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Animal Behavior


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01/26/2018 - RS0000000000000000000000396801 (Laela Sayigh) - Animal Behavior 10e
1 An Introduction to
Animal Behavior

The discipline of animal behavior is growing rapidly,

thanks to thousands of behavioral biologists who are
exploring everything from the genetics of bird song
to why women find men with robust chins attractive. A
major reason why the field is so active and broad ranging has to do
with a book published over 150 years ago, Charles Darwin’s On the
Origin of Species.8 As soon as it appeared, scientists realized that
the evolutionary theory of natural selection provided a revolution-
ary way of looking at all living things. Darwin’s influence continues
strongly to this day, which is why this book is entitled Animal Behav-
ior: An Evolutionary Approach.
Knowing that animal behavior, like every other aspect of living
things, has a history guided by natural selection is hugely important.
An understanding of evolutionary theory means that we have a sci-
entific starting point when we set out to determine why animals do
the things they do—and why they have the genetic, developmental,
sensory, neuronal, and hormonal mechanisms that make these be-
havioral abilities possible. As the evolutionary biologist Theodosius
Dobzhansky said long ago, “Nothing in biology makes sense except
in the light of evolution.”11
I hope to explain why Dobzhansky was right. If I succeed, my
readers may come to understand the appeal of the evolutionary ap-
Charles Darwin’s study
in Down House where he proach to animal behavior, which helps scientists identify interesting
developed the theory of
evolution by natural selec- subjects worthy of explanation, steers them toward hypotheses suit-
tion, the foundation for the able for testing, and produces solid conclusions about the validity of
modern study of animal
behavior. these hypotheses.

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The Behavioral Ecology of a Digger Bee

I put an evolutionary approach to animal behavior to work after I moved to
Arizona in the early 1970s and began to explore the desert near my hometown
of Tempe. At that time, on the advice of a colleague, I drove out to the Blue
Point Bridge where a sandy floodplain created by the Salt River had been
colonized by a forest of mesquites. As I wandered among the scattered mes-
quites and paloverdes bordering the river, I came to a large open area where
hundreds, perhaps thousands, of large gray bees were cruising noisily close to
the ground. Although I had been trained as an ornithologist, I had also learned
that insects are delightful, so I stopped to admire the bees as they zoomed this
way and that.
Soon I noticed a bee that had landed on the ground and was digging ener-
getically, using its jaws to loosen the sandy soil and its hindlegs to propel the
debris away from the depression it was creating (Figure 1.1). The bee paid no
attention to me as I came closer but continued to dig as if its life depended on
it. I had read about female bees that tunnel into the ground, creating a nest
burrow with chambers for their offspring and the provisions that the larvae
will feed upon. Therefore I assumed that I had stumbled upon a place where
a great many females were searching for nesting sites and that the bee in front
of me was a female in the process of burrowing underground.
But my tentative explanation for the bee’s behavior received a jolt when the
digger bee stopped digging after a few minutes and drew back slightly in the
shallow pit that it had dug. Shortly thereafter another bee scrambled out of the
opening underneath the waiting gray bee. The ex-digger immediately clam-
bered onto the back of the emerging bee, with which it mated very quickly
(Figure 1.2A). The two bees then flew off together, the one above holding on
to its partner, before coming to rest on a nearby mesquite (Figure 1.2B). As
the lower bee (which was much darker than its mate) clung to a branch tip,
the upper bee proceeded to stroke its partner with its middle pair of legs and
antennae. When I came closer, I could hear a faint intermittent buzzing that
occurred in rhythm with the leg strokes and antennal taps.
I was intrigued. The digger bee was obviously a male, not a female, and he,
and others like him that I observed subsequently, clearly possessed the abil-
ity to detect emerging females below the soil’s surface. How on earth could a

FIGURE 1.1 A bee, Centris pallida, digging in the

ground. Photograph by the author.

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(A) (B)

FIGURE 1.2 Sexual behavior of Cen-

tris pallida. (A) A male copulating with
male bee know exactly where a female was tunneling upward so that he could a female that he had discovered before
meet her by digging down through a centimeter or two of hard-packed soil? she emerged from the ground. (B) After
the female was inseminated, the pair
And why had males of this species (which I later learned was called Centris flew to a nearby mesquite tree, where
pallida) acquired this extraordinary ability? the male engaged in postcopulatory
With respect to the first question, I guessed that digging males could some- courtship with his partner. Photographs
how smell or hear females that had burrowed up close to the surface. You can by the author.
imagine, perhaps, how I might have determined which of these speculations
was correct, research that required me to bury dead female bees in an area
being searched by patrolling males.1
But although I was interested in the sensory abilities that enabled male bees
to find emerging females, I also wanted to learn why male bees of this species
searched for and dug down to meet these females. I did not know a lot about
male bee behavior at the time, but I did know that males of many bee species
mated after finding receptive females at flowers. In “my” bee, males could
find adult females that had yet to fully emerge. There is a puzzle here. Since
finding newly metamorphosed females is only one of several mate-locating
tactics used by sexually motivated male bees, why had males of Centris pallida
settled upon the “find buried females” routine?
When behavioral ecologists, like me, ask questions of this sort about the
behavioral abilities of an animal species, they are inspired by Darwin’s theory
of evolution by natural selection, which argues that living species are the
product of an unguided, unconscious process of reproductive competition
among their ancestors. As Darwin explained, if in the past some individu-
als left more descendants than others because of their distinctive hereditary
attributes, then these reproductively dominant individuals would inevitably
gradually reshape their species in their image. So, if males of a proto–Centris
pallida varied in their mate-finding behavior, and if males could transmit their
particular tactic to their descendants, then over time, the one behavior that
was most successful in helping individuals pass on their hereditary makeup
would come to dominate the species.
The logic of natural selection is such that evolutionary change is inevitable
if just three conditions are met:
1. Variation, with members of a species differing in some of their

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2. Differences in reproductive success, with some individuals having more

surviving offspring than others in their population, thanks to their
distinctive characteristics
3. Heredity, with parents able to pass on some of their distinctive charac-
teristics to their offspring
If there is hereditary variation within a species (and there almost always is)
and if some hereditary variants consistently reproduce more successfully than
others, then the increased abundance of living descendants of the more suc-
cessful types will gradually change the species. The “old” population evolves
into one whose members possess the traits that were associated with success-
ful reproduction in the past.
Because the process that causes evolutionary change is natural, Darwin
called it natural selection. Darwin not only laid out the logic of his theory
clearly but also provided abundant evidence that hereditary variation is com-
mon within species and that high rates of mortality are also the rule. Thus,
alternative forms within a species are forced into an unconscious competition
to be among the relatively few survivors. In other words, the conditions neces-
sary and sufficient for evolutionary change by natural selection are present in
all living things, a point that Darwin demonstrated by showing that people
could cause dogs and pigeons to evolve by selectively breeding those indi-
viduals with hereditary traits that the breeders wanted in future generations
of their domesticated animals.
Therefore, for the purpose of testing evolutionary ideas, we can assume that
whatever trait exists today must have “won” a reproductive competition that
took place in the past. If the assumption is wrong, our tests, if they are fair,
will reveal this point. If the assumption is correct and the trait did win out
over time, then we are dealing with an adaptation. Figuring out exactly how
a putative adaptation contributes to the reproductive success of individu-
als is the central goal of behavioral ecologists, some of whom are happy to
be known as adaptationists. Whatever the label, I believe that Tim Birkhead
speaks for behavioral biologists in general when he writes, “The best thing
of all about being a behavioural ecologist is that one’s enthusiasm for the
natural world actually increases over time. The more we discover, the more
we discover that there is still more to discover.”4
Certainly Darwin would have agreed, especially with respect to the heredi-
tary foundation of evolutionary theory. Although Darwin himself knew noth-
ing about genes, we now can reconfigure his argument to deal with selection
at the level of the gene. Just as hereditary adaptations that increase the repro-
ductive success of individuals will spread through populations over time, so
too the genetic basis for these attributes will increase in frequency. Because
genes can be present in populations in different forms, known as alleles, those
alleles that contribute to the development of traits linked to individual repro-
ductive success will become more common over time; those associated with
reproductive failure will eventually disappear.
Notice that natural selection, whether acting on individual variation or
genetic variation, is not guided by anything or anyone. Selection is not “try-
ing” to do anything. Instead, the better reproducers cause a species to evolve.
Notice also that the only kinds of hereditary characteristics that will become
more common in a species are those that promote individual reproductive
success, which do not necessarily benefit the species as a whole. Although
“for the good of the species” arguments were often made by biologists not
so long ago, it is entirely possible for adaptations (and particular alleles) to
spread through populations even if they do nothing to “perpetuate the spe-

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cies.” Indeed, traits and alleles can be naturally selected that are harmful to
group survival in the long run.

Discussion Question
1.1 In order to explain how the blind process of natural selection—a
process dependent on random events (mutations)—can generate complex
adaptations, Richard Dawkins invites us to imagine that an evolved attribute
is like an English sentence—like a line from Shakespeare’s Hamlet, such as,
METHINKS IT IS LIKE A WEASEL.9 The odds that a monkey would produce
this line by tapping at a typewriter are vanishingly small, one in 10,000
million million million million million million (1 in 1040). These are not good
odds. But instead of trying to get a monkey or a computer to get the “right”
sentence in one go, let’s change the rules so that we start with a randomly
generated letter set, such as SWAJS MEIURNZMMVASJDNA YPQZK. Now
we get a computer to copy this “sentence” over and over, but with a small
error rate. From time to time, we ask the computer to scan the list and pick
the sequence that is closest to METHINKS IT IS LIKE A WEASEL. Whatever
“sentence” is closest is used for the next generation of copying, again with
a few errors thrown in. The sentence in this group that is most similar to
METHINKS … WEASEL is selected to be copied, and so on. Dawkins found
that this approach required only 40 to 70 runs (generations) to reach the tar-
get sentence. What was Dawkins’s main point in illustrating what he called
cumulative selection? In what sense is this example not a perfect analogy
for natural selection?

Natural selection theory helps biologists identify aspects of living things

worth studying. If you are aware of the way in which natural selection works,
then traits that appear to reduce rather than raise an individual’s reproductive
success are surprising. We will call these challenges to evolutionary theory
Darwinian puzzles (and we will call your attention to them with an icon of
an ant on a puzzle piece). Biologists deal with these puzzles by developing
possible explanations based on natural selection theory for how the surprising
trait might actually help individuals reproduce and pass on their genes. For
example, rather than proposing ideas about how male digger bee behavior
benefits the species as a whole, the behavioral ecologist tries to come up with
one or more explanations for how male digging behavior might promote the
reproductive success of individual males. Males of Centris pallida that could
find and dig down to hidden virgin females would seem to have an advantage
in mating with those females when they crawled out of their emergence tun-
nel. The male’s advantage would be particularly great if, once having mated,
the freshly emerged female was no longer receptive.1

Discussion Question
1.2 In experiments in which parent birds are given extra nestlings to rear,
the adults usually rear larger numbers of youngsters to fledging than they
do naturally.30 Why does this finding pose a Darwinian puzzle? How might
the possibility that egg production and incubation require considerable
effort15,24 help an adaptationist develop hypotheses that may resolve the

Darwinian hypotheses are testable because they often can be used to produce
predictions that can then be checked against reality. In the case of the bee, we
can predict that (1) given the males’ enthusiasm for virgins, a Centris pallida

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female either mates just once in her life or uses the sperm
of her first partner to fertilize her eggs. We can also pre-
dict that (2) in other bee species in which females remain
sexually receptive after mating and do not give male
number one a fertilization advantage, males will be far
less likely to search for virgin females than males of Cen-
tris pallida. In addition, we would expect that (3) males
of Centris pallida should not let fellow males gain access
to receptive females if they can prevent it.
Notice that all three predictions or expectations are
based on the assumption that males are in a race to
inseminate as many females as possible while other
males are trying to do the same thing. And, as a matter
of fact, (1) females of Centris pallida almost certainly do
mate just once, judging from the fact that nesting and
flower-visiting females are rarely, if ever, pursued or
contacted by sexually motivated males. Moreover, (2)
in other bee species in which females do mate several
times, males often meet their mates at pollen- and nectar-
producing flowers rather than at their emergence sites
FIGURE 1.3 A pair of native bees
belonging to the genus Perdita
(Figure 1.3). Finally, (3) males of Centris pallida are indeed
copulating on a desert poppy. This spe- highly aggressive in defense of digging sites and they sometimes lose to other
cies of Perdita is just one of many bee males, often larger ones, that displace them from spots where virgin females
species that use flowers as a rendez- are about to emerge (Figure 1.4).
vous site for mating. Photograph by the
Discussion Question
1.3 Someone proposes that the reason males of Centris pallida often fight
for access to females is to ensure that only the best males, the largest and
most physiologically competent individuals, the ones with the best genes,
get to mate. Is this hypothesis based on natural selection theory? Why or
why not? How would you test the idea?

FIGURE 1.4 Males of Centris pallida

fighting. These individuals are strug-
gling to control a spot from which a
female is about to emerge. Photograph
by the author.

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FIGURE 1.5 Hanuman langur

females and offspring. Males fight
to monopolize sexual access to the
females in groups like this one.

Natural Selection and Infanticide

Let us apply natural selection theory to another case, which came to notice
in a study of Hanuman langurs. These monkeys live in groups (Figure 1.5) of
several females and their offspring accompanied by one or a few adult males.
In the course of this research, male Hanuman langurs were seen attacking
and even killing the very young infants of females in their own group (Figure
1.6A). The puzzle here is obvious: how can it be adaptive for a male langur to
harm the offspring of females in his group, particularly since attacking males
can be and sometimes are injured by mothers defending their babies (Fig-
ure 1.6B)? Indeed, some primatologists have argued that the very unpleasant

(A) FIGURE 1.6 Male langurs commit infanticide. (A) A nursing baby
langur that has been paralyzed by a male langur’s bite to the spine
(note the open wound). This infant was attacked repeatedly over a
period of weeks, losing an eye and finally its life at age 18 months.
(B) An infant-killing male langur flees from an aggressive protective
female belonging to the band he is attempting to join. A, photograph
by Carola Borries; B, photograph by Volker Sommer, from Sommer.28

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FIGURE 1.7 A male lion carrying a

cub that he has killed. The conditions
under which infanticide occurs in this
species are very similar to those associ-
ated with male infanticide in Hanu-
man langurs. Photograph by George

infanticidal behavior of these males was not adaptive but was instead the aber-
rant aggressive response by males to the overpopulation and crowding that
occurred when langurs came together to be fed by Indian villagers. According
to these observers, overcrowding caused abnormal aggressive behavior.7 But
the behavioral ecologist Sarah Hrdy used natural selection theory to try to
solve the puzzle of infanticide in a different way, namely by asking whether
the killer males were behaving in a reproductively advantageous manner.19 By
committing infanticide, the males might cause the baby-less females to resume
ovulating, which otherwise would not happen for several years in females that
retain and nurse their infants.
Hrdy tried to explain how infanticide might have spread through Hanu-
man langur populations in the past as a reproduction-enhancing tactic for
individual males. Hrdy’s potential explanation for the evolution of the behav-
ior leads to a number of expectations, of which the most important is the pre-
diction that males will not kill their own progeny but will focus their attacks
on the offspring of other males. This prediction in turn generates the expecta-
tion that infanticide will be linked to the arrival of a new male or males into
a band of females, with the associated ejection of the father or fathers of any
baby langurs in the group. In cases of this sort, the new males could father
offspring more quickly if they first killed the infants in the band. Females
who lose their infants do resume ovulating, and that enables the new males
in the band to become fathers of their replacement offspring. Since these pre-
dictions have been shown to be correct for this species5 as well as some other
primates,3,23 various carnivores (Figure 1.7), horses, rodents, and even a bat,20
we can safely conclude that infanticide as practiced by male langurs is indeed
an adaptation, the product of natural selection.

Discussion Question
1.4 Because the reproductive success of female langurs is almost certainly
lowered when a newly installed male kills their young infants, selection
should favor countermeasures against infanticidal males. In this light, why
might already pregnant females mate with a new male soon after a takeover
even though they are not ovulating? What significance do you attach to the
discovery that when mares are impregnated by stallions at a stable away
from their home location, they will also copulate repeatedly with the males
in their home stables upon their return?2

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The Science of Behavioral Biology

Let me emphasize that although many persons think that adaptive means
“good” or “desirable,” in evolutionary terms adaptive only means “reproduc-
tively advantageous for individuals” or “beneficial for the genes that underlie
the development of the trait.” When Hrdy proposed that infanticide might be
adaptive, she was of course not trying to justify in moral terms the behavior
of killer males. Thoroughly cruel and ugly behaviors can evolve by natural
selection if they happen to enhance the ability of individuals to pass on their
genes to the next generation. Infanticidal males that cause some other males’
offspring to die are behaving adaptively if they are not themselves seriously
injured by the mothers and if the mothers of the deceased offspring come into
estrus and mate with the killer males. Often both conditions apply, which is
why Hrdy and others have concluded that langur infanticide is an adaptation
exhibited by some males under some conditions.
In contrast, an explanation for infanticide based on the claim that over-
crowding leads to hyperaggression with incidental attacks on infants pro-
duces a prediction that has not been confirmed by additional study. Thus
adult male langurs living in natural areas away from villagers that supply
them with extra food still exhibit infanticide, which contradicts the idea that
infanticide is an aberrant behavior linked with unnatural conditions.
Behavioral ecology and the other equally important components of behav-
ioral biology are scientific disciplines. By this I mean that researchers in these
fields use a particular kind of logic to evaluate potential explanations for puz-
zling phenomena. We used this logic to decide that male digger bees search
for and dig down to reach emerging females because this behavior helps them
inseminate virgin females, the only kind of females that will mate with them
and produce their offspring.
This explanation can be tested by identifying what a researcher must be able
to observe if the hypothesis is true. If it is, virgin females will mate with their
discoverers but foraging females will not be sexually receptive. When several
predictions derived from a hypothesis are shown to be true, the hypothesis
gains credibility; if, on the other hand, the expected results do not materialize,
the hypothesis loses support. Well-tested hypotheses are the basis for sound
scientific conclusions, which take the form of “this idea is probably right” or
“this potential explanation is almost surely wrong.”
The Power of Scientific Logic
Scientists often pat themselves on the back for using what they believe is
a very effective means for solving puzzles about the natural world. But at
least on some issues, the general public is far more skeptical. An illustrative
example involves the current question of what is causing the Earth’s climate
to warm up. Almost all climate scientists have claimed that by burning fossil
fuels, humans are mainly responsible for the recent rise in the temperature of
the atmosphere. But according to a poll by the Pew Research Center (http:// released on October 22, 2009, only a third of all citizens of
the United States believe that human activity is responsible for climate change.
Some skeptics think that climate scientists are fudging the data in order to
get grants for themselves and their colleagues. This strategy would, however,
require that other climate scientists refrain from commenting on the fraudulent
behavior of certain of their fellow scientists. Such restraint is unlikely given
that scientists are competitive people who review the ideas of their colleagues
at every step of the process, starting right from the beginning when they rate
the grant proposals of their fellow scientists. Should a study become funded
(and many do not) and should it lead to published research articles, the con-

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clusions presented in these articles might even then be examined skeptically

because of the benefits to academics of demonstrating that so-and-so’s con-
clusion is wrong. The successful critic gets a publication or two on this point
as well as the social esteem that comes from being known as someone who
gets things right. As a result, science tends to be self-correcting, not because
scientists are selfless saints but precisely because researchers are competitive
individuals who strive for high social status in the community of their peers.
Yes, sometimes the pressures to succeed in academia lead researchers to
see what they want to see from their studies. A researcher can mistakenly
claim to have secured a result that the data do not support. Or a scientist may
ignore an inconvenient finding or reject it outright on spurious grounds. Some
scientists, including well-known ones, have even engaged in outright fraud. A
fairly recent case involved a stem cell researcher, Dr. Hwang Woo-suk, found
guilty by a South Korean court of having manufactured data that appeared
in two papers on embryonic human stem cells (see the Reuters online news
report [] entitled “South Korean stem cell scientist accused
of fraud”). Before the accusations against Hwang had been aired, these papers
had been considered major breakthroughs in the effort to devise methods to
treat Alzheimer’s disease and the like.
Note, however, that the reason we know that scientists are capable of self-
deception and fraud is largely from the work of other scientists, who have
gained social rewards from ferreting out mistakes and identifying scientific
malfeasance when it occurs. The skepticism of scientists and their willing-
ness to critically examine and reexamine the findings of others means that by
the time a scientific consensus is reached, it is likely to have been thoroughly
vetted. A scientific consensus has been achieved on the global warming prob-
lem.14 Eventually, perhaps most of us will accept that the Earth is warming up
and that people (and their machines) are the culprits. We should, since most of
us agree that airplanes are safe to fly, light switches generally work, cornfields
tend to produce more corn than ever, computers do what they are supposed
to do, medical procedures and drugs actually cure illnesses, and so on—all
matters that have been established via scientific consensus. Indeed, almost
every aspect of modern life, from agriculture to zoo management, is based
on scientific research, which involves many rounds of hypothesis testing and
critical review before a position becomes widely accepted.
This book presents a sampler of the conclusions reached by behavioral
researchers—along with the test evidence that underlies these conclusions.
One of my major goals is to encourage my readers to realize how scientists
evaluate hypotheses in ways that are generally considered fair and logical
(at least by other scientists). The cases reviewed in the chapters ahead have
been selected with this goal in mind. Chapter 2 takes up what many con-
sider to be the premier puzzle for behavioral ecologists, namely the evolution
of self-sacrificing behavior in social insect colonies, a puzzle that continues
to generate scientific review and debate. Chapter 3 examines the adaptive
value of the social behavior of animals other than social insects. Chapter
4 looks at the evolution of communication signals. Chapters 5 and 6 are
dedicated to the adaptationist analysis of antipredator behavior, foraging
behavior, and habitat selection. Chapters 7, 8, and 9 explore the behavioral
ecology of various elements of reproductive and parental behavior. Chapter
10 introduces the concept of the proximate (immediate) causes of behavior

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and how these causes differ from the ultimate (evolutionary) causes that
Chapters 1–9 examine. Chapters 11, 12, and 13 then consider the evolution-
ary basis of the proximate developmental and physiologi-
cal mechanisms that underlie adaptive behavior. Finally,
Chapter 14 offers an example of how both proximate and
ultimate research contribute to an understanding of the
causes of our language skills; the chapter also looks at the
reproductive strategies of our own species. Let’s get started.

1. Evolutionary theory provides the foundation for behavioral biology, the
study of animal behavior.
2. Charles Darwin realized that evolutionary change would occur if “natu-
ral selection” took place. This process happens when individuals differ
in their ability to reproduce successfully, as a result of their inherited
attributes. If natural selection has shaped animal behavior, we expect that
individuals will have evolved abilities that increase their chances of pass-
ing copies of their genes on to the next generation.
3. Researchers interested in the adaptive value of behavioral traits use natu-
ral selection theory to develop particular hypotheses (tentative explana-
tions) on how a specific behavior might enable individuals (not groups or
species as a whole) to achieve higher reproductive success than individu-
als with alternative traits.
4. Adaptationist hypotheses can be tested in the standard manner of all
scientific hypotheses by making predictions about what we must observe
in nature, or in the outcome of an experiment, if a particular explanation
is true. Failure to verify these predictions constitutes grounds for rejecting
the hypothesis; the discovery of evidence that supports the predictions
means the hypothesis can be tentatively treated as true.
5. The beauty of science lies in the ability of scientists to use logic and
evidence to evaluate the validity of competing theories and alternative

Suggested Reading
Three books are essential for all students of behavior: On the Origin of Species
by Charles Darwin8 (you will benefit from James Costa’s annotated ver-
sion of this book6), Adaptation and Natural Selection by George C. Williams,31
and The Selfish Gene by Richard Dawkins.10 Michael Le Page provides links
explaining what is wrong with the common thinking about evolution in
his article “Evolution: 24 myths and misconceptions.”21 For a provocative
essay on the nature of science itself, read Woodward and Goodstein’s article
“Conduct, misconduct, and the structure of science.”32 Excellent books by
behavioral biologists that capture the pleasures of field research include clas-
sics by Niko Tinbergen,29 Konrad Lorenz,22 George Schaller,26,27 and Howard
Evans.12,13 Many delightful accounts of this sort have been written more
recently, too many to list here, but for what it is worth, I especially like the
work of Bernd Heinrich,16,17 Craig Packer,25 and Bert Hölldobler.18

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