relationships can exist across evolutionary
timescales. Therefore, communicative relationships between genes can be active, germline replicators. Moreover, communicating genes are not necessarily within the same cell
or organism. The quorum-seeking example demonstrates that genes in different
individual bacteria can communicate via autoinducer molecules functioning as signs of
population density: it involves displays in the sender and preattunements in the receiver.
There are many examples of specific communicative relationships that have existed
across evolutionary timescales: indeed the ritualized displays associated the classical
ethological view meet this criterion. Specific displays associated with dominance,
submission, warning, courting, and bonding have existed across evolutionary timescales
and in many species: for example, Livingstone, Harris-Warrick, and Kravitz (1980)
demonstrated that serotonin injections in crayfish and lobsters produce characteristic
dominance postures, while injections of octopamine (the phenol analogue of
norepinephrine) produce subordinate postures, and the mating pheromone in the singlecelled yeast Saccharomyces cerevisiae is a peptide molecule that closely resembles
GnRH involved in mating in mammals, including human beings (Loumaye, Thorner, &
Catt, 1982). Both of these imply a conservation of sending and receiving mechanisms
functioning across an enormous span of time.
As noted, there is always the potential for cheaters to exploit a cooperative
relationship, and the active mechanisms to respond to cheaters even in microbial life
noted previously demonstrates that cooperation is never a simple matter. But, although
manipulative communication clearly can be of selfish benefit, it does not follow that all
communication is manipulative: veridical communication must also exist, and indeed, the
presence of lying itself implies an underlying truth. Winston Churchill said in 1944:
“truth is so precious that she should always be attended by a bodyguard of lies”
(REFXX). This statement expresses a fundamental truth about truth and lying, but if there
were not in fact an underlying truth the lie would not be necessary: a bodyguard of lies is
pointless without a body to guard, as it were.
Summary and Implications
In summary, the communicative gene hypothesis makes allowance for biologicallybased cooperative tendencies as well as selfish tendencies, suggesting that built-in
tendencies for genuine altruism, self-sacrifice, attachment, and “true love” can be
products of evolution alongside selfishness and calculations of self-interest. Indeed, when
the nature of communication is taken into account, a gene-selectionist viewpoint arguably
not only allows, but requires, true altruism. This conclusion is supported when we
examine the motivational-emotional systems actually present in the brain. Largely
separate from the debate about the selfish gene position and its implications for altruism,
evidence has been accumulating in the neurosciences for the existence of powerful
prosocial biological emotions (Buck, 1999, 2002). The existence of these prosocial
neurochemical systems seems contrary to the notion that altruism is impossible at the
biological level, and must be learned.
It is noteworthy in this regard that Darwin himself did not deny the possibility of
biologically-based prosocial motives and emotions. Indeed, he argued that compassion
and moral sensitivity—”social instincts and sympathies”—are critical to the social order.
He wrote, “the emotion of love…is one of the strongest of which the mind is capable”
(1872/1998, p. 212).
Prosocial Biological Emotions
Oxytocin and Vasopressin
Most emotions examined by contemporary emotion theories involve selfish and
individualistic concerns: the “primary affects” of Tomkins, Izard, and Ekman and Friesen
(e.g., happiness, sadness, fear, anger, surprise, disgust) all promote the adaptation of the
individual. However, approaches that analyze brain mechanisms of emotion have found
powerful evidence of neurochemical systems that appear to underlie prosocial emotions
(Buck, 1999; 2002; Buck & Renfro, 2006). Based upon early studies of the effects of
brain stimulation, Paul D. MacLean, Detlev Ploog, and others argued that while some
emotions are inherently selfish, directed toward the survival of the individual organism;
others are inherently social, directed at the survival of the species (MacLean, 1993;
Ploog, 1981).
More recently, specific central neurochemical systems have been identified that are
strongly associated with prosocial attachment: social recognition, mating, parental
nurturance, bonding, and play. These systems involve a variety of specific
neurochemicals, including the peptide neurohormones oxytocin (OXY) and vasopressin
(VP). OXY and VP derived from an evolutionary divergence of an ancestral hormone,
vasotocin, that facilitates sociosexual responses in reptiles and birds (Moore, 1987).
Recent evidence suggests that OXY and VP have special roles in social behavior,
particularly nurturance and protective/territorial behavior. The following paragraphs
summarize recent evidence implicating OXY and VP in prosocial behavior.
Prosociality in voles: The neurochemistry of monogamy and polygamy. An area of
research that has produced some of the most remarkable findings involves voles: mousesize rodents of the genus Microtus which exhibit both monogamous and polygamous
lifestyles (Wang & Aragona, 2004). Monogamous prairie voles (Microtus ochrogaster)
show lasting pair bonds that are activated by mating. When a female is exposed to a
chemical in the urine of an unrelated male, she becomes sexually receptive, they mate
repeatedly, and soon become parents. Bonded prairie voles live together in a common
nest, snuggling side-by-side over 50% of the time. Either female or male will defend
their territory by responding aggressively toward intruding voles. Both female and male
care for their pups, with the male helping to build the nest and spending almost as much
time with the young as the female; and if separated the pups become agitated and display
ultrasonic distress calls and stress as evidenced by increases in cortisol. If the bonded
partner dies, a surviving prairie vole will typically live alone rather than take a new mate.
In contrast, the closely related meadow vole (Microtus pennsylvanicus) and montane vole
(Microtus montanus) show none of the signs of strong social bonding displayed by the
prairie vole. They are non-monogamous, nest independently, and breed promiscuously.
The males play no parenting role, even the females abandon their pups soon after birth,
and the pups do not appear to be distressed by abandonment (Carter, Lederhendler, &
Kirkpatrick, 1997; Insel & Young, 2001). Insel (2002XX) has discussed this evidence in
terms of a neurobiological basis for altruistic love, and implications for human altruism.
Oxytocin and VP are both critical to the social bonding of the prairie vole. Brain areas
associated with OXY are larger in the prairie vole than the montane vole (Insel, Young,
& Wang, 1997). In natural settings, mating is associated with OXY release, which
apparently functions to cement partner preferences in the female, so that she prefers the
male she is with when OXY increase occurred (Carter, 1996). Experiments show that
OXY is both necessary and sufficient for the development of pair bonds in the female: an
unbonded female exposed to an unrelated male and OXY together will become bonded
without mating, while an OXY antagonist will block bonding despite mating (Williams,
Insel, Harbaugh & Carter, 1994).
Similarly, VP is necessary and sufficient for bonding in the male prairie vole: VP
stimulates the formation of a partner preference even without mating, and VP antagonists
prevent the formation of partner preferences even after extensive mating (Insel & Young,
2001). The distribution of VP receptors in the brains of monogamous and polygamous
males is different, with the prairie vole having a higher density of VP receptors (termed
V1aRs) in the ventral forebrain in an area associated with dopamine-mediated reward
(Lim et al., 2004; Young, Lim, Gingrich, & Insel, 2001). Incredibly, the polygamous
meadow vole male can be made to act like a monogamous prairie vole male by the
alteration of a single gene: V1aR gene transfer, increasing VP receptors in the ventral
forebrain of male meadow voles, substantially increased partner preference formation,
indicating that “changes in the regional expression of a single gene can have a profound
effect on the social behaviour of individuals within a species” (Lim et al. 2004, p. 756).
The authors suggested that this has the effect of increasing the social memory of the
partner’s olfactory signature, and associating it with dopamine-mediated reward:
“monogamous social organization might be the result of the insertion of the V1aR system
into the ancient pre-existing reward circuit” (p. 756).
Social recognition in mice. There is also evidence that prosocial neurochemical
systems are involved in social behaviors in mice. OXY knock-out (OTKO) mice, bred
without the genes to produce OXY, show profound deficits in social behavior (Young,
2001XX; 2002XX). As pups, OTKO mice are less distressed by social isolation, and they
show no preference for their mothers compared to the strong preference shown by normal
mice. As adults, OTKO mice demonstrate “social amnesia” in that they do not show
evidence of learning to recognize other mice. This is reversed by a single injection of
OXY into the brain prior to, but not after, exposure to another mouse. Young (2001XX)
noted parallels between social deficits in OTKO mice and autism in humans: autism is
characterized by profound social impairments, including deficits in social engagement
and abnormal brain processing of social stimuli, and autistic children may have low
concentrations of OXY in the blood.
Deprivation studies in monkeys and human beings. Although prosocial behavior is
associated with specific neurochemical systems in the brain, early experience in social
relationships appears to be critical for social attachment to develop normally. In Harry
Harlow’s famous research, isolation for the first year of life rhesus monkeys was
associated with serious socio-emotional deficits in adulthood (Harlow, 1971), and
isolated animals manifested deficits in emotional communication as well (Miller, Caul,
and Mirsky, 1967). These deficits are thought to be due to a lack of social experience at
sensitive periods during development. In rhesus monkeys, strong attachment motives and
emotions are present from birth, fearful and angry emotions develop after the first six
months of age, and sexual emotions develop later at puberty. Harlow suggested that in
the first three months, a Maternal (or Parental) Affectional System lays the
socioemotional groundwork for the infant monkey’s emotional life, affording a basic
sense of trust in other monkeys; after six months, a Peer Affectional System allows the
youngster to deal with and communicate fearful and angry emotions in the context of
rough and tumble play; and these communication abilities are crucial in the last,
Heterosexual Affectional System after the sexual systems come on line. Harlow (1971)
suggested that these periods are analogous to infancy, childhood, and adolescence in
human beings, and that if experience in earlier stages is lacking, it can have devastating
effects on later social and emotional functioning.
Tragically, research with children who were institutionalized as infants in Eastern
Europe have shown later socioemotional and emotional communication deficits that on
the surface appear similar to those demonstrated in Harlow’s and Miller et al’s research
(Pollak, Klorman, Thatcher, & Chicetti, 2001; Wismer Fries & Pollak, 2004). Recent
evidence suggests that these children also show deficits in the OXY and VP systems
(Wismer Fries, Ziegler, Kurian, Jacoris, & Pollak, 2005). These authors conclude that
their results “suggest a potential mechanism whose atypical function may explain the
pervasive social and emotional difficulties observed in many children who have
experienced aberrant care-giving…consistent with the view that there is a critical role for
early experience in the development of brain systems underlying basic aspects of human
social behavior” (p. 17237).
The neurochemistry of trust. There is evidence that prosocial neurochemical systems
my even be involved in the complex social deliberations associated with trust in human
beings. Cooperation and competition have been studied in social dilemmas such as the
Prisoner’s Dilemma (PD) game for decades. This research shows that participants often
choose to cooperate, even where the payoffs in the situation would appear to encourage
competition. It is noteworthy that one of the most powerful factors predicting
cooperation is communication before the game (Sally, 1995). For example, Frank,
Gilovich, and Regan (1993) allowed participants to interact prior to playing in a PD, and
were allowed to converse about anything except the game. Cooperation was higher
overall with communication was permitted, but interestingly the players seemed to
accurately feel each other out: the dyads locked into either mutual cooperation or mutual
defection, with relatively few cases of one partner taking advantage of the other. The
intention to cooperate or defect was apparently communicated prior to play. Boone and
Buck (2003) suggested that emotional expressivity acts as a marker for trustworthiness,
and allows trust or suspicion to be displayed nonverbally; and Rauh, Polonsky, and Buck
(2004) found friendly emotional expressiveness and suspiciousness to predict a
participant’s cooperative or competitive first move, respectively, in a PD game.
Recent evidence suggests that OXY may play a role in cooperation in human beings.
Kosfeld et al. (2005) found that OXY presented in an aerosol increased cooperative
behavior, and Wood et al (2005) found that disruption of serotonin functioning increases
competitive behavior in PD games. Thus, remarkably, molecules relevant to attachment
mechanisms can have significant effects upon complex human behavior. It thus appears
that primordial affective motivational-emotional systems can influence complex choices
in human beings involving cooperation and competition.
Other Prosocial Neurochemical Systems
Although evidence for the prosocial functions of OXY and VP is particularly
impressive, other neurochemical systems have prosocial functions as well (See Buck,
1999; Panksepp, 1998 for reviews). These include the endogenous opiates or endorphins,
which Panksepp and colleagues have associated with playful behavior in rats (Panksepp
& Burgdorf, 1999; 2000). Burgdorf and Panksepp (2001) suggest that the positively
reinforcing effects of play are modulated by the endorphins, fitting with evidence of the
role of endorphins in mediating social reward (Panksepp, 1991). Also, gonadotropinreleasing hormone (GnRH) increases sexual proclivities and has rewarding effects as
demonstrated by its ability to establish conditioned place preferences in male rats: these
preferences, however, are absent in gonadectomized animals (deBeun et al., 1991).
Panksepp (1993) has suggested that GnRH “may well prove to be a prime mover in
human libido” (p. 94).
Attachment and Higher-Level Social and Moral Emotions
I have argued that cooperative as well as competitive tendencies have been built-into
the genome from the beginning, and that specific neurochemical systems in the brain are
associated with powerful prosocial motives and emotions. These powerful prosocial
emotions are hiding in plain sight: while they are involved in motivating much of the
behavior of interest to social psychology, they tend to be taken for granted and their
importance is rarely recognized. Just as effectance motives and needs for understanding
underlie tendencies toward cognitive consistency, attribution processes, and attitude
formation and change; attachment motives and needs to be loved underlie tendencies
toward social referencing, modeling and imitation, conformity, and obedience (Buck,
1998). They are involved in every human action and interaction.
Defining Motivation and Emotion
Definitions of “motivation” generally emphasize the activation and direction of
behavior toward a goal; and definitions of “emotion” also involve goal-directed action
but typically note the presence of peripheral physiological responses, expressive
behaviors and subjective experiences or affects (Kleinginna and Kleinginna 1981a,
1981b). Developmental-interactionist (DI) theory suggests that motives and emotions
imply one another: that motives constitute potential for behavior built into a system of
behavior control, and that emotions constitute readouts of motivational potential when
that potential is activated by an effective stimulus. There are three sorts of readout:
Emotion I involves peripheral physiological responding via the autonomic, endocrine,
and immune systems; Emotion II involves expressive displays such as facial expressions
and pheromone releases; and Emotion III involves subjective or affective experience of
desires and feelings (Buck, 1988a). In this view, motivation and emotion are related
similarly to energy and matter in physics. Energy is a potential that is never seen in
itself, but only in its manifestation in matter when activated by an effective stimulus: in
heat, light, and/or force. Thus, the potential energy in an explosive or a coiled spring is
not observable in itself, but it is revealed when activated by lighting the fuse or releasing
the spring. Similarly, motivation is never seen in itself, but only in its manifestations in
emotion: that is, in goal-directed behavior, peripheral physiological responding,
expressive displays, and subjectively experienced desires and feelings.
One feature of the DI view is that it implies that all of the biologically-based motives
and emotions are always turned on. Neurochemical systems underlying the experience
and expression of happiness, sadness, fear, anger, sex, hunger, thirst, etc. are always
activated to some extent, and we can turn our attention to the experience of these
emotions. But, like the feel of the shoes on our feet, this activation is typically weak and
these feeling are unnoticed unless an effective stimulus is presented.
Evolutionary Roots of Motivation and Emotion
Primes and paleoprimes. The above definitions can encompass primary
motivational/emotional states (primes) in human beings and also animals, with the
complexity of the state compatible with the complexity of the brain of the species in
question. DI theory argues that the capacity for the subjective experience of primary
emotions such as happiness, sadness, fear, and anger are associated with activity in
specific neurochemical systems, and studies of drug discrimination and place learning
suggest that animals are also capable of “subjective experience” (Buck, 1999; Panksepp,
1998). However, these definitions can also apply to primary motivational-emotional
systems in microbes whose evolution long preceded the evolution of the brain, which one
might term paleoprimes. Paleoprimes serve functions in simple creatures analogous to
those served by emotions in human beings—activation, approach-avoidance, dispersion,
and aggregation—and these can be observed in their behavior (Buck, 1999). Microbes
are active at some times and quiescent at others. They can be observed to approach some
stimuli (light, warmth) and avoid others. And, as we have seen, microbes also achieve
dispersion, aggregation, and cooperation by releasing molecules (pheromones) that repel,
attract, or otherwise influence others of their species.
Paleosociality. These systems in turn underlie paleosociality, involving the abilities of
microbes to communicate with one another and thereby complete social structures and
organizations (Buck & Renfro, 2006). As communication occurs in the course of
interaction between individual microbes, social organization emerges spontaneously and
effortlessly as a self-organizing system. The mechanism of this emergence through
interaction is spontaneous communication between elements, that is, between individual
microbes. In these creatures, the systems are simple enough that specific sending and
receiving mechanisms can be specified and the system of emergence understood at a
molecular and even genetic level. I suggest that these microbial systems illustrate
fundamental principles of social organization that illuminate mechanisms and principles
of social organization in more complex creatures including human beings.
More specifically, I suggest that a combination of attachment motives and social
comparison processes underlie the natural and effortless emergence of systems of social
and moral emotions that guide every human interchange. Motivational potential inherent
in attachment systems in infants are activated through early interactions with caregivers,
giving rise to fundamental needs to love and to be loved which constitute the affective
foundation of sociality. The need to be loved is, therefore, fundamental to human
sociality. With development, interactions with caregivers and peers teach the child rules
that must be followed in order to be loved: thus the child learns that one must meet and
exceed expectations in order to be loved. The need to meet and exceed expectations
therefore requires both a need to be loved and learning what those rules and expectations
are and how to meet them. This learning occurs naturally, effortlessly, and largely
unconsciously during the course of interactions with caregivers, peers, and later, lovers.
Primary Social and Moral Emotions
Unlike biologically-based emotions, DI theory regards social, moral, and also
cognitive emotions to be higher-level emotions, requiring both a physiological base in
neurochemical systems associated with attachment and exploration, and a “cognitive”
consideration of situational and interpersonal contingencies (Buck, 1999). The
neurochemical systems provide the affective “fire” to the higher-level emotions, while
the contingencies determine the quality of the emotion. More specifically, the individual
person (P) is exquisitely aware of success or failure in meeting expectations and being
loved, and P’s own success or failure can be compared with the success or failure of
comparison others (O’s). All possible combinations of success and failure of self and
other yields eight combinations of fundamental interpersonal contingencies that
correspond to eight primary social emotions (PSEs) organized into four pairs of twin
social emotions: if one succeeds one experiences pride/arrogance, if one fails it is
guilt/shame, if the other succeeds it is envy/jealousy, if the other fails it is pity/scorn. The
first of these twins is associated with meeting/exceeding expectations, that second with
being loved.
Attachment and social emotions. There is much evidence in the extensive research
stemming from attachment theory (Bowlby, 1969/1982) that persons who are securely
attached are relatively certain of being loved, while persons with attachment anxiety
worry that they are not loved, and persons with avoidant attachment distrust others and in
effect eschew love (e.g., Mikulciner, 1998; Mikulciner & Shaver, 2003, 2005;
Mikulciner, Shaver, Gillath, & Nitzberg, 2005). I suggest that secure attachment therefore
is associated with relatively less attention to being loved and greater attention to
meeting/exceeding expectations; that anxious attachment is associated with a greater
attention to being loved; and avoidant attachment is associated with relatively low
prosocial needs and therefore relatively weak social emotions. Therefore, a secure person
would be expected to experience pride, guilt, envy, and pity in situations where an
anxious person would experience arrogance, shame, jealousy, and scorn; and that an
avoidant person would tend to not experience any of these emotions strongly with the
extreme being a psychopath with no need to be loved who is incapable of experiencing
any of the social or moral emotions.
In this analysis, attachment is viewed as both a trait and a state. Most children can be
classified as having a specific attachment style, while most adults show a mixed style.
This may be because as social development proceeds, attachment security can
increasingly vary with the personal relationship of P vis a vis O: we may be secure that
we are loved by some persons but anxious about the love of others. So, we tend to feel
pride in comparison with the former and arrogance in comparison with the latter, for
example. Also, we can learn to avoid attachment with some persons. It is all too easy to
learn that certain persons are enemies who do not deserve our love, to whom social and
moral emotions are irrelevant. The ability of even normal human beings to become
situational psychopaths—to destroy others without moral compunction—is all too
apparent, as Hannah Arndt showed in her analysis of the banality of evil (Arndt,
1951/1973).
The dynamics of social emotions. This analysis implies that the eight PSEs are
interrelated: that for example when a person is proud they tend to pity others, and to NOT
to feel guilt or envy of others. Makoto Nakamura, Edward Vieira, Maxim Polonsky, and
I have tested this by giving scenarios about comparative success and failure to University
students in the United States and Japan: for example, if another person won the lottery
and got rich, how would you feel about them, and how would they feel about you? This
study found support for the hypothesized relationships between primary social emotions
in virtually every case, whether labeled in English or Japanese. This supported the
hypothesis of universal labeling: that the words for the eight PSEs could be found in all
languages, and the hypothesis of universal dynamics: that they would be interrelated
similarly in all languages. There were interesting differences between Japan and the
United States as well, consistent with the collectivist-individualist distinction: Japanese
were consistently more embarrassed than Americans, and Americans more proud than
Japanese, across all of the scenarios. It was also interesting that in both the US and Japan,
pity and scorn were negatively correlated, suggesting that there are two ways of
responding to the less fortunate, perhaps related to the security of the individual: secure
persons feel pity while anxious person feel scorn when the other fails (Buck, Nakamura,
Vieira, and Polonsky, 2005, submitted for publication).
Primary moral emotions. This analysis has been extended to the analysis of eight
primary moral emotions (PMEs), where success or failure for self and other is combined
with the judgment that the outcome is just or unjust. When one’s success is just the result
is triumph, when unjust it is modesty; when one’s failure is just the result is humiliation,
when unjust it is indignation; when the other’s success is just the result is admiration,
when unjust it is resentment; when the other’s failure is just the result is contempt, when
unjust it is sympathy. The PMEs are related to the PSEs: for example, envy and jealousy
can go with either admiration or resentment depending upon whether the other's success
is seen as justified. Research is presently under way to analyze the labeling and
dynamics of PSEs and PMEs in Japan, Ukraine/Russia, and India with Makoto
Nakamura, Maxim Polonsky and Sripriya Rangarajan.
Dominance-submission versus civility. The dynamics of social and moral emotions
are illustrated in Figure 1, which illustrates the social and moral emotions in a situation of
dominance and submission. The successful figure on the left exudes triumph, pride and
arrogance; and regards the inept figure on the right with contempt and scorn. The
unsuccessful figure feels guilt, shame, humiliation, and indignation; and regards the other
with envy, jealousy, and resentment. These can be strong acute emotions; they can be
fleeting as one might feel as one sees a person driving by in an expensive car, or they can
be chronic, unremitting, and grinding; leading to a lack of authentic social contact and
communication, the exacerbation of stress, unhappiness, and depression—perhaps in both
parties—whose true cause may be unrecognized.
---Figure 1--On the other hand, if the two figures show each other civility, a pattern of positive
interpersonal emotions can result. Even despite differences in wealth and status, it is
possible for two persons to have a relationship of mutual trust and respect in which each
regard the other as following the rules fairly and with a sense of justice. Each can then
regard their own successes with modesty, and respond to the other with a sense of mutual
gratitude for following the rules and admiration for their deserve success. These are the
ingredients for authentic communication and the powerful stress-buffering that can come
with social support.
This view of PSE's and PME's implies that sociality and morality arise spontaneously
and effortlessly from interaction: a spontaneous restructuring of socio-emotional
experience analogous to Piaget's (1971) assimilation and accommodation process in the
realm of cognitive development. From this point of view, organized religion is not
necessary to morality, and indeed can potentially get in the way of morality: even
promoting the situational psychopathy of religious intolerance and conflict. Similarly, as
Benson Ginsburg and I have suggested, this viewpoint suggests that kin selection and
reciprocity, rather than being the bases of altruism, are actually mechanisms to restrict
loving and altruistic feelings to kin and comrade: rather than underlying altruism, kin
selection and reciprocity are at the roots of xenophobia.
References
Allee, W. C. (1951). Cooperation among animals. New York: Henry Shuman.
Allee, W.C. (1931). Animal aggregations: A study in general sociology. Chicago: University
of Chicago Press.
Arendt, H (1951/1973). The Origins of Totalitarianism. New York: Harcourt.
Ben-Jacob, E., Becker, I., Shapira, Y., & Levine, H. (2004). Bacterial linguistic
communication and social intelligence. Trends in Microbiology. 12. 366-372.
Boone, R. T., & Buck, R. (2003). Emotional expressivity and trustworthiness: The role of
nonverbal behavior in the evolution of cooperation. Journal of Nonverbal Behavior. 27(3). 163182.
Bowlby, J. (1969/1982). Attachment and loss: Vol. I. Attachment. New York: Basic Books.
Buck, R. (1982). Spontaneous and symbolic nonverbal behavior and the ontogeny of
communication. In R. Feldman (Ed.) The Development of Nonverbal Behavior in Children. New
York: Springer Verlag.
Buck, R. (1976) Human motivation and emotion. (2nd ed 1988). New York: Wiley.
Buck, R. (1984). The Communication of Emotion. New York: Guilford
Buck, R. (1985). Prime theory: An integrated view of motivation and emotion. Psychological
Review. 92, 389-413.
Buck, R. (1988). Nonverbal communication: Spontaneous and symbolic aspects. American
Behavioral Scientist, 31, pp. 341-354.
Buck, R. (1988a) Human motivation and emotion. (2nd ed.). New York: Wiley.
Buck, R. (1989). On the semiotics of emotion: Spontaneous and symbolic communication.
In W.A. Koch (Ed.) For a Semiotics of Emotion, pp. 1-11. Bochumer Beitrage zur Semiotik.
Buck, R. (1992). Epistemological fundamentals: Knowledge-by-acquaintance and spontaneous communication. Journal of Pragmatics, 17(5-6), pp. 447-454.
Buck, R. (1994). Social and emotional functions in facial expression and communication: The
readout hypothesis. Biological Psychology, 38, 95-115.
Buck, R. (1994). The neuropsychology of communication: Spontaneous and symbolic aspects. Journal of Pragmatics, 22, pp. 265-278.
Buck, R. (1999). The biological affects: A typology. Psychological Review. 106(2), 301-336.
Buck, R. (2002). The genetics and biology of true love: Prosocial biological affects and the
left hemisphere. Psychological Review. 109. pp. 739-744.
Buck, R. (2002a). "Choice" and "emotion" in altruism: Reflections of the Morality of Justice
versus the Morality of Caring. Behavioral and Brain Sciences. 25. 254-255.
Buck, R. (2004). The gratitude of exchange and the gratitude of caring: A developmentalinteractionist perspective of moral emotion. In R. A. Emmons and M. McCullough (Eds.), The
Psychology of Gratitude. (100-122). New York: Oxford University Press.
Buck, R. (2005). Measuring emotional experience, expression, and communication: The
slide-viewing technique. In V. Manusov (Ed.), The Sourcebook of Nonverbal Measures.
Mahwah, NJ: Lawrence Erlbaum Associates.
Buck, R., & Ginsburg, B. E. (1991). Emotional communication and altruism: The
communicative gene hypothesis. In M. Clark, (Ed.), Altruism. Review of Personality and Social
Psychology. Vol. 12. (pp. 149-175) Newbury Park, CA: Sage Publications,.
Buck, R., & Ginsburg, B. E. (1997a). Communicative genes and the evolution of empathy.
In W. Ickes (Ed.), Empathic accuracy. (pp. 17-43). New York: Guilford.
Buck, R., & Ginsburg, B. E. (1997b). Communicative genes and the evolution of empathy:
Selfish and social emotions as voices of selfish and social genes. In C. S. Carter, I. I.
Lederhendler, and B. Kirkpatrick (Eds.), The integrative neurobiology of affiliation. (pp. 481483). New York: The New York Academy of Sciences.
Buck, R., & Ginsburg, B. E. (2000). Communicative genes in the evolution of behavioral and
social systems: Empathy and altruism. Convention of the American Political Science
Association, Washington, DC. August 30-September 3, 2000.
Buck, R., & Renfro, S. (2006). The biological foundations of social organization: The
dynamic emergence of social structure through nonverbal communication. In V. Manusov and
Miles Patterson (Eds.). Handbook of Nonverbal Communication. Sage Publications, In press.
Buck, R., & Van Lear, C. A. (2002). Verbal and nonverbal communication: Distinguishing
symbolic, spontaneous, and pseudo-spontaneous nonverbal behavior. Journal of Communication.
52. 522-541.
Buck, R., Nakamura, M., Vieira, E. T., Jr., and Polonsky M. (2005). “A DevelopmentalInteractionist Theory of Biological and Higher Level Emotions: A Cross-National Comparison of
America and Japan.” Plenary presentation at the Symposium: New Perspectives in Affective
Science. Kyoto University, Kyoto, Japan. January 2005. Paper submitted for publication.
Burgdorf, J., & Panksepp, J. (2001). Tickling induces reward in adolescent rats. Physiology
& Behavior. 72. 167-173.
Carter, C. S., (1996). Peptides, steroids, and pairbonding. Presentation at the New York Academy of
Sciences Conference on the Integrative Neurobiology of Affiliation, Georgetown University,
Washington, D.C., March 14-17, 1996.
Carter, C. S., Lederhendler, I. I., and Kirkpatrick, B. (Eds.), The integrative neurobiology of
affiliation. Annals of the New York Academy of Sciences. Vol. 807. (pp. 260-272) New York:
The New York Academy of Sciences.
Clarke, C. H. (1981). Motility and fruiting in the bacterium Myxococcus xanthus. In J. M.
Lackie and P. C. Wilkinson, (Eds.), Biology of the chemotactic response. (pp. 155-171).
Cambridge: Cambridge University Press.
Cohn, D. F., and Schmidt, K. L. (2004). The timing of facial motion in posed and
spontaneous smiles. International Journal of Wavelets, Multiresolution, and Information
Processing. 2. 1-12.
Costerson, J. W., Stewart, P. S., & Greenberg, E. P. (1999). Bacterial biofilms: A common cause of
persistent infections. Science. 284. 1318-1322.
Darwin, C. (1872 orig.). The expression of the emotions in man and animals. (3rd Ed.) New
York: Oxford University Press. 1998.
Dawes, R. M., McTavish, J., Shaklee, H. (1977). Behavior, communication, and
assumptions about other people’s behavior in commons dilemma situation. Journal of
Personality and Social Psychology, 35, 1-11.
Dawkins, R. (1982). The extended phenotype: The gene as the unit of selection. Oxford: Oxford
University Press.
Dawkins, R. (1989). The selfish gene: New edition. New York: Oxford.
Dawkins, R. (1994). Burying the vehicle. Behavioral and Brain Sciences, 17, 616-617.
Dobzhansky, T. (1937). Genetics and the origin of species. New York: Columbia University Press.
Dawkins, R., & Krebs, J. R. (1978). Animal signals: Information or manipulation? In J. R.
Krebs & N. B. Davies, (Eds.), Behavioural ecology: An evolutionary approach. Oxford:
Blackwell Scientific, pp. 282-309.
de Beun, R., Geerts, N. E., Jansen, E., Slangen, J. L., et al. (1991). Luteinizing hormone releasing
hormone-induced conditioned place preferences in male rats. Pharmacology, Biochemistry, and
Behavior, 39, 143-147.
de Waal, F. B. M., and Tyack, P. L. (2003). Animal social complexity: Intelligence, culture,
and individualized societies. Cambridge, MA: Harvard University Press.
Eberhard, A., Burlingame, A. L., Eberhard, C., Kenyon, C. L., Nealson, K. H., &
Opppenheimer, N. J. (1981). Structural identification of autoinducer of Photobacterium fischeri
luciferase. Biochemistry. 20. pp. 2444-2449.
Eibl-Eibesfeldt, I. (1975). Ethology: The biology of behavior (2nd ed.), New York: Holt,
Rinehart & Winston.
Engebrecht, J., Nealson, K., & Silverman, M. (1983). Bacterial bioluminescence: Isolation
and genetic analysis of functions from Vibrio fischeri. Cell. 32. pp. 773-781.
Farrow, Tom F. D.; Zheng, Ying; Wilkinson, Iain D. (2001). Investigating the functional
anatomy of empathy and forgiveness. Neuroreport: For Rapid Communication of Neuroscience
Research, Vol 12(11), Aug 2001. pp. 2433-2438.
Foster, K. R. (2005). Hamiltonian medicine: Why the social lives of pathogens matter.
Science. 308. 1269-1270.
Frank, R. (1988). Passions within reason: The strategic role of the emotions. New York:
Norton.
Frank, R. (2001). Cooperation through emotional commitment. In R. M. Hesse (Ed.), Evolution
and the capacity for commitment (pp. 57 – 76). New York, Russell Sage Foundation.
Frank, R. H. (2004). In defense of sincerity detection. Rationality and Society. 16(3). 287305.
Frank, R., Gilovich, T., & Regan, D. T. (1993). The evolution of one-shot cooperation: An
experiment. Ethology and Sociobiology, 14, 247 – 256.
Fuqua, C., Winans, S.C., & Greenberg, E. P. (1996). Census and consensus in bacterial
ecosystems: The LuxR - LuxI family of quorum-sensing transcriptional regulators. Annual
Reviews of Microbiology, 50, p 727.
Gallio, M., Sturgill, G., Rather, P., & Kylsten, P. (2002). A conserved mechanism for
extracellular signalling in eukaryotes and prokaryotes. Proceedings of the National Academy of
Sciences. 99(19). Pp. 12208-12213.
Gerisch, G., Fromm, H., Huesgen, A., & Wick, U. (1975). Control of cell contact sites by
cyclic-AMP pulses in differentiating Dictyostelium cells. Nature (London) 255, 547-549.
Gerisch, G., Krelle, H., Bozarro, S., Eitle, E., & Guggenheim, R. (1980). Analysis of cell
adhesion in Dictyostelium and Polysphondylium by the use of Fab. In A. S. G. Curtis and J. D.
Pitts (Eds.), Cell adhesion and motility. (pp. 293-307). Cambridge: Cambridge University Press.
Gottleib, G. (1984). Evolutionary trends and evolutionary origins: Relevance to theory in
comparative psychology. Psychological Review, 91, 448-456.
Greenberg, E. P. (1997). Quorum-sensing in gram-negative bacteria. ASM News 63(July), 371.
Griffen, A. S., West, S. A., & Buckling, A. (2004). Cooperation and competition in pathogenic
bacteria. Nature.430. 1024-1027.
Hamilton, W. D. (1963). The evolution of altruistic behavior. American Naturalist, 97, 354-356.
Hamilton, W. D. (1964). The genetical evolution of social behavior. Journal of Theoretical
Biology. 31. 295-311.
Harlow, H. F. (1971). Learning to love. San Francisco: Albion.
Hauser, M. D. (1996). The evolution of communication. Cambridge, MA: MIT Press.
Hellingwurf, K. J. (2005). Bacterial observations: A rudimentary form of intelligence? Trends
in Microbiology. 13. 152-158.
Hentzer, M., & Givskov, M. (2003). Pharmacological inhibition of quorum sensing for the
treatment of chronic bacterial infections. Journal of Clinical Investigations. 112. 1300-1307.
Insel, T. R., and Young, L. J. (2001). Neurobiology of social attachment. Nature
Neuroscience Review. 2. 129-136.
Insel, T. R., and Young, L. J. (2001). Neurobiology of social attachment. Nature
Neuroscience Review. 2. 129-136.
Insel, T. R., Young, L., & Wang, Z. (1997). Molecular aspects of monogamy. In C. S. Carter,
I. I. Lederhendler, and B. Kirkpatrick (Eds.), Annals of the New York Academy of Sciences. Vol.
807. The integrative neurobiology of affiliation. (pp. 302-316) New York: The New York
Academy of Sciences.
Jurgens, U. (1979). Neural control of vocalization in nonhuman primates. In H. L. Steklis
and M. J. Raleigh (Eds.), Neurobiology of social communication in primates. New York:
Academic Press, 11-44.
Kenny, D. A. (1994). Interpersonal perception: A social relations analysis. New York:
Guilford.
Kleinginna, P. R., & Kleinginna, A. M. (1981a). A categorized list of motivation definitions,
with suggestions for a consensual definition. Motivation and Emotion, 5, 263-291.
Kleinginna, P. R., & Kleinginna, A. M. (1981b). A categorized list of emotion definitions,
with suggestions for a consensual definition. Motivation and Emotion, 5, 348-379.
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005). Oxytocin
increases trust in humans. Nature. 435, 673-676.
Krebs, J. R., & Dawkins, R. (1984). Animal signals: Mind-reading and manipulation. In J.
R. Krebs & N. B. Davies, (Eds.), Behavioural ecology: An evolutionary approach. (2nd Edition,
pp. 380-402). Sunderland, MA: Sinauer.
Kreft, J-U. (2004a). Conflicts of interest in biofilms. Biofilms. 1. 265-276.
Kreft, J-U. (2004b). Biofilms promote altruism. Microbiology. 150. 2751-2760.
Lackie, J. M. (1986). Cell movement and cell behaviour. London: Allen & Unwin.
Lim, M. M., Wang, Z., Olazabal, D. E., Ren, X., Terwilliger, E. F., & Young, L. J. (2004)
Enhanced partner preference in a promiscuous species by manipulating the expression of a single
gene. Nature. 429. 754-757.
Livingstone, M. S., Harris-Warrick, R. M., & Kravitz, E. A. (1980). Serotonin and
octopamine produce opposite postures in lobsters. Science, 208(4439), 76-79.
Losick, R., & Kaiser, D. (1997). Why and how bacteria communicate. Scientific American,
276(2), 68-73.
Loumaye, E., Thorner, J., & Catt, K. J. (Dec 24, 1982). Yeast mating pheromone activates
mammalian gonadotropins: Evolutionary conservation of a reproductive hormone? Science,
218(4579). 1324-1325.
MacLean, P. D. (1993). The cerebral evolution of emotion. In M. Lewis and J. Haviland
(Eds.), Handbook of Emotions. (pp. 67-83) New York: Guilford.
Mikulciner, M., & Shaver, P. (2003). The attachment behavioral system in adulthood:
Activation, psychodynamics, and interpersonal processes. In M. P. Zanna (Ed.), Advances in
Experimental Social Psychology. (Vol. 35, pp. 53-152). San Diego, CA: Academic Press.
Mikulciner, M., & Shaver, P. (2005). Mental representation of attachment security:
Theoretical foundation for a positive social psychology. In M. W. Baldwin (Ed.), Interpersonal
Cognition. (pp. 233-266). New York: Guilford Press.
Mikulciner, M., Shaver, P., Gillath, O., & Nitzberg, R. A. (2005). Attachment, caregiving,
and altruism: Boosting attachment security increases compassion and helping. Journal of
Personality and Social Psychology, 89, 817-839.
Mikulincer, M. (1998). Attachment working models and the sense of trust: An exploration of
interaction goals and affect regulation. Journal of Personality and Social Psychology, 74, 12091224.
Miller, R. E., Caul, W. F., & Mirsky, I. A. (1967). Communication of affects between feral
and socially isolated monkeys. Journal of Personality and Social Psychology, 7, 231-239.
Moore, F. L. (1987). Behavioral actions of neurohypophysial peptides. In D. Crews (Ed.),
Psychobiology of reproductive behavior: An evolutionary perspective. (pp. 61-87). Englewood Cliffs,
NJ: Prentice Hall.
Newell, P. C. (1981). Chemotaxis in the cellular slime moulds. In J. M. Lackie and P. C.
Wilkinson (Eds.), Biology of the chemotactic response. (pp. 89-114). Cambridge: Cambridge
University Press.
Olson, S. (1989). Shaping the Future: Biology and Human Values. Washington, D.C.:
National Academy Press.
Panksepp, J. (1991). Brain opioids: A neurochemical substrate for narcotic and social
dependence. In Cooper, S. (Ed.), Theory in psychopharmacology. (pp. 149-175). London:
Academic Press.
Panksepp, J. (1993). Neurochemical control of moods and emotions: Amino acids to neuropeptides.
In M. Lewis and J. Haviland (Eds.), Handbook of Emotions. New York: Guilford.
Panksepp, J. (1998). Affective neuroscience: The foundations of human and animal emotions.
New York: Oxford University Press.
Panksepp, J. and Burgdorf, J. (2000). 50-kHz chirping (laughter?) in response to conditioned
and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables.
Behavioural and Brain Research, 115, pp. 25-38.
Panksepp, J., Nelson, E., & Bekkedal, M. (1997). Brain systems for the mediation of social
separation-distress and social-reward: Evolutionary antecedents and neuropeptide intermediaries.
In C. S. Carter, I. I. Lederhendler, and B. Kirkpatrick (Eds.), Annals of the New York Academy of
Sciences. Vol. 807. The integrative neurobiology of affiliation. (pp. 78-100) New York: The New
York Academy of Sciences.
Piaget, J. (1971). Piaget’s theory. In: P. Mussen (Ed.). Handbook of Child Development, Vol. I.
(pp. 703-732). New York: Wiley.
Ploog, D. (1981). Neurobiology of primate audio-vocal behavior. Brain Research Reviews,
3, 35-61.
Pollak, Seth D., Klorman, Rafael, Thatcher, Joan E., Cicchetti, Dante (2001). P3b reflects
maltreated children's reactions to facial displays of emotion. Psychophysiology, 38(2), Mar 2001.
pp. 267-274.
Preston, S. D., & deWaal, F. B. (2002). Empathy: Its ultimate and proximal bases.
Behavioral and Brain Sciences. 25. 1-72.
Rachlin, H. (2002). Altruism and selfishness. Behavioral and Brain Sciences. 25. XX
Rauh, C., Polonsky, M., and Buck, R. (2004). “Cooperation on the First Move: Trust,
Emotional Expressiveness and Avatars in the Prisoner’s Dilemma Game”
Redfield, R. J. (2002). Is quorum sensing a side effect of diffusion sensing? Trends in
Microbiology. 10. 365-370.
Riedel, K., & Ebert, L. (2002). Communication in bacterial biofilms. Biomedical Progress.
15. pp. 69-74.
Sabatelli, R. M., Buck, R., & Kenny, D. A. (1986). A social relations analysis of nonverbal
communication accuracy in married couples. Journal of Personality, 54(3), 513-527.
Sally, D. (1995). Conversation and cooperation in social dilemmas: A meta-analysis of
experiments from 1958 to 1992. Rationality and Society, 7(1), 58 - 92.
Schaefer, A. L., et al. (1996). Quorum-sensing in Vibrio fischeri: Probing autoinducer-LuxR
interactions with autoinducer analogs. Journal of Bacteriology, 178, 2897.
Shimkets, L. J. (1999). Intracellular signaling during fruiting-body development of
Myxococcus xanthus. Annual Review of Microbiology. 53. 525-549.
Sober, E., & Wilson, D. S. (1998). Unto others. Cambridge, MA: Harvard.
Strassmann, J. E., Zhu, Y., & Queller, D. C. (2000). Altruism and social cheating in the social
amoeba Dictyostelium discoideum. Nature. 408. 965-967.
Swift, S., et al., (1996). Quorum sensing: A population-density component in the
determination of bacterial phenotype. Trends in Biochemical Sciences, 21, 214.
Town, C. D., & Stanford, E. (1979). An oligosaccharide-containing factor that induces cell
differentiation in Dictyostelium discoideum. Proceedings of the National Academy of Sciences
USA. 76. 308-312.
Town, C. D., Gross, J. D., & Kay, R. R. (1976). Cell differentiation without morphogenesis in
Dictyostelium discoideum. Nature. 262. 717-719.
Travisano, M., & Velicer, G. J. (2004). Strategies of microbial cheater control. Trends in
Microbiology. 12. 72-78.
Trivers, R. L. (1971). The evolution of reciprocal altruism. Quarterly Review of Biology, 46,
35-57.
Vicker, M. G., Schill, W., & Drescher, K. (1984). Chemoattraction and chemotaxis in
Dictyostelium discoideum: Myxaamoeba cannot read spatial gradients of cyclic adenosine
monophosphate. Journal of Cell Biology, 98, 2204-2214.
Visick, K. L., Foster, J., Doino, J., McFall-Nagai, M., & Ruby, E. G. (2000). Vibrio fischeri
lux genes play an important role in colonization and development of the host light organ. Journal
of Bacteriology. 185. 2080-2095.
Wang, Z., and Aragona, B. J. (2004). Neurochemical regulation of bonding in male prairie voles.
Physiology and Behavior. 83(2). 319-328.
Warner, R. M., Kenny, D. A., & Stoto, M. (1979). A new round robin analysis of variance for
social interaction data. Journal of Personality & Social Psychology, 37(10), 1742-1757.
Waters, C. M., & Bassler, B. L. (2005). Quorum sensing: Cell-to-cell communication in
bacteria. Annual Review of Cell and Developmental Biology. 21. 319-346.
Williams, G. C. (1966). Adaptation and natural selection: A critique of some current evolutionary
thought. Princeton: Princeton University Press.
Williams, J. R., Insel, T. R., Harbaugh, C. R., & Carter, C. S. (1994). Oxytocin administered
centrally facilitates formation of a partner preference in prairie voles (Microtus ochrogaster).
Journal of Neuroendocrinology. 6. 247-250.
Wilson, D. S., & Sober, E. (1994). Reintroducing group selection to the human behavioral
sciences. Behavioral and Brain Sciences. 17, 585-654.
Wilson, E. O. (1975). Sociobiology: The new synthesis. Cambridge, MA: Belknap.
Wismer Fries, Alison B., Pollak, Seth D., (2004). Emotion understanding in
postinstitutionalized Eastern European children. Development and Psychopathology, 16(2), pp.
355-369.
Wismer Fries, Alison B., Ziegler, Toni E., Kurian, Joseph R., Jacoris, Steve, & Pollak, Seth
D. (2005). Early experience in humans is associated with changes in neuropeptides critical for
regulating social behavior Proceedings of the National Academy of Sciences. 102. pp.1723717240.
Wynn-Edwards, V. C. (1962). Animal dispersion in relation to social behaviour. Edinburgh: Oliver
and Boyd.
Young, L. J., Lim, M. M., Gingrich,B., & Insel, T. R. (2001). Cellular mechanisms of social
attachment. Hormones-and-Behavior. 40 (2): 133-138.
Figure Captions
Figure 1. In a dominant-submissive relationship, conflict can be exacerbated by moral
considerations: The perception of unfairness.