## 1. Sociobiology as Behavioral Ecology



The first meaning of "sociobiology" is a term for a range
of work that is more often currently referred to as *behavioral
ecology*. Behavioral ecology is a science that uses evolutionary
theory and especially adaptationist methods to try to understand
animal behavior. Consider, for example the female parasitic jewel
wasp. This wasp lives and lays its eggs in blowfly pupae; after a
female wasp of this species is born and reaches adulthood she mates
with one of the males also occupying her pupa, and then emerges and
flies off to lay her eggs in another pupa. The jewel wasp is
haplodiploid, and females can control the sex of each of their
offspring by controlling whether or not the egg is fertilized when she
lays it. What is particularly interesting about this wasp is that the
percentage of females to males she lays depends on whether she got to
the pupa first. If she is first to the pupa she lays a number of eggs,
with mostly females (about 91.3%) and some males (about 8.7%).
However, if she lays eggs in a pupa after another female has been
there (this is called *superparasitism*), she lays a lot more
sons than daughters. Behavioral ecologists are interested in
understanding why animal behaviors like this have the peculiar
features they do.



Behavioral ecology is sometimes characterized in terms of its
relationships to the earlier "ethology" whose most famous
practitioners are probably Konrad Lorenz and Niko Tinbergen. Tinbergen
(1963) famously described four types of questions that an ethologist
might ask in trying to understand some pattern of animal behavior,
such as the egg laying strategy of the jewel wasp above. First, the
ethologist could ask questions about the *proximate causes* of
the behavior: for example, what neurological or psychological
mechanisms lead the wasp to lay her eggs in the pattern she does? What
mechanisms are responsible for the *development* of that
mechanism--what developmental processes build the neural tissue
that directly causes the egg laying behavior? Second, the ethologist
could ask two ultimate, evolutionary questions about the behavior:
what is the *evolutionary function* of the behavior, i.e. how
does laying eggs in that pattern contribute to the wasp's
reproductive success, to the reproductive success of its ancestors,
and hence to the behavior's history of evolution by natural
selection (if that is its history) in the jewel wasp population? Also,
what is the *phylogeny* of the behavior, i.e. where did it
arise in the evolutionary tree of the jewel wasp?



Unlike ethologists, behavioral ecologists studying animal behavior at
first tended to focus on the third question, the question of
evolutionary function, at the expense of the others (Griffiths, 2008;
Krebs and Davies, 1997). Griffiths (2008) has argued such a focus by
the behavioral ecologists on questions of function at the expense of
questions of causation, development and phylogeny (but especially
development) was highly problematic, since the four questions cannot
be properly answered independently. Development constrains the
evolution of biological traits in multiple ways, and behavior
especially, since behavior depends on development at both neurological
and psychological levels. Behavioral ecologists, however, for a long
time took the complexity of the developmental resources contributing
to behavior as a reason for (at least temporarily) avoiding such
studies as part of their study of the evolution of behavior. Grafen
(1984) argues that the problem with developmental approaches to
behavior is that they are hard and lengthy to perform, especially if
the *only* or *primary* purpose of the developmental
work is to check that the trait in question does indeed have an
evolutionary history that can be understood using adaptationist
methods. Grafen argues that if behavioral ecologists had to perform
developmental or psychological studies to be relatively confident of
their conclusions about the evolutionary history of traits, they would
probably never get as far as evolutionary studies, since such
developmental and genetic work would take a very long time. Worse,
such studies might well have no inherent interest of their own and
represent a waste of time and resources for the scientist--not
all traits have an interesting or enlightening developmental
background or are produced by interesting and unknown psychological
mechanisms. Instead, Grafen argues that behavioral ecologists should
use what he calls the "phenotypic gambit" in studying the
evolution of behavioral traits. This involves assuming that the
developmental, psychological and genetic proximate causes of a
behavioral trait, such as the jewel wasp's egg-laying strategy
are of a type that will permit scientists to "pretend"
that they are very straightforward when building evolutionary models,
and yet still end up with models that give approximately the right
answers about the primary processes, conditions and constraints acting
on that trait during its evolution (for another similar view see
Maynard Smith, 1982, 6ff).



Since Grafen wrote his article, however, there has been a certain
shift in non-human behavioral ecology away from the phenotypic gambit
and in favor of paying attention to proximate mechanisms, not simply
because these enlighten whether a behavioral strategy could evolve by
natural selection in any particular case, but also the nature of the
fitness costs and benefits that accrue to an organism sometimes depend
on how the adaptive problem they face is solved. For example, Lotem et
al. (1995) appeal to the type of learning mechanism used by parenting
great reed warblers to detect the presence of cuckoos in their nests:
this limits how reliable their detection of cuckoo eggs can be.
Similarly, Shuker and West (2004) argue that the constraints on the
egg laying strategy of the parasitic jewel wasp cannot be properly
understood without paying attention to the limits on the detection
mechanisms the wasp uses to determine the presence or absence of
*other females*, versus other females' *eggs* in
each area.



Perhaps the most important analytical tool of the behavioral ecologist
is the *optimality model* (Maynard Smith, 1978): however,
frequency dependent models, which do not assume population fixation of
a trait, such as evolutionary stable strategy models (Maynard Smith,
1982) (see also the entry on
 evolutionary game theory)
 and dynamic models, such those employed in studying life history
traits (Roff, 1992), are also used. Optimality models are designed to
show which of a set of possible variant behavioral strategies would
maximize a local fitness
 currency[2]
 under a range of ecological conditions and constraints implicitly or
explicitly represented in the mathematical structure of the model.
These conditions are supposed to represent the *selection
conditions* of the trait (the conditions responsible for driving
its evolution by natural selection - Brandon, 1990); however,
they are usually derived by observing the conditions under which the
organism is currently living, since these are assumed generally to
have remained much the same as the conditions under which the organism
evolved (Turke, 1990). Werren (1980) provided just such a model for
the jewel wasp above; the model suggests that the reason for the
change in the ratio of sons to daughters when a female wasp finds an
occupied pupa is due to the potential opportunity to mate with the
daughters of the first wasp. If only the first wasp lays her eggs on
the pupa, then the hatching daughters mate with their brothers and all
their offspring are entirely descendants of the first wasp. This means
the first wasp needs to produce very few sons--only enough to
mate with all the females; the second generation reproductive success
of the first wasp is maximized by maximizing the number of daughters.
However, where there is a superparasitic wasp, the superparasitic
wasp's sons can mate with the large numbers of daughters of the
first wasp. The superparasitic wasp needs to maximize the number of
the females in the pupa that breed with her sons as opposed to their
brothers, whilst at the same time limiting the amount of competition
amongst her sons. So if she has only a few eggs to lay, it makes sense
for her to lay almost all sons; as brood sizes grow larger, it makes
sense to gradually increase the proportion of daughters in the mix.
Werren calculated the optimal percentages of males and females for
each brood size. His observations of male to female ratios fit the
predictions of this model quite well but not perfectly.



There is some debate among various philosophers and behavioral
ecologists about what exactly optimality models like Werren's
are being used to demonstrate. Orzack and Sober (1994) claim that
behavioral ecologists like Werren use optimality models to demonstrate
that the traits in question are adaptations, i.e. that the traits have
evolved by natural selection. Furthermore, Orzack and Sober take
optimality models to be *censored* models, that is, they are
designed to determine the outcome of natural selection in a population
where natural selection is the only important force, and hence show,
given the model correctly predicts the observed features of the trait
being studied, that natural selection was the most important force in
its
 evolution[3].
 The idea then, is that the relative success of Werren's model
is supposed to demonstrate that natural selection was the most
important force in the evolution of the jewel wasp's egg-laying
strategy--other forces may have been involved, but they are not
as causally important. However, various other philosophers have argued
that such models do not make such strongly adaptationist assumptions;
Potochnik (2009), for example, argues that optimality models are only
designed to show the general role that natural selection and other
forces (such as developmental constraints) are playing, and are not
designed to test strong adaptationist hypotheses about the behavioral
strategies in question--i.e. in our case above, the success of
the model is intended to show that natural selection was acting on the
jewel wasp's strategy, and that the *way* it was acting
on the jewel wasp's strategy was via the effects of competition
between the male wasps in the pupa, the variations in brood size and
the other conditions and constraints to which Werren's model
appeals. The success of the model is *not* intended to show
that natural selection was the only important force involved in the
evolution of the jewel wasp's strategy. For other criticisms of
the censored model view, see Rice (2012) and Bolduc and Cezilly
(2012).



However, interestingly, some behavioral ecologists have claimed that
they do not use optimality models to test whether or not natural
selection is acting on a trait, but instead assume the operation of
natural selection in order to test hypotheses about the conditions and
constraints acting on the trait (Parker and Maynard Smith, 1990). This
could be problematic, if it means behavioral ecologists baldly accept
the view that natural selection optimizes most traits and never
properly test this claim. However, one interpretation of Parker and
Maynard Smith (1990) is not that behavioral ecologists have an
unfalsifiable commitment to the idea that natural selection is an
optimizer. Instead, they are claiming that testing hypotheses about
the operation of natural selection itself is not what the behavioral
ecologists are focusing on. The behavioral ecologists are making the
preliminary assumption that a trait is an adaptation in order to test
other hypotheses about it--they "pretend as if" the
trait were an adaptation, and use that assumption to detect
*deviations* from optimality that might reveal interesting
tradeoffs and constraints--the nature of the deviation can
suggest what might be missing from the model. This of course has the
upshot that when the models initially fail, the scientists do not look
for alternative non-adaptationist hypotheses, but instead
*initially* look for new constraints, tradeoffs and conditions
under which selection might be operating. For example, Giraldeau
(1997) describes deviations from optimality in the evolution of
photopigments in the rods (as opposed to cones) in the retinas of fish
that live in certain sorts of marine environments where a shift in
photosensitivity would be useful; Giraldeau uses this deviation to
suggest the presence of a molecular constraint on the evolution of the
rod cells. Presumably, repeated failures to find ways to fill in the
gaps in these optimality models could ultimately result in the
scientists concerned considering alternative, non-adaptationist
explanations. So in order for the behavioral ecologists do this work
they do not need to be committed to the strong view that natural
selection is always the most important force in the origin of traits;
this heuristic requires at most the view that natural selection
usually *locally* optimizes (i.e. optimizes only relative to
possibly severe constraints).



However, another way to understand how the behavioral ecologists are
using optimality models, one that is not so often considered, is that
they are interested in providing a *functional description* of
the traits they are studying (Kitcher, 1987; see also Bolduc and
Cezilly, 2012, for a similar view in terms of decision patterns rather
than behavioral strategies). One of the things that may concern a
behavioral ecologist is how exactly to describe the nature of the
behavior that they are considering: what component behavioral
dispositions (from among all of the organism's behavior) make up
each strategy, and how those dispositions hang together as an
adaptation. They need to give a description of the relationship
between the organism's behavior and its environment, and how it
contributes to the organism's fitness. In the jewel wasp case,
the behavioral ecologists have observed the wasps lay different egg
sex ratios on different occasions. The question is how to make sense
of these different sex-ratio laying behaviors: the guess is that these
different behaviors hang together somehow, as manifestations of a
particular egg-sex-ratio adjusting strategy; and that having this
particular strategy, this particular pattern of egg-sex-ratio laying
behavior, *does something for* the female wasp when considered
as a whole. But why should a behavioral ecologist accept that any
particular such a functional description is true?



An optimality model can allow a behavioral ecologist to find and test
such a functional description in two ways. First, an optimality model
(explicitly or implicitly) includes a *strategy set*, which is
a set of descriptions of possible behavioral strategies; the model
picks out one of these strategy descriptions as the one that is
maximally adaptive. On Werren's model, the strategy set would be
an (implicit) set of descriptions of the range of possible sex-ratio
adjusting strategies that a jewel wasp could use (i.e. each strategy
involves a different set of choices about sex ratios in a *full
range* of relevant conditions like parasitism, superparasitism and
different brood sizes). The idea is that an optimality model can pick
out which member of this set is a description of the maximally
adaptive strategy - on this view of what the behavioral
ecologists are doing, Werren's model is designed to pick out the
optimal sex ratio egg laying strategy description from the strategy
set. The hypothesis is that this description of the *maximally
adaptive* strategy will be the *correct* description of
what the wasp is doing. If it is the correct description, then Werren
can now predict what son/daughter ratios he should see the wasp lay in
cases so far unobserved. These predictions allow him to test if the
description is correct - if these predictions are true, then on
this view, Werren has confirmed that the description of the particular
sex-ratio adjusting strategy derived from his model is the correct
description of what the wasp is doing.



Second, the description of the strategy picked out by the model is not
simply a description of it as a series of behavioral dispositions
(i.e. dispositions to lay different sex ratios under different
conditions), but of the relationships between those dispositions and
various ecological features that determine the fitness of those
dispositions. For example, in the jewel wasp case, the presence of
other female competitors, flexibility in brood size, the capacity of
sons to mate multiple times, the impossibility of migration of sons
between pupae and so on, are features of the environment that
determine whether any potential egg laying strategy of the jewel wasp
is maximally adaptive, and a well confirmed optimality model can show
how. Consequently, contingent on obtaining the appropriate evidence
that this is the correct model, the description of the strategy given
by a successful model is (implicitly or explicitly) a
*functional* description of the strategy--a description of
how the behavior contributes to the fitness of the organism. For a
more detailed discussion of the role of optimality modeling in
biology, see the entry on
 adaptationism.


## 2. "Pop Sociobiology"



The second way that "sociobiology" has come to be
understood is as a particular approach to understanding specifically
*human* behavior which Philip Kitcher (1985) calls "Pop
Sociobiology" (as opposed to his description of "narrow
sociobiology" which is roughly equivalent to "behavioral
ecology" above). Pop Sociobiology is so-called because it is a
view about how to study human behavior described in a variety of
literature written by Wilson and
 others[4]
 for a general, rather than an academic audience. In this literature,
Wilson and the other "Pop sociobiologists" present some
speculative and
 preliminary[5]
 sketches of how an evolutionary science of human behavior might
proceed: Wilson's main focus in *On Human Nature*
(Wilson, 1978) and to a lesser extent the last chapter of
*Sociobiology* (Wilson, 1975) is to show that such a science is
possible, to describe some of the techniques that might be used in
pursuing it, and to sketch some possible evolutionary analyses for
certain particular human behaviors. Because of its presentation in the
popular press, "Pop Sociobiology" was probably important
in shaping popular perceptions of the nature of sociobiology in
general (for example, the *Time* article, "Why you do
what you do" 1977, 110 (Aug 1), 54) and consequently drew the
ire of the critics. Unfortunately, the intensity of this debate may
have led to a certain amount of mischaracterization of the
sociobiologists' views. This section will address the main
concerns that the critics raised about Wilson's early
"Pop" sociobiology, and discuss whether and how far these
are fair descriptions of his views.



*Genetic determinism*. In a variety of articles major critics
of sociobiology such as Stephen J. Gould (1977, 251-259; 1978)
and the so-called "Sociobiology Study Group" (hereafter
SSG) (Allen et al., 1975; Sociobiology Study Group of Science for the
People, 1976) claim that sociobiologists are strong genetic
determinists. For example, according to the SSG Wilson believes that
there are particular genes "for" behavioral traits,
including indoctrinability, territoriality, warfare and reciprocal
altruism, and that these genes are subject to natural selection in a
relatively straightforward way. Indeed, the SSG (1976) argue that
claiming that traits have a selective origin requires that there are
genes "for" them; Wilson's apparent acceptance that
traits may often have a strong cultural component is said to be an
error, since if this is true then evolutionary theory tells us nothing
about the origin of such traits. Gould (1977) similarly claims that
sociobiologists do not realize that genes only produce traits with a
contribution from the environment.



Both of these claims are believed, even by other critics, to be unfair
analyses of the views of the sociobiologists, and especially
Wilson--for example, Kitcher, one of the strongest critics of
sociobiology, takes Gould and the SSG to task on this point (Kitcher,
1985, 22-23). In *On Human Nature* Wilson describes genes
as, essentially, difference makers--he explicitly claims that
differences in genes, even for heritable traits, only explain the
variance in traits across a population; they are by no means
independent causes for any trait in individuals and variation in the
environment also accounts for part of the variation in any trait
(Wilson, 1978, 19). In at least one paper responding to the SSG Wilson
says that, on the question of the relative contributions to the
variation in human behavior from variation in genes vs. variation in
the environment, his "own views lie closer to the
environmentalist than the genetic pole" (Wilson, 1976, 183).
Wilson also does seem to be trying to support his claim that there are
some human behaviors which are probably highly heritable: he describes
a variety of different sorts of evidence that might identify them.
This evidence includes cross cultural appearance (e.g. Wilson, 1975,
550; Wilson, 1978, 20, 129); plausible homology with other closely
related species (especially chimpanzees) (e.g. 1978, 20, 27, 151);
early development of the trait in question (e.g. 1975, 551; 1978,
129); differences between individuals that arise without differences
in their developmental environment (e.g. 1978, 128-130); genetic
syndromes that cause behavioral differences (e.g. 1978, 43-45);
and twin studies (e.g. 1978, 145). Finally, Wilson claims that trying
to change human behavior from its heritable form usually fails or
causes misery (Wilson, 1978,
 20)[6];
 he describes the failures of certain attempts to change the features
of normal human behavior by massively changing the social environment,
such as the persistence of family ties under slavery (Wilson, 1978,
136) and in the Israeli kibbutzim (1978, 134). Of course, whether or
not all of the above is good evidence for his claims is very much up
for debate (Kitcher, 1985; Sociobiology Study Group of Science for the
People, 1976). It is worth bearing in mind that while Wilson thinks
the evidence that some human behaviors are heritable is overwhelming
(Wilson, 1978, 19) he does see many of his specific proposed
evolutionary explanations as preliminary and speculative rather than
fully formed (for example, Wilson is explicit that his discussion of
homosexuality is preliminary: 1978, 146). For more discussion of the
problems relating to heritability when studying the evolution of
behavior, see section 4.2. below and the entry on
 heritability.



*Ignoring learning and culture*. As a concomitant of the
objection that Pop Sociobiology was committed to genetic determinism,
its central players are also often accused of being insensitive to the
problem of learning and culture, i.e. to the problem that many traits
in which they are interested are simply not subject to natural
selection at all, and that this state of affairs may indeed be common
in humans (Kitcher, 1985; Sociobiology Study Group of Science for the
People, 1976). However, Wilson, for example, clearly recognized the
important role of culture in many behavioral traits (Wilson, 1976);
indeed, he thought that even minor genetic differences that made a
difference in behavior could be exaggerated by acquired
culture--this is the so-called "multiplier effect"
(although it is seriously in question whether the multiplier effect
works - Maynard Smith and Warren, 1982). Furthermore, partly in
response to these concerns on the part of his critics Wilson
eventually went on to publish *Genes, Minds and Culture* with
Charles Lumsden (Lumsden and Wilson, 1981), which was an attempt to
consider the effects of cultural transmission on the nature and spread
of behavioral traits, and of the interaction between genes and
culture. The book, however, was subject to heavy criticism (see, for
example, Kitcher, 1985; Lewontin, 1981; Maynard Smith and Warren,
1982). The main concern raised was that there was little substance in
the models the book provided--the most interesting features of
these simply followed from the assumptions built into them, in
particular, assumptions about the degree to which genes kept culture
"on a leash" (Lumsden and Wilson, 1981, 13; Wilson, 1978,
167).



*Strong adaptationism.* The third problematic feature ascribed
to Pop Sociobiology was its reliance on an overly strong form of
adaptationism. In both papers by the SSG (1976) and by Gould and
Lewontin in their famous "Spandrels of San Marco" paper
(Gould and Lewontin, 1979), the critics of sociobiology argue that
sociobiologists are committed to a "Panglossian"
adaptationism. While the "Spandrels" paper is directed at
"adaptationists" generally, sociobiologists were some of
its clear targets (for example, David Barash's (1976) work on
jealousy in male bluebirds).



The central accusations of the "Spandrels" paper were as
follows: that adaptationists treat all traits as adaptations; that
when "atomizing" individuals into traits to study they
take no care to establish that the traits so atomized could actually
independently evolve by natural selection; that they ignore
developmental constraints on evolution; that they fail to identify
traits that are prevalent due to causes other than natural selection;
that they fail to distinguish between current adaptiveness and a past
history of natural selection; that they generate adaptationist
hypotheses, fail to test them properly and replace one such hypothesis
with another, ignoring other interesting kinds of evolutionary and
non-evolutionary explanation. Instead, according to Gould and
Lewontin, adaptationists tell purely speculative, untestable
"just so" stories and present them as science fact.



Again, insofar as Wilson and other sociobiologists are being purely
speculative this criticism may be warranted: quite a lot of the
evolutionary explanations of particular human behaviors Wilson
describes in the first and last chapters of *Sociobiology* and
in *On Human Nature* *are* speculation on his part
(although not entirely speculation). Perhaps the speculative
adaptationist stories are appropriately described as "just so
stories"; the question is whether such stories, *treated*
as preliminary hypotheses, are problematic in themselves. Furthermore,
while Wilson made no attempt to test any of his speculative
hypotheses, behavioral ecologists do try to test adaptationist
hypotheses about humans and other animals. Again, the proper question
is whether these tests are appropriate or sufficient to establish the
truth of the hypotheses in question. Gould and Lewontin do, however,
make some more sophisticated objections to adaptationist methods; some
of these will be discussed in Section 4.


## 3. Sociobiology as Human Behavioral Ecology



Human behavioral ecology (HBE), or human evolutionary ecology, is the
current evolutionary social science most closely related to
Wilson's sociobiological project; it is the project that is
sometimes still referred to as "sociobiology" by some
philosophers of science (Griffiths, 2008; Sterelny and Griffiths,
1999). "Sociobiology" is most often used this way as a
term of contrast with "evolutionary psychology", another
current evolutionary social science project inspired by early
sociobiologists, and also much developed from how early sociobiology
was conceived: see the entry on
 evolutionary psychology
 for a discussion. Other common names for HBE are "evolutionary
anthropology" (Smith, 2000) or "Darwinian ecological
anthropology" (Vayda, 1995) (due to most of its practitioners
having a background in, or being based in anthropology departments,
and using anthropological fieldwork as the main means of testing their
hypotheses about human behavior). The different names tend to be used
when the researchers concerned are emphasizing the connections of
their field with anthropology or with non-human behavioral ecology.
HBE has a great deal in common with the non-human behavioral ecology
described above. In particular, it shares its focus on behavior,
rather than the psychological mechanisms described in evolutionary
psychology. Unlike non-human behavioral ecology it has continued to
use Grafen's (1984) phenotypic gambit, in that its practitioners
usually do not attempt to discover or describe the genetic or other
resources employed in the development of the behavior in which they
are interested; nor, for that matter, do they usually attempt to
discover the underlying psychology. There are, however, some
differences of emphasis, in that the questions about human behavior
addressed by the human behavioral ecologists (HBEs) are sometimes
different from those addressed by the non-human behavioral
ecologists.



To understand the purposes of the HBE project, let's consider one
of its classic examples: Kaplan and Hill's (1992) work on prey
choice strategies amongst the Ache foragers of Paraguay. Just as in
non-human behavioral ecology, behavioral strategies in HBE are usually
described as complex behavioral dispositions. Behavioral dispositions
involve behavioral responses to local stimuli; behavioral strategies
then involve producing a set of different responses to a set of
different stimuli (i.e. the *response conditions* of the
strategy). According to Kaplan and Hill, the Ache prey choice strategy
involves choosing a variety of different potential prey items from the
environment; whether or not a prey item is taken depends on a number
of circumstances acting as the response conditions: for example, the
presence of prey with certain specific features, such as the caloric
return of the prey given the time necessary to process it (known as
the profitability); the rate at which that prey occurs in the
environment; whether or not the prey is encountered on their search;
and the search time available on a foraging trip. HBEs usually
describe behavioral strategies in terms of an "epigenetic"
or decision rule, which is usually given as a mathematical function
mapping values for the response conditions in the environment onto the
appropriate values for the parameters of the behavioral output. Kaplan
and Hill's work also provides such an epigenetic rule (see
Kaplan and Hill, 1992, 170), which describes the relationships between
search time, profitability and so on, to decide which prey will be
taken on encounter when the Ache are out foraging. Kaplan and
Hill's observations suggest that, on the whole, the Ache are using
a strategy which is close to the maximally adaptive strategy suggested
by their prey choice model. The question, then, is how to interpret
Kaplan and Hill's method; what is the purpose of showing that the
Ache have a strategy of this kind?



In a few places, remarks by human behavioral ecologists suggest that
the purpose of HBE is simply to demonstrate that human behavior is
maximally adaptive: for example, Smith et al. (2001, 128) claim that
"... human behavioral ecology applies the theoretical perspective
of animal behavioral ecology to human populations, examining the
degree to which behavior is adaptively adjusted to environmental
(including social) conditions". One possible interpretation of HBE
work, therefore, is that they test the hypothesis that human behavior
is adaptive (in contrast to the hypothesis that it consists of
adaptations). By using methods derived from non-human behavioral
ecology (such as optimality and game theoretic models), HBEs can
demonstrate that the behaviors humans actually engage in tend to be
optimal relative to the constraints and tradeoffs acting on them (i.e.
they are "locally optimal"). Kaplan and Hill seek to
demonstrate that the Ache's prey choice behavior is in fact
adaptive, as do other HBE studies that use the same method. On this
interpretation, an important purpose of the project is to deflect some
of the criticisms directed at Pop Sociobiology: HBEs explicitly accept
that social learning of general purpose reasoning may be responsible
for human behavioral strategies such as the Ache's. However, this
is ultimately irrelevant; one way or another, natural selection has,
in effect, "seen to it" that humans behave in ways that tend
to maximize their reproductive success. This is also consistent with
the HBEs' emphasis on the phenotypic gambit.



Alternatively, however, one could take these remarks to be a
description of the HBEs primary method rather than the nature of their
hypotheses, and that their hypotheses are (as the above quote also
suggests) similar to those of non-human behavioral ecology. This is
consistent with other theoretical discussions of HBE work including
some by the same authors--see for example, Irons (1998), Smith
(2000), Winterhalder and Smith (1992). On this interpretation, the
purpose of Kaplan and Hill's work is to test the hypothesis that
humans have a behavioral adaptation for prey choice, of which the
Ache's prey choice strategy is only a local
manifestation. Showing that the Ache's behavior is highly
adaptive is supposed to be a local test of the hypothesis: the Ache
are a group that have to engage in prey choice and hence it is
possible to test for a human behavioral adaptation in this context. By
confirming this hypothesis, Kaplan and Hill can then achieve two
further goals: they can determine which conditions led to the
evolution of the larger prey choice strategy and, by confirming a
functional description of that strategy, they can determine what
causes the Ache (specifically) to choose the prey they do in their
local environment.



On this interpretation, the prey choice strategy as a whole (i.e. not,
for example, the *Ache's* specific, locally appropriate
set of prey choices, but the general human prey choice strategy of
which they are a manifestation) is presumed for heuristic purposes to
be an adaptation to certain conditions in the past that led to that
strategy being selected for; i.e. the *selection conditions*
for the strategy. Supposing that it is reasonable to take behavioral
strategies as such to be able to be adaptations (see the later
discussion in section 4) the selection conditions of a given
behavioral strategy will usually include the response conditions
(because presumably it takes the production of overt behavior in order
for selection to act on a behavioral strategy) but possibly also
features of the larger context which made it highly adaptive to
respond in that way to those response conditions. In other words, in
the prey choice case, profitabilities, prey densities and search time
availability would presumably have been among the selection conditions
of a prey choice strategy (presuming it is an adaptation). But so
would larger details about the environment not explicitly included in
these models, such as the limits on human capacity which determine
which prey are accessible in that environment, the ecology which
determines which prey are in the environment, and so on. On this
interpretation, therefore, HBEs are interested in identifying the
selection conditions of human behavioral strategies; this parallels
standard interpretations of non-human behavioral ecology described
earlier.



However, HBEs are anthropologists, and hence also want to describe the
local causes of the overt behaviors they observe people engaging in in
their fieldwork; this can be done by identifying the local
manifestations of the response conditions of the strategies those
people are using. Identifying these response conditions is a matter of
identifying the correct functional description of those strategies
(Kitcher, 1987). So how might such strategies he described? It is
worth pointing out that this is quite difficult to do: what HBEs
observe in the field is sets of overt behaviors in a context of a
variety of ecological conditions any of which could be the response
conditions. It may be far from obvious exactly why those behaviors are
occurring, and which local conditions are the stimuli to which the
behavior is a response. Indeed, it may not even be obvious which overt
behaviors are manifestations of the same strategy. In the Ache case,
what Kaplan and Hill observed is not a complete prey choice strategy,
but a variety of occasions on which individuals or groups of Ache
people took or did not take prey they encountered whilst out foraging,
among many other sorts of foraging and other types of behaviors. The
question is which, if any, of the overt behaviors on these occasions
manifested a single prey choice strategy, and how these overt
behaviors are related to each other and to the environmental
conditions in which they occur. If human behavioral strategies are
adaptations, however, then the relationships between behavioral
responses and local ecological conditions that resemble those of the
human evolutionary past can be expected to be locally optimal,
*ceteris paribus*; this means that the response conditions of
the strategy will (allegedly) be those (along with additional
plausible selection conditions) that made the behavior *fitness
maximizing* in the environment in which it evolved, and in any
environment that is relevantly similar (Irons, 1998). This permits the
HBEs to pick out the correct description of the strategy using an
optimality model; identifying the causes of the Ache's behavior in
particular is a matter of identifying how the response conditions of
that strategy manifest locally in their environment. 



HBEs, like behavioral ecologists studying non-human animals, tend to
use optimality modeling to find strategy descriptions and sets of
plausible selection conditions that make sense of observed patterns of
behavior as locally optimal adaptations, and the reasoning works in
much the same way. However, there are a few differences, most notably
in how models are chosen. In cases where the structure of the problem
might be unique to the human case and where the current environment is
expected to be different from the situation under which the strategy
originally evolved, the model HBEs choose will often be unique and at
least some of the proposed selection conditions identified by
appealing to information about the fossil record. A nice example might
be human life history, where the human situation is relatively unique:
for example, compared to other primates humans have unusually long
lives and childhoods, and long life after menopause. As a consequence,
the human behavioral ecologists have to appeal to the fossil record in
detail to determine what sorts of evolutionary transitions might have
been involved (Hawkes, 2003; Kaplan et al., 2000). Where the structure
of the adaptive problem humans face and the conditions acting on their
behavior is expected to mirror those in non-human animals and to be
very similar to those humans encountered in their evolutionary past,
the choice of model is often a standard one from non-human behavioral
ecology; the proposed selection conditions can be based on the current
conditions observed in foraging societies. In the Ache foraging case,
this is exactly what happens: the prey choice models used by Kaplan
and Hill are those used to understand similar sorts of strategies in
non-human animals. This is because Kaplan and Hill expect the relevant
conditions acting on human prey choice--such as profitabilities and
search times--to mirror very closely those acting on non-human
animals.



Some differences also arise in how models are tested in HBE verses
non-human animal behavioral ecology. The description of that strategy
picked out by the model will usually include descriptions of potential
behavioral responses to conditions (or values for parameters of those
responses) that go beyond what has already been observed; this means
the model predicts that these responses should also occur if the
description of the strategy is correct. For example, in Kaplan and
Hill's prey choice case, the model predicts patterns of Ache
prey choice that the observers had not yet seen, such as which prey
the Ache should and should not take on encounter and under what
circumstances. The model, therefore, can be tested by looking for a
situation in which the response conditions of the strategy obtain and
observing whether the behavior in response to those conditions is as
the model suggests. This is partly why such rules are tested in
foraging societies--because many of these strategies have
response conditions which reflect conditions presumed to be present in
the human evolutionary past, and which may obtain in foraging
societies but not in industrial of agricultural societies. For
example, obviously in Kaplan and Hill's foraging case, few if
any industrial or agricultural societies routinely engage in foraging
that is a primary source of nutrition, and hence don't present
an opportunity for individuals to *do* prey choice of the right
type. The other reason for performing these tests in foraging
societies is because the HBEs want to understand the local causes of
overt behavior in these societies in particular.



However, just as in non-human behavioral ecology, differences between
the predicted and described behavioral strategies require scientists
to build new models, or suggest additional conditions or constraints
to add to the original models; there must be independent evidence that
these conditions or constraints obtain. Kaplan and Hill's
observations do depart from what their model predicts: the Ache engage
in a number of prey choice decisions that are not obviously fitness
maximizing. In particular, men often seem to ignore many calorie rich
food sources from plants and sometimes smaller animals, and women do
not pursue larger game. The question then is how to proceed: HBEs
often suggest changes to the model that might account for these
failures of prediction; often, they do give some independent evidence
for their suggestions. For example, one of Hawkes' proposed
explanations for why male hunting behavior often fails to meet prey
choice expectations (similar failures are found in many societies
besides the Ache) is that men pursue large game for reasons other than
merely collecting calories--they are also interested in showing
off in order to get other fitness rewards, such as additional sexual
partners or better alliances with other men. Hawkes was able to show
that men's prey choice decisions were consistent with this view
(Hawkes, 1991).


## 4. Central criticisms of Sociobiology and Behavioral Ecology



There are a number of philosophical criticisms of behavioral ecology
and its methods; this section will address some of these
criticisms.


### 4.1 Adaptationism



Perhaps the most important of all of the criticisms of "Pop
Sociobiology" was that it was excessively adaptationist; similar
sorts of criticisms are leveled at modern descendants of sociobiology,
such as behavioral ecology. Behavioral ecologists, including HBEs, are
really methodological adaptationists (Godfrey Smith, 2001), in that
they assume that natural selection is optimizing the trait they are
studying as a heuristic, in order to establish other things about that
trait; as such, no strong commitment about the power of natural
selection is necessarily required on their part (as discussed
earlier). This did lead many behavioral ecologists to regard Gould and
Lewontin's (1979) criticisms as a cautionary tale, rather than
as properly directed at them--see, for example, Gould and
Lewontin's objection that adaptationist hypotheses were
untestable, which the behavioral ecologists could easily rebut (Mayr,
1983). Similarly, Parker and Maynard Smith (1990) responded to Gould
and Lewontin's objection that adaptationists do not properly
account for phylogenetic and developmental constraints; Parker and
Maynard Smith argued that they are taken into account--even where
developmental constraints and tradeoffs are not explicitly represented
in optimality models, they are often built into the strategy set or
are otherwise implicit in those models. However, it is reasonable to
point out that Parker and Maynard Smith's paper did not fully
respond to Gould and Lewontin's objection: Gould and Lewontin
recognized that adaptationist models appeal to constraints; their
worry was that such constraints are appealed to *ad hoc* to
fill in gaps in models, and are not subjected to any external
test.



Another objection to adaptationist methods from Gould and Lewontin
that has persisted as a criticism of behavioral ecology is that these
methods do not allow scientists to consider non-adaptationist
explanations for the traits to which they are applied, such as whether
those traits were fixed by drift or are simply side effects of other
traits (i.e. whether they are "spandrels"). In principle,
correctly pursued, adaptationist methods can help identify cases where
a trait is a non-adaptation: drift, for example, can be identified by
comparing the distribution of traits expected under selection and
under drift with actual population distributions (Sober, 2005); the
question is whether the types of methods used in behavioral ecology
are the most efficient at detecting these cases (Lewens, 2009). Some
philosophers have argued that methodological adaptationism is more
pernicious in practice than it looks in principle, because real
evolutionary social scientists are not good at dropping adaptationist
hypotheses for a trait even when there is a strong case to be made
that they should (see, for example, Lloyd, 2005, esp. Chapter 8). For
further discussion of all these problems, see the entry on
 adaptationism.


### 4.2 The Heritability of Behavioral Traits



While it seems that the accusation that the early "Pop"
sociobiologists were genetic determinists was probably unfair, there
is a related objection that can be raised to both "Pop"
sociobiology and to the later forms of human and non-human behavioral
ecology, i.e. that any trait's being an adaptation requires that
that trait be *heritable*, and most human behaviors are not
heritable. To say a trait is heritable in the simplest sense is just
to say that if the parent has that trait, then the trait tends also to
appear in the offspring (i.e. to say the trait is heritable simply
means that the trait is *inherited reliably*). The more
demanding population genetic definition of heritability is that a
heritable trait *T* is one where variation in *T* can be accounted for
primarily by variation in genes as opposed to variation in the
environment (see also the entry on
 heritability).
 Heritability in this sense is supposed to be required for natural
selection because in order for natural selection to spread a variant T
in a population, when *T* increases the average number of offspring of
its possessors, those offspring have to reliably also have *T* if *T* is
to spread at the expense of the other variants. The problem, however,
is that many human behavioral traits do not seem likely to be
heritable in this way: they tend to vary greatly across and even
within cultures and environments, whereas human genetic variation is
much too low to account for such differences (Buller, 2005; Cosmides
and Tooby, 1987).



However, HBEs can get around this problem, by pointing out that local
patterns of overt behavior are manifestations of more general
strategies; differences in the environment cause the manifestations of
different elements of these complex behavioral dispositions humans
possess. For example, the patterns of foraging behavior of the Ache
people in the Paraguay rain forest (Hill and Hurtado, 1996) and the
Inuit in the Arctic (Smith, 1991) are very different, and the genetic
differences between these groups are insufficient to explain them.
However, both could be simply local manifestations of a larger and
more general foraging strategy (or strategies) which humans possess,
which could be heritable and an adaptation. A behavioral strategy is,
after all, simply a complex behavioral disposition, which involves
responding in a variety of specific ways to a set of environmental
cues, most of which would be achieved by having an appropriate
psychological mechanism or mechanisms underlying the set of
dispositions. In which case, heritability of a behavioral strategy
only depends on there being a psychological mechanism or mechanisms
that produces that strategy reliably, and that mechanism's
itself being heritable. Of course, whether there are such heritable
mechanisms for the behavioral strategies in which the HBEs are
interested is likely to be a matter of some controversy.



What's more, some philosophers have argued that it is possible
for traits to be adaptations in the standard sense even when they are
not heritable according to the population genetic
 definition[7].
 Despite the claim above that heritability in the population genetic
sense is required as a condition of the action of natural selection,
technically all that is required for natural selection to occur on a
trait *T* is for *T* to be heritable in the weaker sense, i.e. that it be
robustly transmitted, such that the trait variant in a parent tends to
turn up reliably in the offspring. The reason heritability in the
population genetic sense was believed to also be necessary for natural
selection was that genes were believed to be the only developmental
resource transmitted to offspring, so only if variation in traits
followed variation in genes would traits be subject to natural
selection for the reasons described above. However, recently a variety
of philosophers and scientists have argued (Odling-Smee et al., 2003;
Sterelny, 2003, 2007, 2012) that natural selection can occur on traits
even if traits vary most with the environment rather than genes,
*so long as environments can themselves be transmitted down
lineages*; Sterelny's suggestion is that this might be
achieved by robust niche construction. This has an interesting
consequence: if highly reliably transmitted cultural traits could be
subject to natural selection, standard evolutionary methods and models
of the sorts used in behavioral ecology could be used to understand
the evolution of such traits.



This is the not the end of the problem, however. Some philosophers
have argued that not all traits that are culturally transmitted or
learnt can be properly understood using adaptationist methods, because
many of these traits are not heritable even in this weaker sense, and
hence cannot be adaptations (Driscoll, 2009; Driscoll and Stich, 2008;
Kitcher, 1990). Worse, such traits could appear highly adaptive on
evolutionary models. For example, traits which are subject to highly
adaptive individual learning or adaptive social transmission processes
in populations (Henrich and Boyd, 1998; Henrich and Gil-White, 2001)
are nevertheless not adaptations because they are not shaped by
natural
 selection[8].
 This is because in many of these cases, the features of the
environment that make the trait appear adaptive may not actually have
featured as selection conditions in the causal history of the trait
(or perhaps as causes in any sense). In such cases, evolutionary
methods popular in sociobiology and the current evolutionary social
sciences (such as optimality modeling) will make traits appear to be
adaptations to those conditions when they are not. For a more detailed
discussion of dual inheritance theory, gene culture co-evolution and
the associated theory, see the entry on
 cultural evolution.


### 4.3 Behavioral vs. Psychological Focus



Another problem for behavioral ecology and sociobiology is their focus
on trying to understand the biological basis of *behavior* as
such. The behavioral focus made sense to those behavioral ecologists
influenced by Lorenz and Tinbergen's ethology, but once
cognitive psychologists became interested in applying evolutionary
thinking to their work, the effects of the cognitive revolution in
psychology began to have an effect on some of the
"sociobiological" thinkers, and they transformed
sociobiology into evolutionary psychology (Cosmides and Tooby, 1987;
Tooby and Cosmides, 1990). The result of the cognitive revolution in
psychology was that many psychologists came to regard the proper
target of explanation in psychology to be genuinely psychological
states or mechanisms rather than behavioral dispositions (as in
Skinnerian Behaviorism) (Chomsky, 1959). In cognitive science since
the middle of the twentieth century, psychological states and
mechanisms have largely been understood in computational and
materialist terms, that is, that the mind is the brain, and that brain
states and mechanisms are essentially computational states and
computers respectively (though almost certainly not serial computers).
Psychological descriptions, then, are simply descriptions of these
brain systems in computational or information-processing terms;
generally they appeal to representations, decision rules and
algorithms that brain systems process. The shift in methodology and
theory represented by this change in approach was extremely
significant. But it also appears to have made cognitive psychologists
interested in evolution averse to thinking of behavioral dispositions
as proper targets of evolutionary explanation, just as they were
averse to thinking of them as the proper targets of psychological
explanation (Cosmides and Tooby, 1987). This issue never seems to have
arisen for the human behavioral ecologists; indeed, not only is
behavior treated as the only proper target of evolutionary
explanation, but psychology is explicitly ignored in favor of behavior
for methodological reasons--the focus on behavior is part of the
"phenotypic gambit" (Grafen, 1984) which (as described
above) simplifies evolutionary modeling and the process of deriving
explanations from it in human behavioral ecology.



The importance of the issue to the evolutionary psychologists has led
to a series of arguments traded between the human behavioral
ecologists and evolutionary psychologists for preferring behavior over
psychology and vice versa. Two main arguments have been raised in
favor of considering behavior the proper target of explanation, both
from. The first is purely practical: behavior is relatively
straightforwardly observable whereas psychological mechanisms are not,
to the extent that the nature of only a few psychological mechanisms
has been uncontroversially demonstrated (one of the few examples might
be the mechanisms for learning language) (Alexander, 1990). The second
is that only behavior can be an adaptation because only behavior is
the actual causal nexus between the organism and its environment
(Alexander, 1990; see the same idea in early form in Skinner,
1984).



The central problem with both of these arguments is that, while they
are true of overt behavior, they are not true of the behavioral
dispositions or strategies (complex behavioral dispositions) which are
the actual targets of explanation in behavioral ecology--or at
least, no more true than of psychological mechanisms. Behavioral
dispositions do not causally interact with the environment except
insofar as they lead to the actual manifestation of overt behavior;
they are also no more "straightforwardly observable" than
psychological mechanisms since they cannot be observed until overt
behavior in manifested, and even then distinguishing between different
strategies with overlapping component behavioral dispositions is also
difficult.



Arguments for the claim that only psychological mechanisms should be
considered to be adaptations rest on the idea that behavior is really
only ever a manifestation of the underlying psychology. Behavior is
not an adaptation so much as it is the effect of an adaptation.
Cosmides and Tooby (1987) also argue that the really interesting
evolutionary generalizations emerge at the level of psychology, not
behavior. Again, however, this argument depends on understanding
"behavior" as "overt behavior", individual
chunks of physical activity that are not necessarily reproduced over
time and which do not occur in evolutionary social science
generalizations, verses understanding "behavior" as
"complex behavioral strategies", which do seem potentially
transmissible (via the psychological mechanisms that support them). It
is also notable that such strategies are the subject of a significant
evolutionary literature--such as evolutionary game theory, on
which Cosmides and Tooby themselves depend: the argument for expecting
their famous "Cheater Detection" module (Cosmides, 1989;
Cosmides and Tooby, 1992) is derived from Axelrod and Hamilton (1981)
and Trivers' (1971) work showing that TIT FOR TAT, which
requires its players to be able to detect cheaters on reciprocally
altruistic interactions, is an evolutionary stable
 strategy[9].



More recently, philosophers have also presented some arguments for one
side or the other of this issue. Buller (2005, 50-52), for
example, argues that behaviors cannot be adaptations because they are
not heritable, whereas psychological mechanisms are. However,
Buller's discussion does not make the distinction between overt
behaviors and behavioral strategies described above. Buller argues
that behaviors could disappear from the population for generations if
the necessary response conditions never arose, but yet still emerge
again if the stimulus reappeared, and this suggests that these
behaviors are not inherited as such rather than the underlying
psychological mechanism. In this he is right as long as he means the
overt behaviors; behavioral dispositions or strategies could also
remain present and be inherited in the absence of the response
conditions. Moreover, Buller's description of a
"psychological mechanism" in this context sounds rather
like a behavioral disposition (2005, 52-53).



Another argument in the philosophical literature for thinking that
behaviors are not the proper targets of natural selection explanations
is that behaviors are not *quasi-independent* (Lewontin, 1978)
in the way they need to be to evolve by selection in their own right
(Sterelny, 1992; Sterelny and Fitness, 2003; Sterelny and Griffiths,
1999). This is because many behavioral strategies will depend on
multi-purpose mechanisms that cannot change during evolution without
those changes ramifying to the other strategies those mechanisms
produce. However, Driscoll (2004) argues that this is not necessarily
the case; multi-purpose mechanisms, in order to be able to produce
more than one strategy, would have to have branching algorithms;
variation in any of these mechanisms necessary to generate variation
in any one strategy need only occur on the branch relevant to the
strategy in question and need have little or no effect on the other
branches. Instead, whether an evolutionary explanation is properly
directed at the behavioral or psychological level depends on the
case.


## 5. Conclusion



Sociobiology, despite its complicated history, remains of interest to
philosophers and has some import for certain important philosophical
debates. One such question is whether human beings should be
understood to have a *nature*, a set of traits which for Wilson
in particular are those heritable traits that have been fixed in the
population by natural selection (Wilson, 1978). Consequently, this
'nature' can be discovered and understood using the
standard adaptationist methods used in other areas of biology. Most
importantly, Wilson suggests that some of the characteristics that
make up human nature are specifically *behavioral*.



Quite apart from the fundamental interest of the question of whether
there is a human nature, the issue is important because it might have
a significant moral or social upshot: what society we can have, and
indeed what society we should have might depend on what human nature
is like (Wilson, 1978). It was this concern that ignited the
"sociobiology wars" in the early days after the
publication of *Sociobiology*. The "Sociobiology Study
Group" was concerned that Wilson was trying to argue that many
problematic or harmful features of current societies, such as
oppressive gender roles, negative race relations and interpersonal
aggression might be unchangeable (Sociobiology Study Group of Science
for the People, 1976). Philosophers of biology have strongly resisted
the idea that humans have a 'nature' in anything like the
traditional sense of a fixed essence (Hull, 1986; Lewens, 2012; Lloyd
and Crowley, 2002) but there is also some debate about whether humans
could be said to have a nature in the sense of a set of evolved traits
in much the way that Wilson suggests (e.g. see Machery, 2008, 2012;
for a critique see Powell, 2012). Philosophers in this area are
instead focusing on notions of human nature that take into account the
flexibility of human development and the capacity of human beings to
construct their own development and hence their own
'nature' (Griffiths, 2009; Ramsey, 2013; Stotz, 2012).



Another hope on the part of philosophers is that understanding the
evolution of cognition might give us some insight into the nature of
certain human psychological traits that have particular philosophical
interest. One such trait is our moral psychology. Moral psychology is
of interest to philosophers who hold naturalistic views of ethics
because they believe moral values depend in part on features of that
psychology; understanding that psychology and how it evolved would
give us insight into what the correct moral values are. Understanding
the origins of human moral psychology might also help answer certain
metaethical questions (Street, 2006). As Wilson hoped, scientists
working in disciplines which are the modern descendants of
sociobiology have contributed to our understanding of the way that
norms, including moral norms, might have become established in human
evolution (see, for example, Henrich and Boyd, 2001; Sripada, 2005).
Philosophers still strongly disagree, however, on how the evolution of
moral psychology, especially for the acquisition of norms, should be
understood (Dwyer, 2006; Sripada and Stich, 2006; Sterelny, 2010).



Other debates surrounding sociobiology are still ongoing. For example,
while methodological adaptationism has become and remained the
standard approach in behavioral ecology, not all philosophers are
convinced that this is an entirely benign practice - there are
still concerns about the assumptions that this methodology requires
(see, for example, Lewens, 2009; Lloyd, 2005). Similarly, there has
been an increasing interest in the role of culture in the nature and
history of human behavior; work studying the evolution of culture has
increased since Lumsden and Wilson (1981) published their book.
Philosophers and scientists are still addressing questions about how
and how far cultural traits can be said to evolve; and, as discussed
above, whether traits that have evolved in this way can be considered
adaptations in any sense (Driscoll, 2011; Fracchia and Lewontin, 1999,
2005; Henrich et al., 2008; Sperber, 2006; Sterelny, 2006).