Animal Behaviour

Copyright 2011 Cold Spring Harbor Laboratory Press. Not for distribution.
Do not copy without written permission of Cold Spring Harbor Laboratory Press.
Preface
the tapestry of biology: It is sparked when neurons fire in response to stimuli in the external world, it forms the interactions that lead to reproduction and genetic propagation, and it enhances complex group function, even when it emerges from seemingly simple self-organizing principles. Animal behavior is the most integrative endeavor of biologyits practitioners vary from those interested in the molecular, hormonal, and neural control of behavior to those who concentrate on its adaptive significance, historical patterns, and ecological consequences. As such, animal behavior provides the interface between proximate and ultimate biologythe processes internal to the animal and the consequences external to it. As an example, an animals sensory system is exquisitely designed to perceive and organize the details of its external world, and few would argue the potency of natural selection in bringing about such an adaptation. But selection does not act directly on a sensory system; it acts on the behaviors that emerge from the interaction between the sensory system and the world around it. Nor does behavior evolve directly; rather it comes about from heritable changes in its underlying mechanism. How can we hope to understand animal behavior, or more generally, the science of life, if we commit to the parochialism of proximate versus ultimate questions and the mantra that they have nothing to do with one another? A subtext of this book is that we welcome the demise of the old proximate ultimate dichotomy and celebrate what we hope will become a seamless segue from molecules and neurons to adaptation and evolution in the quest to understand why animals behave the way they do. Both of our research programs have benefited from continual discussion and interactions across the proximate ultimate boundaries of animal behavior. Walter Wilczynski was a postdoctoral associate studying the neuroscience of auditory systems in the Section of Neurobiology and Behavior at Cornell University at the same time that Michael J. Ryan was completing a thesis on sexual selection and acoustic communication in the same department. We were both hired at the University of
N I M A L B E H AV I O R W E AV E S I T S E L F T H R O U G H O U T
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Copyright 2011 Cold Spring Harbor Laboratory Press. Not for distribution. Do not copy without written permission of Cold Spring Harbor Laboratory Press.
P R E FAC E
Texas in the early 1980s, W.W. in the Department of Psychology and M.J.R. in what was then the Zoology Department (and later morphed into the Section of Integrative Biology). We quickly began a series of research collaborations on the mechanisms and evolution of acoustic communication in anurans that continues to this day. It was through these interactions that we both became convinced that integrative animal behavior consists of more than cataloging data at different levels of analysis but is most potent when it uses information at each level of analysis to inform research and interpretations at other levels. We also became convinced that this interaction is symmetric, with proximate details being as important to understanding ultimate processes as evolution is critical for understanding the precise design of mechanisms of animal behavior. It is in this spirit that we set out to present our view of integrative animal behavior. Our book is not intended to be an exhaustive review of the field of animal behavior but instead an introduction from an integrative perspective. It is aimed at upperlevel undergraduates, graduate students, and others wanting exposure to this particular approach to animal behavior. The field of integrative animal behavior is so vast that it is impossible to cover exhaustively. Our strategy was to discuss the areas of animal behavior that both were historically of great interest to the field and continue to receive considerable interest among researchers and students. Necessarily, some interesting areas were omitted or mentioned only briefly to keep the size of the book manageable: These neglected topics include aposematic coloration, plant animal interactions, and many areas of great interest to comparative psychologists, such as animal learning and conditioning and the growing field of animal cognition. There is a dearth of behavioral development in this book, in part because the marriage of this historically important field and the current rages in evo-devo and eco-devo seem not yet to be consummated. In those areas of animal behavior we have covered, we hope to provide the reader with a sense of their basic ideas and research problems as well as examples of both classic and contemporary research. The references we provide for each chapter are meant to do the same. We aimed to provide a collection of classic papers, new research findings, and several review papers, chapters, and books that will afford the interested reader an entry into the field as well as credit those works that provide its foundation. Unavoidably, we neglected some important and interesting work, especially from the large amount of new research coming into the field every day. We apologize in advance for any oversights. In preparing this book, we drew heavily on others that are more specialized and provide a greater depth on aspects of behavior, neuroscience, and behavioral endocrinology. Most are included in the references in various chapters where they were most helpful, but we feel it important to express our appreciation and mention those here, as they would be excellent resources for readers who want more depth in various areas covered in our book. Every biologist who thinks herself educated should have read Darwins On the Origin of Species. If interested in behavior, she should add The Descent of Man, and Selection in Relation to Sex, as well as The Expression of the Emotions in Man and Animals. The nine editions of John Alcocks Animal Behavior, An Evolutionary Approach have schooled many generations of behaviorists
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over the last 35 years, and the textbook An Introduction to Behavioral Ecology and the collected writings, Behavioral Ecology, An Evolutionary Approach, by John Krebs and Nick Davies, have performed a similar task for the subdiscipline of behavioral ecology. Few textbooks combine both the excitement of animal behavior and concise and critical analyses of theory and data as do those of Alcock and of Krebs and Davies. A new set of textbooks has recently updated the field and they fill a role similar to that of the old Krebs and Davies. On the more mechanistic end of the animal behavior spectrum, Ralph Greenspans An Introduction to Nervous Systems and Gunther Zupancs Behavioral Neurobiology are complementary in providing excellent introductions to neuroscience as well as to neural mechanisms of behavior and neuroethology. Several books were especially helpful in providing background on the endocrinology of behavior: Randy Nelsons textbook An Introduction to Behavioral Endocrinology, Elizabeth Adkins-Regans Hormones and Animal Social Behavior, the edited book Behavioral Endocrinology, by Jill Becker and colleagues, as well as the five-volume work Hormones, Brain and Behavior, edited by Donald Pfaff and colleagues. The latter is a major reference in the field of behavioral and neural endocrinology. We also were greatly aided by numerous colleagues who provided comments and criticism of the chapters, shared unpublished data and background information, and engaged in discussions that clarified numerous issues. In particular, we would like to thank Karin Akre, Kim Hoke, and Deborah Lutterschmidt for their insightful reviews of the entire manuscript, and the Cold Spring Harbor Laboratory Press editor Judy Cuddihy for her exquisite attention to both detail and organization. In addition, we thank Elliott Albers, Greg Ball, Robert Bridges, David Cannatella, Lars Chittka, David Crews, Steve Emlen, Matthew Grober, Kim Huhman, Jonathon Losos, Robert Mason, Michael Meany, Kirsten E. Nicholson, Steve Nowicki, John Phillips, Joan Strassman, Greg Sword, David Quellar, and the late Jerry Waldvogel. They have all helped improve the quality of this work. We would also like to acknowledge the support we have been fortunate to receive for our research. Mike Ryans work has received support from the National Science Foundation, the Smithsonian Tropical Research Institute, and the Clark Hubbs Professorship in Zoology. His department also provided a semester faculty leave to work on the book. Walt Wilczynskis research has been supported by the National Science Foundation, the National Institute of Mental Health, the Smithsonian Tropical Research Institute, and the Center for Behavioral Neuroscience, a Science and Technology Center established with funding by the National Science Foundation with continuing support from Georgia State University. We would also like to thank the past and present members of our own labs, who drove our research and our intellectual engagement with animal behavior and all the areas of science that connect to it. It is not inappropriate to thank in advance our future students and colleagues as well, for helping us explore areas of animal behavior yet to come. M.J. Ryan W. Wilczynski
H A P T E R
Questions in Animal Behavior
M A G I N E A N A N I M A L T H AT D O E S N OT B E H AV E . Then try to imagine being interested in an animal that does not behave. Without doubt, there are aspects of an animals biologyits morphology, brain, and genes, its ecology and evolutionary history that spark the interest of many scientists. But it is the animals behavior that often focuses the attention of scientists and nonscientists, children and adults. One cannot imagine the success of the plethora of wildlife documentaries flooding the public airways if the animals in them did not behave. Animal behavior is the fulcrum between the processes internal to the individual its genetics, neurobiology, and physiologyand all that is external to it, including the environment, its social surroundings, and the other species it eats or is eaten by. Details of an animals behavior have been shaped by millennia of selection molding them within the constraints imposed by the details of the animals biology and endowing the animal with the capacity to respond flexibly to its surroundings in a manner that can sometimes be both exquisite and enigmatic. These factors make animal behavior one of the most integrative endeavors in biology: It encompasses both proximate and ultimate questions, how the behavior works, and why it has come to work as it does.
TINBERGENS FOUR QUESTIONS

In 1973 Niko Tinbergen was awarded the Nobel Prize in Physiology or Medicine, along with Karl von Frisch and Konrad Lorenz, as one of the founders of ethology, the study of animal behavior in its natural environment. In an attempt to organize this new endeavor, he codified the study of behavior in a 1963 paper, On aims and methods of ethology, by proposing four general questions: causation, ontogeny, survival value, and evolution. Today we know these as mechanisms, acquisition,
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adaptive significance, and evolutionary history. The first two questions address proximate causes and the latter two ultimate causes. All four questions can address the same behavior. We can illustrate this by considering a male songbird perched on a treetop vigorously singing its complex song in a feat of acoustic acrobatics. How can we explain this behavior? It depends on what question we ask and what we mean when we ask it (Fig. 1.1). Why does a bird produce the complex acoustic patterns we know as song? This question can be rephrased to ask, how does he make the song? The mechanism of singing involves accessing a neural code in the brain that drives the respiratory patterns
Mechanisms
Seminlunar membrane Tracheal rings Syringeal muscles Bronchial rings Internal typaniform membrane Interbronchial foramen
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5 4 3 2 1 0 1
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Psarocolius a. angustifrons P. a. alfredi
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Males song repertoire size
Figure 1.1. A deep understanding of animal behavior requires answers to all of Tinbergens four
questions. One example is, Why do birds sing? Here we represent a singing male oropendola, a member of the New World blackbird family, and (clockwise from top, left) the morphology of the syrinx that enables complex song production, the brain circuitry involved in song learning, a phylogeny of some oropendola taxa and sonograms of the song they produce, and a hypothetical relationship between male song repertoire size and the number of offspring sired. (HVC) High vocal center; (nXIIts) hypoglossal nucleus; (DLM) dorsolateral anterior thalamic nucleus; (LMAN) lateral magnocellular nucleus or the nidopallium; (RA) robust nucleus of the arcopallium.
Q U E S T I O N S I N A N I M A L B E H AV I O R
and muscles of the birds vocal organ, the syrinx, to produce a pattern of sound pressure fluctuations that can be interpreted by a receiver. The mechanism also involves the biomechanical details of the syrinx, which functions similarly to our larynx. There are some elegant characteristics of the songbird syrinx that endow these birds with the ability to make two separate songs at once, the two-voiced song, which results in some of the most complicated vocal repertoires in the animal kingdom. We can answer this same question another way: How does he know how to make the song? We know that songbirds acquire their song through learning. To produce these complex acoustic patterns, they must be exposed to songs of another member of their species, a conspecific, during a sensitive period early in their life. These two answers to the same question both concern proximate issues in behavior, the underlying mechanisms governing the behavior, and how the behavior is acquired. We can also ask why the bird singsthat is, what is the function of song? Questions about the function of behavior address its adaptive significance and ask how a behavior influences the fitness of the animal producing it. Male songs have multiple functions. These songs are used to interact acoustically with other males and as courtship signals to females. Variation in song among males is under evolutionary selection because it influences a males reproductive success. In many species, for example, females prefer males with larger song repertoires, so it seems that large repertoire size could have evolved under selection generated by female mate choice. This is a functional explanation of why birds sing complex songs, and it is rooted in understanding the potential adaptive significance of the behavior. We can ask again: Why does the bird sing a complex song? A seemingly simple answer is: Because it is a songbird. This answer is not as glib as it might first appear; it is an informed response motivated by concerns about the past. Not all birds have complex songs. Thus, we can ask about the evolutionary history of the trait. Complex song does not occur randomly among birds. Instead, the occurrence of complex song shows a strong historical pattern. Complex song is common within one phylogenetic group of birds, the oscines or songbirds, and is not common in other groups. This group of birds is also among the few that learn song and that have an anatomically complex syrinx. Questions about evolutionary history ask where a behavior came from. Questions of function and history are usually considered ultimate questions. It is important to understand what questions are being asked of an animals behavior. Why does a bird sing complex song? has at least four answers: because it has a complex syrinx, because it learned the song of an adult, because selection favors complex songs, and because it is a songbird. The field of animal behavior has been replete with disagreements because different researchers were asking different questions, not just because they were arriving at different answers. Tinbergens four questions were meant to resolve some of these problems.
CHAPTER 1
TINBERGENS ONE QUESTION

In the same 1963 paper, Tinbergen proposed a more general question that concerns all animal behaviorists: Why do animals behave the way that they do? He suggested one had to address each of his four questions to arrive at a complete understanding of animal behavior (i.e., to answer his one question). This will be a subtext running throughout this book. Animal behavior encompasses research disciplines that sometimes have little overlap. Mechanisms of behavior are traditionally the domain of neurobiologists and physiologists, whereas studies of the acquisition of behavior are often conducted by comparative psychologists who study learning or geneticists interested in behavioral genetics. Behavioral ecologists have been at the forefront of understanding the adaptive significance of behavior, whereas studies of the history of behavior have been conducted by those with a background in phylogenetics. These are fields of science that often have little interaction, publish in different journals, and embrace different research traditions. Yet none of this makes any difference to the behavior being studied. The fact that a neurobiologist has never been in the field does not negate the importance of natural selection in shaping the neural circuit being studied; nor does the ignorance of a field biologist about the black box controlling behavior exclude the critical importance of this mechanism for the animals survival. We hope to demonstrate throughout this text that an integrative analysis of animal behavior attempts to obtain a deep and complete understanding of behavior by addressing each of Tinbergens four questions. There are two reasons to strive for such integration. Because there are different aspects to behavior, we must address all of them to truly answer Tinbergens one question about why animals behave the way that they do. But another important reason is that answers to questions at one level of analysis can inform answers at other levels. We can briefly illustrate this point by developing the issue of birdsong further. One function of birdsong is to provide information about species identity. Thus, the divergence of song between populations can contribute to speciation. Although the songbirds two-voiced syrinx is primarily responsible for the acoustic features of the song, the morphology of the birds beak can also influence what the song sounds like, specifically its trill rate and frequency range. But the beak not only influences what comes out of the bird but also what goes into it. Beak morphology is critpagos ical for feeding, and nowhere is this shown more clearly than in the Gala finches. Many popular accounts of the voyage of the Beagle credit the adaptive radiation pagos finches as providing Charles Darwin with insights that were critical of Gala to development of his theory of natural selection, although it did not happen until Darwin returned to England and the ornithologist John Gould drew his attention back to these birds. Although these finch species are very similar in size and color, they differ quite profoundly in the variety of their beak morphologies. Divergence
in these finches was driven by diet, and their beaks evolved to complement and enable the diet. It is very remarkable that a nearly perfect gradation of structure in this one group can be traced in the form of the beak, from one exceeding in dimensions that of the largest gros-beak, to another differing but little from that of a warbler, as Darwin stated in The Voyage of the Beagle. These birds evolved large, parrot-like beaks for eating fruit, grasping and probing beaks for hunting insects, and crushing beaks for crushing seedslarger beaks for larger seeds and smaller beaks for smaller seeds (Fig. 1.2). Jeffrey Podos showed that not only does the beaks form vary with diet, but it also varies with song; males with larger beaks that eat large pagos seeds have a slower pulse rate and more restricted frequency range than Gala finches with smaller beaks. Thus, selection that results in the evolution of beaks to promote feeding efficiency incidentally causes evolution of song differences among birds with different diets. It has been suggested that divergence of songs contributes to speciation between populations that not only eat different things but also sound different. The above example uncovers a relationship between feeding ecology, song behavior, and speciation. The critical insights were how beaks influenced song and diet and how song functioned in mate recognition. We will investigate a few additional examples of such synergisms between different levels of analysis.
Platyspiza crassirostris
Camarhynchus psittacula
Camarhynchus parvulus
Cactospiza pallida
Certhidea olivacea
Geospiza conirostris
Geospiza difficilis
Geospiza fuliginosa
Geospiza magnirostris
Tree finch Parrot-like bill Fruit eater Grasping bill Insect eater
Warbler finch Probing bill Cactus eater
Ground finch Crushing bill Seed eater
Figure 1.2. In Darwins finches, bill morphology is closely related to diet. The middle of the figure shows species of all of the finches included in the analysis. Each finch (from left to right) corresponds to each column, from left to right, in the diagram above. The diagram at the top of the figure has three rows. The top row illustrates the ecological group to which each finch belongs, the middle row the type of bill, and across the bottom row a description of their diet. Each of these rows corresponds to the color-coded legend at the bottom of the figure. For example, the finch Platyspiza crassirostris is a tree finch (top row, blue) with a parrot-like bill (middle row, light gray) who eats fruit (bottom row, light blue).
CHAPTER 1
SYNERGISMS BETWEEN DIFFERENT LEVELS OF ANALYSIS Evolutionary History Informs Function

Female mate choice has been a major topic within behavioral ecology for many years. As Darwin pointed out in his theory of sexual selection, this behavior is responsible for the evolution of some of the most bizarre morphologies and behaviors in the animal kingdom. One controversial aspect of Darwins proposal was why females should prefer certain male traits. The search for this answer usually assumes that male traits provide information to the female about the males physical or genetic quality. However, studies of mate choice in swordtails reveal another possibility.
Mate Choice in Swordtails

Swordtails are live-bearing fishes in which the lower rays of the caudal fin are extended into a sword-like appendage. Swordtails are close relatives of platyfish, which are in the same genus (Xiphophorus), although platyfish usually lack these sword-like appendages. Mate choice experiments in Xiphophorus helleri show that females prefer males with longer swords (Fig. 1.3). Most behavioral ecology studies would stop there and speculate about what sword length tells the female about the males health or genes. But in a series of studies by Alexandra Basolo, the focus of preference for swords shifted to a species without swords, the platyfish Xiphophorus maculatus. When a plastic sword was appended to a male platyfish, the females preferred the male with the artificial sword. Experiments with other platyfish and even other live-bearing fish yielded similar results. How can one interpret these results, with females preferring a male trait that does not exist in nature? Although the phylogenetic relationships within Xiphophorus are not fully resolved, it appears that swordtails are all each others closest relatives, and they inherited swords from a common ancestor after they diverged from the platyfish. However, as both swordtails and platyfish prefer males with swords, we assume that the preference was inherited from a common ancestor that would have existed before the swordtails and platyfish diverged. This historical logic suggests that the preference for the sword predated the evolution of the sword. If this interpretation is correct, it suggests that the sword was already favored by females when it evolved, as opposed to the alternative, that the sword evolved first as a signal of male quality and females then evolved a preference for it. Of course, female preferences for the trait and the traits themselves can both evolve further once the interaction of trait and preference is established. There is more, however, to the swords tale. In many species of live-bearing fish, females prefer larger males. It has been suggested that the sword is an energetically cheap way to make the male larger. In experiments by Gil Rosenthal and Christopher Evans using video animations, females compared two males of the same total body length (measured from the tip of the snout to the base of the tail), but one male had a sword, whereas the other male was lacking a sword. Actually, because these
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Figure 1.3. Fishes in the genus Xiphophorus are either swordtails or platyfish. Swordtails have elongated caudal rays that form the sword, which are lacking in platyfish. Alexandra Basolo showed that female swordtails prefer normal males with swords to males in which the sword is surgically removed, and that female platyfish prefer males with swords that are surgically added to normal swordless males. The same is true for some close relatives that lack swords. The preference for the sword therefore evolved before the sword itself. The conclusion is that males evolved traits that exploit preexisting female preferences.
were animations, the two males had the same body and the same courtship behavior. Female X. helleri preferred the male with the sword to the one without a sword. But when size was manipulated such that the swordless male was as long as the male with the sword, the females did not show a preference. Thus, female X. helleri prefer longer males whether or not a sword adds to their length. It appears that males evolved swords to exploit a preexisting female bias for larger males. These studies on the swords of swordtails provide an excellent example of how information on the evolutionary history of the behavior can inform us about how it evolved.
CHAPTER 1
Mechanism Informs Function

Few natural scenes are as stunning and breathtaking as the fall foliage in northeastern North America. The trees are ablaze in riotous reds, yellows, and oranges as they prepare to drop their leaves for the winter. Plant physiologists have offered several explanations for this autumnal explosion of color. Some of the colors, such as yellow, are by-products of disintegration; as the green chlorophyll disappears, the underlying colors are revealed. But certain products (red anthocyanins) are produced only in the fall, and these products have several functions. They are antioxidants, they might function as sinks for harmful metals, and they also might warm the leaves and protect them against ultraviolet (UV) light.
Autumn Leaves and Aphid Vision

A strikingly different explanation for fall colors was offered by the evolutionary biologist W.D. Hamilton, one of the great thinkers of biology in the 20th century, and published posthumously in 2001. He posited that these are warning colors that the trees use to signal herbivores, such as aphids, to stay away. This should be an honest signal, that is, a reliable indicator of the signalers quality, in that the brighter the leaves, the more toxic they are to the herbivore. The more yellow the leaves of a species of tree, the more likely it is to be colonized by aphids. Thus, it was suggested that these species need to invest more in warning signals to repel aphids, an argument that was independently proposed and addressed with a game theory model by Marco Archetti. A basic assumption of the warning color argument is that the insects perceive the difference between red and yellow. The mind-bending question we ask ourselves at this point is, When two people say they see an object they report is colored blue, how can we be sure they are really experiencing the same color as we are? We cannot. But we can be sure that other species do not necessarily have the same experience of color that we have. An animals sensation of color can be determined if we know the spectrum of sunlight that strikes an object, the spectrum of light reflected by that object, the spectral sensitivities of the receivers photopigments, and the interaction of different photopigment classes in the color perception system. Does the aphid see the same explosion of brilliance in the fall foliage that triggered such gifted poetry from Robert Frost? Hardly, according to Lars Chittka ring. Aphids, like all other herbivorous insects studied to date, lack and Thomas Do a long-wavelength or red-sensitive cone. Their three classes of cones are sensitive to wavelengths in the very short (ultraviolet), short (blue), and medium (green) wavelengths (Fig. 1.4). In Figure 1.4D we see how green, yellow, and red leaves from a bird-cherry tree, whose reflectances are illustrated in Figure 1.4B, would excite each of the three classes of aphid photoreceptors. Most animals that perceive true color, or hue, do so with a color opponency system that compares the output from pairs of different cone classes. Behavioral
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Figure 1.4. An analysis of how aphids perceive colored leaves. (A) A leaf reflects light from the sun and is seen by an aphid with green (G), blue (B), and ultraviolet (U) photoreceptors. (B) The reflectance spectra of three different colored leaves from the bird-cherry tree, Prunus padus. To humans, these leaves appear green, red, and yellow. (C ) The wavelengths perceived by the green peach aphid is influenced by the spectral sensitivities of its UV, blue, and green photoreceptors; the tentative spectra are shown here. (D) The degree to which each of these three classes of photoreceptors are excited by the three different leaf colors varies considerably. (E ) This figure shows the summed excitation of the photoreceptors. The integration of the photoreceptors is based on an opponency system with positive input from the green photoreceptor and negative input from the other two receptors. Based on behavioral data, a mechanism of this kind is presumably what many insect herbivores use as a greenness detector. (F ) The summed excitation of the color opponency system by the three birdcherry leaves and a blue-purple flower (Ajuga genevensis) is illustrated on a one-dimensional scale. We see that the yellow leaf produces an even more positive signal from the greenness detector than the green leaf, which contradicts the behavior hypothesis that green and yellow should be perceived quite differently.
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experiments suggest that aphids perceive color by an opponency system with medium versus short wavelength components, with an excitation spectrum as in Figure 1.4E. Insect herbivores generally use such a mechanism as a greenness detector, with positive input through the green photoreceptor and negative ones through the short wavelength receptors. Modeling this color opponency mechanism, the aphids perception of the bird-cherry leaves and a blue flower can be represented in one-dimensional greenness (Fig. 1.4F). As expected, the green elicits a more positive response than red. Whereas yellow and red both appear bright to humans, red appears dull to aphids. Interestingly, insects that rely on such a color opponency system are stimulated even more strongly by yellow than by green. Hence yellow has been referred to as a super-normal foliage-type stimulus. If this is true, then aphids should find yellow attractive and not repellent; in fact, it should be even more attractive than green. This is what was reported as data supporting the original signaling hypothesis: Tree species with more yellow had more aphids. The suggestion that trees use bright colors as warning signals to insects was an insightful and logically consistent hypothesis about the function and adaptive significance of fall foliage. This hypothesis predicts, however, that red and yellow should be less attractive to aphids than green. But the details of the aphids color vision ring paper also notes that there are aphid suggest the opposite. The Chittka and Do species that prefer green to yellow, indicating the possibility of species differences. Nevertheless, knowledge of the mechanisms of insect color perception leads us to dismiss the hypothesis of foliage as an honest signal to herbivores.
Acquisition Informs Evolutionary History

Tinbergens question of evolution asks about the contribution of evolutionary history to current behavior. In many cases, the behavioral similarities between siblings, parents, and offspring, as well as the similarities between different species, result from shared genes that influence the same behavior. The sucking and the grasping reflexes in human neonates, which are shared with all mammals and all primates, respectively, are good examples. Patterns of shared behaviors throughout a familys or a species history often result from genomic transmission across generations. Not all patterns of behavioral inheritance or similarity result from genomic transmission. Behaviors can be culturally transmitted across generations. Song learning in oscines is a good example. Populations of conspecific birds can have distinctively different versions of the same conspecific songdialects. These dialects are not encoded in the genes but result from the combination of song learning and cultural drift due to different copying errors among populations. Similarities in personality in humans, such as the extrovert introvert continuum, can have a substantial genetic component as shown by studies of monozygotic twins. When this is the case, the evolution of the behavior in question can be analyzed using standard population genetic approaches. Whenever there are genetic contributions
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to behavior, however, there is sure to also be an environmental component. These gene-by-environment interactions have made the old nurture nature debate something of an anachronism. It is even more complex when the environmental effect is personified in cultural transmission from mother to offspring.
Cross-Generational Transmission of Stress by Maternal Behavior

A remarkable study of nongenomic transmission of personality-like behavioral traits occurs in rats. There is natural variation in maternal behavior in rats including maternal licking-grooming and arched-back nursing (LG-ABN). The quantity of these maternal behaviors shown by the mother predicts the degree to which these same behaviors will be exhibited by her daughters when they later become mothers. Thus, these maternal behaviors are transmitted across generations. This transmission is not genomic, however. Cross-fostering experiments show that high-LG-ABN females reared daughters who later exhibit high LG-ABN, even though their biological mothers were low-LG-ABN females. Similarly, a pup whose biological mother was high LG-ABN but was raised by a low-LG-ABN mother later matured into a low-LG-ABN mother herself. Thus, mothering style is predicted by a pups adopted, not its biological mother. There is also a correlation between maternal behavior and how offspring behave. Offspring of high-LG-ABN mothers are less fearful as adults and show a more modest hypothalamic pituitary adrenal response in stressful situations. Crossfostering experiments also show that the correlation between these traits is not a genetic one. Behavioral manipulation can bring about the same effect. Handling of pups increases maternal behavior toward the pups and decreases the pups response to stress. The influence of maternal behavior on their offspring in adulthood can also be elucidated at the genomic level. Stress reactivity is modulated by expression of genes in brain areas known to regulate the stress response. In comparison to offspring of low-LG-ABN mothers, the offspring of high-LG-ABN mothers exhibit increased serotonin expression in the hippocampus, which eventually results in the expression of a transcription factor nerve growth factor-inducible protein A (NGFI-A) (Fig. 1.5). NGFI-A then binds to a glucocorticoid receptor gene, which results in increased expression of the hormone receptor in offspring raised by high-LG-ABN mothers. Why is this not a genetic trait? Not all inherited changes in phenotypes are due to changes in DNA sequences. Epigenetics refers to the class of mechanisms responsible for nongenomic inherited changes, and DNA methylation is one of these mechanisms. It plays an important role in gene expression as it can silence a gene without changing its DNA sequence. Demethylation leads to a marked expression of the genes proteins and is a critical component of the epigenetic code. The differences in gene expression associated with stress reactivity between adult rats subjected to high versus low levels of maternal
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Mother High licking/grooming
Pups
Increased serotonin tone and stimulation of 5-HT7 receptor
Demethylation of Nr3c1 exon 1, acetylation of histones around Nr3c1
Increased NGF1-A expression in hippocampus NGF1-A GR Permanent increase in NGF1-A-driven glucocorticoid receptor (GR) expression in hippocampus
Adult High hippocampal glucocorticoid receptor Low glucocorticoid level in response to stress High licking/grooming behavior in adult mothers
Figure 1.5. An illustration of how maternal behavior in rats is transferred epigenetically across generations. A series of traits in adult rats can be traced back to the maternal behavior that they received as pups. High maternal behavior is characterized by high levels of licking and grooming. This natal experience increases the levels of serotonin in the hippocampus, which, in turn, leads to the increased expression of the transcription factor NGF1-A. In addition, there is demethylation of the first exon of the glucocorticoid receptor (GR) gene in the hippocampus, whereas the surrounding histones are acetylated. This creates a glucocorticoid receptor gene that is permanently more open to transcriptional activation by NGF1-A, which eventually results in more glucocorticoid receptors in the hippocampus of the adult rat. It is this difference in the number of receptors that accounts for the differences between endocrine and behavioral features of adult rats that received high versus low levels of maternal behavior when they were pups.
care (LG-ABN) appear to be linked to differences in DNA methylation. These differences were shown to emerge in the first week of life, and, like the behavioral traits, they persist into adulthood and can be reversed with cross-fostering. Exposure to a high-LG-ABN mother causes demethylation of the NGF1-A binding site; however, methylation is not reversed when pups are exposed to low-LG-ABN mothers. This provides the mechanism that allows a long-term effect of NGF1-A gene expression. These results show that maternal behavior, fear response, gene expression, and DNA methylation can all be nongenomically transmitted across generations. If the correlations between these traits within a population were examined using standard breeding value analysis based on mother daughter correlations, or these suites of
13
traits among species were compared using standard phylogenetic character analyses, these patterns of behavioral variation would mistakenly be characterized as having a strong genetic component, whereas in reality these patterns are evidence of cultural evolution through epigenetics and not genetic evolution.
Function Informs Mechanisms

Just as knowledge about mechanisms can inform us about function, the function of behavior can often result in the discovery of mechanisms previously unknown. Two classic examples are echolocation in bats and magnetic orientation in pigeons.
Bats Listening in the Dark

Bats have long had a place in myth and lore because of their nocturnal wanderings. This same behavior has generated curiosity from naturalists who for centuries have asked how bats can fly at such low light levels. A series of very clever experiments by Lazzaro Spallanzani and his colleagues in the 18th century in which bats were deprived of various senses demonstrated quite clearly that bats used neither vision nor odor to navigate. Spallanzani first concluded that bats must have a sixth sense that we will never understand, but later experiments by Swiss naturalist Charles Jurine suggested that they use their hearing. The famous French anatomist Georges Cuvier, however, disagreed. With apparent hubris and without the constraints of data, he declared that the patterns of air currents the bats wings generate during flapping would be disrupted by nearby objects. The touch sensors in the bats wings, he suggested, could then detect these disturbances and use this information for navigation. According to his theory, bats did not reckon by sight or sound, but by touch. The acceptance of this theory seemed to be based only on Cuviers sterling reputation as an anatomist, and some of his acolytes mocked Spallanzanis hearing hypothesis with disdain, asking, If bats see with their ears, do they hear with their eyes? Final resolution of this conundrum had to wait until the middle of the 20th century. Donald Griffin and Robert Galambos, novice graduate students at Harvard University at the time, made use of then recently available techniques to once again ask the question that had preoccupied Spallanzani for so long. They showed that the bats ear was sensitive to ultrasonics (frequencies above the upper human limit of hearing, 20 kHz), that only deaf and silenced bats were unable to navigate an obstacle course, and that successful avoidance was correlated with the bats production of echolocation signals. There seems to be little question that it was the behavior of nocturnal flight that drove scientists to finally uncover the mechanism of echolocation, which almost seems like the sixth sense that Spallanzani once attributed to bats. Recent research by John Zook has suggested that Cuvier might have been partially correct in his assertion that bats see with their wings. Zook showed that the bats wings
14
CHAPTER 1
are, in fact, endowed with touch sensors that contribute to navigation. Merkel cells are common mammalian touch receptors, and bat wings have Merkel-like cells with the addition of a tiny hair protruding from the center. Electrophysiological studies showed that these cells are responsive to air flowing over their surfaces. These cells can be desensitized pharmaceutically. Under these conditions, bats were capable of straightline flight but fumbled badly when confronted with an object they needed to avoid. The philosopher Thomas Nagel asked, What is it like to be a bat, pointing out that although we might be able to understand the mechanisms of echolocation, we could never experience itwe could never really know what it is like to be a bat. Our imaginations now are further challenged in trying to conceive what it would be like to navigate with our skin. In the discovery of echolocation in bats, scientists were motivated by what the animals could do. In the discovery of magnetic orientation in pigeons, they were motivated by what animals could not do.
Pigeons Flying in the Fog

Pigeons are well known for their abilities to home over long distances, which is why carrier pigeons have been used to carry messages for at least 3000 years since their skill was first tapped by the Egyptians and Persians. Understanding how they do this has been the subject of many scientific careers. It was known that pigeons use the sun as an orientation cue. But pigeons can also home successfully on cloudy days. One of the preeminent researchers in this field was William Keeton of Cornell University in Ithaca, New York. Ithaca is characterized by a wealth of overcast days, which allowed Keeton ample opportunity to study homing without the sun. In a typical experiment, pigeons were driven some distance from the loft and released, and their vanishing direction at the release site was noted, as was the time that they returned to the home loft. Although many birds use the position of the sun as an orientation cue, Keetons pigeons usually returned to the home loft on cloudy as well as sunny days, suggesting that there must be another backup navigation system that could guide the birds homeward when the sun was not visible. There was an exception, however. If the pigeons were transported and released by one particular research assistant, the birds tended to vanish. This person drove an old Volkswagen Beetle with the motor in the back. When the cage of birds was placed in the cars back seat, the birds were adjacent to the motor. Keeton surmised that the motors generator might be disrupting the magnetic field in the vicinity, and he decided to determine if the pigeons were using the earths magnetic field in their orientation. He placed small bar magnets on the heads of some pigeons and non-magnetic bars on the heads of others. On sunny days the pigeons were able to return successfully but not on cloudy days. Thus Keeton concluded, and many subsequent studies have confirmed, that pigeons use magnetic cues as a backup system to their use of solar cues.
15
These studies of behavioral mechanisms led to a cascade of studies addressing how animals gain access to the geomagnetic field. Where is their compass and how does it work? A recent summary by Henrik Mouritsen and Thorsten Ritz points out that many birds have two sources for detecting magnetic fields. One is based on light-dependent processes in the eyes, where there are putative magnetosensory molecules, cryptochromes. The other relies on putative magnetosensory clusters of magnetite in the upper beaks of some birds. We will return to a discussion of these mechanisms in Chapter 5. In studies of both bat echolocation and birds, we have stellar examples of how studies of a behaviors function often inevitably lead to further questions about the behaviors underlying mechanisms.
CONCLUSIONS
Animal behavior is a phenomenon that transcends the typical categories that partition the biological sciences. To facilitate understanding between those working at different levels of analysis, Tinbergen codified the study of animal behavior with his four questions: mechanisms, acquisition, function, evolution. Tinbergen also indicated that a complete understanding of animal behavior would need to address each question. In some cases, it appears that a correct understanding of any one question depends on knowledge of the others. It is in that spirit that we offer our view of an integrative analysis of animal behavior.
BIBLIOGRAPHY
Archetti M. 2000. The origin of autumn colours by coevolution. J Theor Biol 205: 625 630. Basolo A. 1990. Female preference predates the evolution of the sword in swordtail fish. Science 250: 808 810. ring TF Chittka L, Do . 2007. Are autumn foliage colors red signals to aphids? PLoS Biol 5: e187. doi: 10.1371/journal.pbio.0050187. Darwin C. 1845. Journal of researches into the natural history and geology of the countries visited during the voyage of H.M.S. Beagle round the world, under the Command of Capt. Fitz Roy, R.N., 2nd ed. John Murray, London (The Voyage of the Beagle). Darwin C. 1859. On the origin of species. Murray, London. Galambos R. 1942. The avoidance of obstacles by flying bats: Spallanzanis ideas (1794) and later theories. Isis 34: 132140. Grant P . 1999. Ecology and evolution of Darwins finches. Princeton University Press, Princeton, NJ. Griffin D. 1958. Listening in the dark. Yale University Press, New Haven, CT. Hamilton WD, Brown SP . 2001. Autumn tree colours as a handicap signal. Proc Biol Sci 268: 1489 1493. Keeton W. 1974. The orientational and navigational basis of homing in birds. Adv Study Behav 5: 47 132.
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Mouritsen H, Ritz T. 2005. Magnetoreception and its use in bird navigation. Curr Opin Neurobiol 15: 406 414. Nagel T. 1974. What is it like to be a bat? Philos Rev 83: 435 450. Nottebohm F . 1996. The King Solomon Lectures in Neuroethology. A white canary on Mount Acropolis. J Comp Physiol A 179: 149156. Podos J. 2001. Correlated evolution of morphology and vocal signal structure in Darwins finches. Nature 409: 185188. Rosenthal GG, Evans CS. 1998. Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size. Proc Natl Acad Sci 95: 4431 4436. Tinbergen N. 1963. On aims and methods of Ethology. Z Tierpsychol 20: 410 433. Weaver IC, Cervoni N, Champagne FA, DAlessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7: 847 854. Zook JM. 2006. Somatosensory adaptations of flying mammals. In Evolution of nervous systems (ed. Kass JH), pp. 215226. Academic Press, Oxford.
Index
A
Acacia ants, 23 24, 24f Acanthodactylus boskianus, 65 Acanthodactylus scutellatus, 65 Acetylcholine, 37 Acquisition of behavior, 35 57 evolutionary history informed by, 10 13, 12f overview of, 35 36 Acromyrmex lobicornis, 220 Adaptive function, 18 25 pagos finches, 4 Adaptive radiation of Gala Adaptive significance of bird songs, 3 as one of Tinbergens four questions, 2f, 3 Aggregation, neural basis of, 201202, 202f Aggression adult social, 215222 infanticide, 235 236 learning and, 231235 neural and hormonal mechanisms of, 227231 in females, 230231 in males, 227 230, 228f, 230f testosterone surge after winning, 231 positive reinforcement of successful, 233 siblicide, 235, 236238 Akre, Karin, 137 Alarm calls evolution of, 198 of ground squirrels, 23, 23f of vervet monkeys, 139 Allelic variation, in genes, 18f Altruism, 22 24 cooperation and, 197204 eusociality, 208211, 209f
green beard gene, influence of, 204205, 206f Hamiltons rule, 199 kin recognition and, 204 205 role of faces in human, 207 Amphibians. See also Frogs call recognition in frogs, 30, 31f, 32, 146 149, 148f, 151 newts (Taricha), 76, 77f sex determination in, 123 Ancestral behaviors, estimating, 30 32, 31f Anglerfish, 187, 188 Anolis lizards conditioned place preference, 234 235, 235f convergent evolution, 28 dewlaps, 27 30, 28f, 29f ecotypes, 28 habituation and sensitization in, 232, 233f Antagonistic pleiotrophy, 162 Anthropomorphism, 138 Ants acacia, 23 24, 24f dear enemy effect, 220, 221f parasite-induced behavior in, 78 79, 78f serotonin effects in, 229 Aphids, color perception by, 8 10, 9f Appetitive behavior, 59 66 caching and hoarding, 62 66, 63f, 65f overview of, 59 60, 60f physiological drive for, 60 62 Aquatic garter snake (Thamnophis sirtalis), 76 77, 77f Archetti, Marco, 8 Arctic tern, migration of, 90 91, 90f Armpit effect, 206 ran, 162 Arnqvist, Go
Page references followed by f denote figures; those followed by t denote tables.
___
245
246
INDEX
Artificial neural networks, simulating brain evolution with, 32 Asexual reproduction, 122 Associated reproductive pattern, 129 130, 130f, 133 Assortative mating, 21 Attractiveness, heritability of, 176 Auditory cues, and parental behavior, 194195, 195f Auditory hunting by owls, 69 71, 70f, 72f Audubon, John, 99
B
Bacteria, orientation along magnetic fields, 113 Barn owl (Tyto alba), auditory hunting by, 69 71, 70f, 72f Bartness, Timothy, 61 Basolo, Alexandra, 6 Bateman, Angus J., 160 Batemans principle, 161, 161f, 187 Bats echolocation in, 13 14, 39 touch sensors in wings, 13 14 Bayesian inference, 26 pagos finches, 4 5, 5f Beak morphology, of Gala Beecher, Michael, 152, 154 Bees eusociality in, 209211, 209f neuromodulation in, 49 Behmer, Spencer, 84 Beltian bodies, 24, 24f Berthold, Arnold Adolph, 128 Berthold, Peter, 93 Biological species concept, 143 Birds. See also Birdsong; specific species auditory hunting by owls, 69 71, 70f, 72f pagos finches, 4 5, 5f beak morphology of Gala caching, 62 66, 63f, 65f cooperative breeding in, 198 199, 237 cooperative sexual displays, 199, 200f dear enemy effect, 220221 female social aggression, 230 magnetic sensing in, 14 15, 113116, 113f migration in, 90 99, 90f, 94f, 101, 103f monogamy in, 183185, 187, 188, 196 navigation by, 108 overproduction of young, 237 288 parental behavior in, 190191, 191f, 196 seasonality and, 131 132, 132f sex determination in, 123 siblicide in, 236238 territoriality, 217 Tinbergens four questions applied to singing, 2 3, 2f
Birdsong beak morphology influence on, 5 developmental stress effect on, 170171 dialects, 10, 17, 160 female preference for complex, 173174 as function of habitat, 134, 135f of great tits, 134, 135f learning, 151 154, 152f neural plasticity and, 50 51 signal variation and physiological response, 159 160 Tinbergens four questions applied to, 23, 2f Blackcap (Sylvia atricapilla), 93 96, 94f Blue-footed booby, siblicide in, 238 Born to Sing: An Interpretation and World Survey of Bird Song (Hartshorne), 174 Brain evolution, simulating with artificial neural networks, 32 Brain masculinization, 227228 Breeding, cooperative, 197, 198199, 237 Brenowitz, Eliot A., 50, 152, 154 Brodie, Edmund D., III, 76 Brooding behavior, 190 191 Brood pheromone, 49 Bruce, Hilda M., 235 Bruce effect, 235 Bufo. See Toads Buhl, Jerome, 101 Bullfrog (Rana catesbeiana), call recognition in, 146 147, 148f, 151 Bullhorn acacias, 23 24 Burmeister, Sabrina, 159
C
Caching, 62 66, 63f, 65f Caenorhabditis elegans, sex determination in, 124 Call recognition, neural mechanisms of, 146 151, 148f, 150f Canaries, 159, 160 Capranica, Robert, 146147, 151 Caretta caretta (loggerhead sea turtles), navigation by, 115, 116f Carolina wrens (Thryothorus ludovicianus), dear enemy effect in, 221 Castration, aggression reduction with, 227, 228f Causation, 35 Celestial compass, 114 Central nervous system (CNS), 41 Central pattern generators (CPGs), 42 44, 43f, 48 49, 53 Cervus elaphus (red deer), territoriality in, 216 217, 216f Cheney, Dorothy, 139
INDEX
247
Cheng, Mae-Feng, 157, 158 Chittka, Lars, 8, 10 Chorus frogs, mating calls of, 145146, 145f Christy, John, 175 Cichlid fish coloration of, 135, 136f, 137 sexual imprinting in, 154156, 155f Circadian rhythms calibration of navigation compass, 114 described, 101 in Drosophila, 53 seasonality and, 131 Circuits, neural, 37, 42 Clayton, David, 174 Climate change, influence on migratory behavior, 93 Cnemidophoris uniparens (whiptail lizard), 124, 159 CNS (central nervous system), 41 Coevolution of predator and prey, 76 77, 77f Red Queen effect, 21 Color vision, 8 10, 9f Communication, 133139 degradation and attenuation of signal, 134 human language and music metaphor, 138139 mate recognition, 144 156 reproductive synchronization, 156 160 signal-receiver adaptations for active space, 134137, 136f signal-receiver adaptations for active time, 137138 signal reliability, 169172, 170f Comparative studies of adaptation, 27 30 Compass, navigation by calibration, 114 earths magnetic field, 112 114, 113f sensing polarized light as, 108112, 110f sun and star, 108, 109f Competition, migration due to, 91 Concorde Fallacy, 83 Conditioned defeat behavior, in Syrian hamsters, 225, 225f Conditioned place preference, 233235, 234f Conflict, aggression and, 215 238 Control of behavior, 36 57 experiential and environmental, 55 57 genetic, 52 55, 54f hormonal, 51 52 neural, 36 51 Convergent evolution, in Anolis lizards, 28, 30 Cooperation altruism and, 197 204 breeding, cooperative, 197, 198199, 237 eusociality, 208211, 209f
neural basis of, 201 204, 202f, 203f sibling, 199 Cooperative reproduction, in eusociality, 208211, 209f Cost of males, 122 Courtship cooperative sexual displays, 199, 200f display in fiddler crabs, 175, 175f indirect benefits to females, 162, 162f versus parental care, trade-off in, 195196 in ringdoves, 157 158, 157f signal reliability, 169 species-specific traits, 144 Cowbirds, 191 Cox, George, 91 92 Coyne, Jerry, 143 CPGs (central pattern generators), 4244, 43f, 4849 Craig, Wallace, 59 Crews, David, 129 Cricket acoustic communication, 149151, 150f Crop milk, 190 Crustaceans, parasite-induced behavior in, 79 Cryptochromes, 15 CsA gene, 205 206, 206f Cuckoos, sensory exploitation in, 173 Cue-based learning, 62 64 Cultural transmission of behaviors, 10 Cummings, Molly E., 173 Cuvier, Georges, 13 Cyprinodon variegatus ( pupfish), dear enemy effect in, 221, 222f
D
Dacelo novaeguineae (laughing kookaburra), 237 Darwin, Charles descent with modification, 18, 25, 26 pagos finches, 4 5, 5f Gala on sounds, 174 theory of natural selection, 18, 19 theory of sexual selection, 6, 19, 160, 163 Dawkins, Richard, 24, 83, 139, 205, 206 Day, Lainy, 65 Day length, reproductive seasonality and, 131133 Dear enemy phenomenon, 219 222, 221f, 222f Decision circuit, in toad brain, 69 Defeat, response to social, 225227, 225f, 226f Delville, Yvon, 225226 Density-dependent selection, in Drosophila foraging, 87 The Descent of Man and Selection in Relation to Sex (Darwin), 19 Desert locusts, migration of, 99, 100101, 102f Dewlaps, Anolis, 27 30, 28f, 29f
248
INDEX
DHT (dihydrotestosterone), 125, 227228, 230 Dialects, in birdsong, 10, 17 Dictyostelium discoideum, 205 206, 206f Dihydrotestosterone (DHT), 125, 227228, 230 Dinoflagellates, 77 Direct selection, 20, 21, 167 Disassociated reproductive pattern, 129130, 130f Disassortative mating, 171 Diurnal migrators, 108 DNA methylation, 11 12, 12f Dominance, 222 227 Dominance hierarchies, 222 223 Dopamine neuromodulator, 47, 48 neurotransmitter, 37 as reinforcer of aggression, 231 ring, Thomas, 8, 10 Do Drosophila genetic basis of behavior, 53 genetics of foraging behavior, 86 87 neuropeptide F effects in, 61 period gene, 176 Drosophila melanogaster courtship call of, 53, 54f segregation distorter, 24, 25f Drosophila sechellia, foraging by, 53 Drosophila simulans foraging by, 53, 75 heritability of attractiveness, 176 Drummond, Hugh, 238 Dugatkin, Lee A., 55
E
Ear cricket, 149, 150f ear, 147, 148f frog, 173 matched filter hypothesis, 147 Earths magnetic field as a compass, 112114, 113f Echolocation in bats, 13 14, 39 Electrical synapses, 37 Electric fish, 4041, 40f, 44 46, 45f Electric organ discharge, 40 41, 40f, 44 46, 45f Electroreception, 39 41, 40f active, 40 41 magnetic sensing and, 113114 passive, 40 Elephant, sexual dimorphism in, 188 Emlen, J. Merritt, 80 Emlen, Stephen, 108 Emlen funnel, 93, 95, 108 Environmental control of behavior, 55 57 Epigenetics, 11 13
Epinephrine, 37, 48 Estrogen aggression facilitation by, 230231 maternal behavior and, 190, 192 reproductive synchronization and, 158 role in sexual differentiation, 125 126, 126f seasonality in levels of, 133 testosterone conversion to, 125, 126, 227228, 230 Eusociality, 208211 in honeybees, 209211, 209f similarity to polyandry, 187 Evans, Christopher, 6 E-vector, 109112, 110f Evolution. See also Evolutionary history of aposematic signaling, 76 pagos finches, 4 5, of beak morphology of Gala 5f coevolution of predator and prey, 76 77, 77f convergent in tetrodotoxin producers, 76 77 of cooperative behavior, 197199 of defense mechanisms in prey, 76 definition, 17, 22 of eusociality, 210 forces causing, 17 of four-chambered heart, 26 of gift giving in males, 173 of migration, 91 93 modern synthesis, 143 natural selection, 18, 18f optimal foraging and, 85 87 of pit organs in snakes, 71, 73 of polyandry, 187 of polygyny, 186187, 189 Red Queen effect, 21 of sex, 122 of sexual dimorphism, 187 sexual selection, 19 21 of sexual strategies, infanticide and, 236 siblicide and, 237 Evolutionary history comparative studies, 27 30, 28f, 29f estimating ancestral behaviors, 30 32, 31f evolutionary pattern, 26 27 function informed by, 6 7, 7f informed by acquisition, 10 13, 12f as one of Tinbergens four questions, 2f, 3 of songbirds, 3 rg-Peter, 67 Ewert, Jo Experience effect on mate recognition, 154 156, 155f mate-choice copying, 55 57, 56f as outcome determinant in social aggression, 224 227, 225f, 226f Extra-pair matings, 188, 196
INDEX
249
F
Faces, role in human altrusim, 207 Fall foliage color, 8 10, 9f Farrell, William J., 234 Felsenstein, Joseph, 30 Female aggression, mechanisms of, 230231 Female mate choice, 20 21 attraction to elaborate traits, 163, 167, 175 in fiddler crabs, 175, 175f leks, 168 preferences, heritability in, 176 signal reliability, 169172, 170f in swordtails, 67, 7f Females mating strategies, 160163 sex determination, 123 128 Fiddler crabs, 175, 175f Field crickets (Teleogryllus spp.), mate guarding in, 218 Fish coloration of cichlids, 135, 136f, 137 electric, 40 41, 40f, 44 46, 45f electroreception, 39 41, 40f mate-choice copying, 56, 56f olfactory, imprinting in, 106108, 107f polarized light sensed by, 112 sex determination, 124 sexual imprinting in cichlids, 154 156, 155f Fisher, Ronald, 21, 172, 199 Fitness components of, 18, 19 inclusive, 22, 197 198, 209 natural selection and, 18, 19 Fixed action patterns, 59, 66 Follicle-stimulating hormone (FSH), 158 Food amount hypothesis, for siblicide, 238 Food preferences, 75 77, 77f Foraging, 59 87 appetitive behavior, 59 66 caching and hoarding, 62 66, 63f, 65f overview of, 59 60, 60f physiological drive for, 60 62 consummatory behavior auditory hunting in owls, 69 71, 70f, 72f common patterns in sensory basis of prey capture, 74 infrared prey sensing by snakes, 71, 7374, 73f overview of, 59 60, 60f visual prey capture in toads, 66 69, 67f, 68f exploitative, 77 79 food preferences, 75 77, 77f optimal, 79 87, 82f, 84f, 85f, 86f parasite-induced behavior, 77 79, 78f
Four-chambered heart, evolution of, 26 Fox, James H., 151 Frishkopf, Lawrence S., 146 ngara frogs Frogs. See also Tu call recognition in, 30, 31f, 32, 146 149, 148f, 151 ear, 173 green tree frogs (Hyla cinerea), 159 Fruit flies. See also Drosophila Batemans principle, 160161, 161f FSH (follicle-stimulating hormone), 158 Function adaptive, 18 25 evolution of behavior and, 17 33 informed by evolutionary history, 6 7, 7f informed by mechanism, 810, 9f, 13 15
G
GABA (gamma-aminobutyric acid), 37 Galambos, Robert, 13 pagos finches, beak morphology of, 45, 5f Gala Gamete size, 161 Game theory model, 8 Gamma-aminobutyric acid (GABA), 37 Gammarus lacustris, 79 Gap junctions, 37 Gene expression, differences in, 53 55 Genetic control of behavior, 52 55, 54f Genetic relatedness, in haplodiploid systems, 209f, 210211 Genetics of migratory behavior, 93 97 Genetic variation, generated by sexual reproduction, 122 Gene variants, 53 Genomics, mating system, 176179, 178f Ghrelin, influence on foraging behavior, 61 Glutamate, 37 Glycine, 37 Glycogen, depletion during migration, 98 GnRH (gonadotropin-releasing hormone), 158 Goddard, Renee, 221 Goldstein, Jr., Moise H., 146 Golgi tendon organ, 42f Gonadal steroid hormones aggression and, 227231, 228f, 230f influence on migration, 103 as neuromodulators, 48 organizationalactivational effects of, 51 52 parental behavior and, 189193, 191f role in sex determination, 125 130, 129f, 130f seasonality in levels of, 133 Gonadotropin-releasing hormone (GnRH), 158 Goodson, James, 201 202 Gould, John, 4
250
INDEX
Gray, John, 163 Great tits foraging decisions of, 82 83, 82f songs of, 134, 135f Green anole lizards (Anolis carolinensis). See Anolis lizards Green beard genes, 205206, 206f Greenness detector, 9f, 10 Green tree frogs (Hyla cinerea), 159 Greylag geese, 152 Griffin, Donald, 13 Griffith, Simon C., 188 Ground squirrels (Spermophilus lateralis), 23, 23f, 132 Gru sser-Cornehls, Ursula, 67 Gut, regression in migrating birds, 98 Gymnotids, 40, 40f, 44 45
H
Habituation aggression learning, 232 birdsong and, 174 Haig, David, 205 Haldane, J.B.S., 22 23 Hamilton, W.D., 8, 22, 197198, 205, 237 Hamiltons rule, 22, 199 Hamsters aggression in conditioned defeat behavior, 225, 225f development of aggression, 225226, 226f hormonal mechanisms, 228229 foraging behavior, 61 hoarding, 62 Handicap principle, 169 170, 172, 175 Haplodiploid determination system, 123, 209210, 209f, 211 Hartshorne, Charles, 174 Hasler, Arthur, 106 Hawryshyn, Craig W., 112 Hearing, mammalian, 38 39, 38f Heart, evolution of four-chambered, 26 Hebets, Eileen, 156 Heritability, 19 Hermaphrodites, 124 Heterospecific matings, 144, 145 Hippocampus, memory formation and, 6465, 65f Hoarding, 62 Hoke, Kim, 149 Home range, 216 Honest signal, 8, 169 Honeybees, eusociality in, 209 211, 209f Hormonal control of behavior activational effects, 51 52 organizational effects, 51 52
Hormones. See also specific hormones activational role in sex differentiation, 128 130, 130f organizational role in sex differentiation, 125 128, 126f releasing, 52 reproductive synchronization by, 156160, 157f seasonality, influence of, 133 trophic, 52 Hosken, David, 176 Hrdy, Sarah Blaffer, 236 Huber, Franz, 149, 151 Huhman, Kim, 225 Humans altruism, role of faces in, 207 effect of oxytocin in cooperative behavior and trust, 203 204 language, 138 139 mate choice, 171 Hunger, 60 62 Hunting. See also Prey capture auditory by owls, 69 71, 70f, 72f cooperative, 197, 198 5-hydroxytryptamine 1 (5-HT1) receptors, 229 Hyenas, siblicide in, 238 Hyman, Jeremy, 220 Hyperphagia, of premigratory birds, 98
I
Imaizumi, Kazuo, 149 Imprinting described, 106 filial, 152 of mate recognition, 154 156, 155f olfactory, 105 108, 107f Inbreeding avoidance, 171 Inclusive fitness, 22, 197 198, 237 Indigo bunting (Passerina cyanea), navigation by, 108, 109f Indirect selection, 21 Infanticide, 235 236 Infidelity, in social monogamy, 188 Infrared prey sensing by snakes, 71, 7374, 73f Ingle, David, 67, 69 Insects. See also specific species eusociality in, 208211, 209f migration of, 99 101, 102f, 103, 104, 105f neuromodulation in, 49 pollinators, 167 sensing polarized light, 110f, 111 sex determination in, 123 winged wingless dimorphism, 96 97, 97f Insurance hypothesis, 237 238
INDEX
251
Invertebrates polarized light sensed by, 109111, 110f sex determination in, 123, 124 Irrational choice, causes of, 83 Isotocin, 201
J
Jacanas, sexual dimorphism in, 188 Jamming avoidance response (JAR) of electric fish, 44 45, 45f Japanese macaques, infanticide in, 236 Jennions, Michael, 176 Jurine, Charles, 13 Juvenile hormone, 49, 103 104
K
Kacelnik, Alex, 84 Kallman, Klaus, 176, 177 Keeton, William, 14 Kin recognition, 171, 204207 Kin selection, 22 24 Kirsch, Peter, 203 Knudsen, Eric, 71 Krakauer, Alan, 199 Krebs, John, 82, 139
Light, sensing polarized, 108 112, 110f Linkage disequilibrium, 21 Liu, Robert C., 194 195 Lizards. See also Anolis lizards foraging by, 65 leopard geckos, sex determination in, 128 whiptail lizards (Cnemidophoris uniparens), 124, 159 Locusts food preference influences in, 84 85, 84f, 85f migration of, 99, 100 101, 102f Loggerhead sea turtles (Caretta caretta), navigation by, 115, 116f Lohmann, Kenneth J., 115, 116f Lorenz, Konrad, 1, 106, 152 Losos, Jonathan B., 27 Luteinizing hormone (LH), 158 Lynch, Kathleen S., 149
M
MacArthur, Robert H., 80 MacDougal-Shackleton, Elizabeth, 159 MacDougal-Shackleton, Scott, 159 Magnetic field, of earth as compass, 112 114, 113f Magnetic orientation in pigeons, 14 15 Magnetic sensing, 14 15, 112117, 113f, 115f Magnetite, 113, 113f Major histocompatibility complex (MHC), 171172, 204 Mak, Gloria K., 50 Male female bonding, 183189 monogamy, 183185 polygyny and polyandry, 185188 promiscuity, 183 185 sexual fidelity versus social bonding, 188 189 Males aggression, mechanisms of, 227 230, 228f, 230f cost of, 122 mating strategies, 160163 sensory exploitation, 173 sex determination, 123128 Mammals hearing in, 38 39, 38f parental behavior in, 191 195, 192f, 195f polyandry in, 187 sex determination in, 123 sexual differentiation in, 125127, 126f siblicide in, 236 Manakins, cooperative sexual displays by, 199, 200f Maps, navigation by, 114117, 115f Markings, territorial, 218
L
Langen, Tom A., 220 Laughing kookaburra (Dacelo novaeguineae), 237 Learning aggression and, 231 235 conditioned place preference, 233235, 234f habituation and sensitization, 232, 233f positive reinforcement of success, 233 cue-based, 62 64 mate recognition, 151 156 neural plasticity, 49 51 optimal foraging and, 83 85, 84f, 85f of song by birds, 3 spatial, 62 65, 63f taste aversion, 75 76 Lehrman, Daniel, 157, 158, 197 Leiser, John K., 221 Leks, 167168, 219, 219f Lemon, William C., 86 Leopard geckos, sex determination in, 128 Lettvin, Jerome Y., 66 67, 146 LH (luteinizing hormone), 158
252
INDEX
Marler, Peter, 139, 152 Mass migration, 99 101, 102f Matched filter hypothesis, 146 147 Mate attraction, cooperation in, 199, 200f Mate choice. See also Sexual selection MHC influence on, 171 predation risk effect on, 175, 175f sexual selection, 20 21 signal reliability, 169172, 170f in swordtails, 67, 7f Mate-choice copying, 55 57, 56f, 75 Mate guarding, 218 Mate recognition learning, 151156 neural mechanisms of, 146 151, 148f, 150f reproductive character displacement, 144146, 145f species recognition, 144 Maternal behavior. See also Parental behavior aggression, hormonal influences on, 230231 cross-generational transmission of stress by, 11 13, 12f Mathematical models of behavior, 8083 Mating assortative, 21 disassortative by MHC type, 171 experience overriding physiology in behaviors, 196 Mating calls character displacement, 145146, 145f of chorus frogs, 145 146, 145f neural mechanisms guiding recognition of, 146151, 148f, 150f signal variation and physiological response, 159160 ngara frogs, 30, 31f, 32, 137138, of tu 207208, 208f Mating strategies, sexual differences in, 160163 Mating systems female mate choice, 167 infanticide in single male systems, 235 lek, 167168 monogamy and promiscuity, 183185 polygyny and polyandry, 185 188 Maximum likelihood technique, 26 Mayr, Ernst, 143 McBride, Carolyn, 53 Mechanism of behavior, 35 57 genetic control of behavior, 52 55, 54f hormonal control of behavior, 51 52 informed by function, 8 10, 9f, 13 15
neural control of behavior, 35 51 overview, 35 36 Medial preoptic area, brain, 229 Meiotic drive, 24, 25f Memory, caching and, 62 65 cue-based, 62 64 spatial, 62 65, 63f Men Are from Mars, Women Are from Venus: A Classic Guide to Understanding the Opposite Sex (Gray), 163 Merkel cells, 14 Mesocricetus auratus (Syrian hamster), aggression in, 225 227, 225f, 226f Mesotocin, 201, 202f Metathoracic ganglion, 100 MHC (major histocompatibility complex), 171 172, 204 Mice Bruce effect, 235 MHC variant recognition, 171 Migration, 89 104 of Arctic terns, 90 91, 90f of blackcaps, 93 96, 94f of desert locusts, 99, 100101, 102f diurnal, 108 environmental and physiological triggers, 101, 103 104, 103f evolution of, 91 93 genetic bases of, 93 97 mass, 99 101, 102f of Mormon crickets, 99 100 of moths, 104, 105f orientation and navigation methods, 104 117 physiological and neural preparations for, 97 99 of salmon, 97 98, 99, 106 of sea turtles, 115, 116f traits involved in, 89 Migratory restlessness, 93, 98, 109f. See also Zugunruhe Mole rats, 208, 210 Monogamy, 183185 Mormon crickets migration, 99 100 nuptial gift, 167 resources in sperm package, 162, 162f Mormyrids, 40, 40f, 44 Morton, Eugene, 134 Moths, migration of, 104, 105f Motor control, 41 47, 43f, 45f Mouritsen, Henrik, 15 Mu llerian duct system, 125, 126f Muscle reflexes, 41 42, 42f
INDEX
253
Mutation, 18, 18f, 19 Mutualisms, 23
NPY (neuropeptide Y), regulation of hunger by, 61 62 Nuptial gifts, 167, 173
N
Nagel, Thomas, 14 Natural selection described, 18, 18f, 19 sexual selection and, 1920 Navigation, 104117 compass calibration of, 114 earths magnetic field, 112114, 113f sensing polarized light as, 108112, 110f sun and star, 108, 109f magnetic sensing, 112117, 113f, 115f mass, 114117, 115f neural basis of, 117 olfactory imprinting, 105 108, 107f subtle orientation, 104105, 105f Nerve growth factor-inducible protein A (NGFI-A), 11 12, 12f Nervous system, organization of, 36 Nesting, territorial behavior during, 217 Nest parasites, 191 Neural control of behavior mate recognition, 146 151, 148f, 150f motor control, 41 47, 42f, 43f, 45f sensory processing, 37 41, 38f, 40f variation in, 47 51 modulation, 47 79 plasticity, 49 51 Neural plasticity, 4951 Neurogenesis, 50 Neuromodulators, 4749 Neurons electrical synapses, 37 electrosensory, 39 motor, 41 42, 42f, 43f neurotransmitters, 36 37, 39 omega, 151 pacemaker, 42 sensory, 41 42, 42f, 43f Neuropeptide F (NPF), 61 Neuropeptide Y (NPY), regulation of hunger by, 61 62 Neurotransmitter, 3637, 39, 47 Newts (Taricha), 76, 77f NGFI-A (nerve growth factor-inducible protein A), 11 12, 12f Norepinephrine, 37, 48 Nowicki, Steve, 170 NPF (neuropeptide F), 61
O
Observational learning learned taste aversions overcome by, 75 in social aggression, 223 224, 224f Occams razor, 26 Octopamine, 37, 49 Olfaction in kin recognition, 204 in parental behavior, 193 194 Olfactory imprinting, 105 108, 107f Oliveria, Rui, 223 Ommatidia, 110f, 111 On the Origin of Species (Darwin), 18, 19 Ontogeny, 35 Opponency system, color, 8, 9f, 10 Optic tectum, 68, 68f, 71, 72f Optimal foraging, 79 87, 82f, 84f 86f assumptions about evolution, 85 87 assumptions about learning, 83 85 basic model, 80 81 testing the model, 8183, 82f Orchids, deceptive, 167, 168f, 173 Orientation. See also Navigation of bacteria along magnetic fields, 113 of indigo buntings during migratory restlessness, 109f subtle, 104105, 105f testing with Emlen funnel, 93, 95 Orr, H. Allen, 143 Owens, Ian P .F ., 188 Owls, auditory hunting by, 69 71, 70f, 72f Oxytocin activational effects of, 51 cooperative behavior and, 201203 as neuromodulator, 48, 51 parental behavior and, 193, 194
P
Parasites, behaviors induced by, 77 79, 78f Parental behavior, 189 197 auditory cues, 194 195, 195f behavioral experience, influence of, 196197 courtship versus parental care, trade-off in, 195196 neural and hormonal changes, 189195 in birds, 190191, 191f in mammals, 191 195, 192f, 195f
254
INDEX
Parental behavior (Continued) olfactory signals, 193 194 parental bonding and parental care distinguished, 189 somatosensory signals, 194 Parsimony, 26, 30 Partridge, Linda, 162 Passenger pigeon, 99 Passerculus sandwichensis (Savannah sparrows), calibration of navigation compass in, 114 Passerina cyanea (indigo bunting), navigation by, 108, 109f Passerine birds, hyperphagia of premigratory, 98 Peacocks, 169170, 170f Peptide hormones, activational effects of, 51 Perceptual world, 37 41 Period gene, 53, 176 Petrie, Marion, 176 P gene, in swordtails, 177 Pheidole gilvescens, 220 Pheidole tucsonica, 220 Phelps, Steven M., 32 Pheromone, honeybee, 211 Photoperiod, reproductive seasonality and, 131133 Photopigments, 109, 110f, 111, 135, 172173 Phylogenetically independent contrasts, 30 Phylogenetics, 26 30, 29f Phylogenetic tree, 26, 27 Pianka, Eric R., 80 Pigeons homing, 114, 115 116 magnetic orientation in, 14 15 Pipefish, 161f, 162 Pit organs, 71, 73 74, 73f Pit vipers, infrared prey sensing by, 71, 73 74, 73f Plasticity, neural, 49 51 Platyfish, 6, 7f Play fighting, in hamsters, 225226, 226f Podos, Jeffrey, 5 Polarized light, as navigation compass, 108 112, 110f Pollack, Gerald S., 149 Pollination, 167 Polyandry, 185 188 Polygyny, 185 188 in red deer, 217 territorial aggression and, 217 Polymorphus paradoxus, 79 Potts, Wayne, 171 Predation risk, effect on female mate choice, 175 Predators avoidance behavior in toads, 66 foraging, effect on, 61
Pretectum, 68, 68f, 69 Prey optimal foraging, 79 87, 82f, 84f 86f tetrodotoxin as predatory defense, 76 77, 77f Prey capture auditory hunting in owls, 69 71, 70f, 72f common patterns in sensory basis of, 74 infrared prey sensing in snakes, 71, 7374, 73f visual in toads, 66 69, 67f, 68f Primary sexual characteristics, 52, 163 Primates dominance hierarchies in, 223 infanticide, 235, 236 Profitability, in optimal foraging model, 80 83, 82f Progesterone aggression inhibition by, 231 maternal behavior and, 190, 192 Prolactin in birds, 158, 190, 191f in mammals, 191f, 193 Promiscuity, 183185, 185f, 236 Pseudoacris spp., mating calls of, 145146, 145f Pufferfish, 76, 77 Pulido, Francisco, 93 Pundamilia spp., 155, 155f Pupfish (Cyprinodon variegatus), dear enemy effect in, 221, 222f
Q
Queen mandibular protein, 211 Queller, David, 205, 206
R
Rana catesbeiana, call recognition in, 146 147, 148f, 151 Rand, A. Stanley, 173 Rats masculinization of embryos in, 127, 127f parental behavior in, 11 13, 12f, 191192, 192f, 193, 194195, 195f taste aversion learning, 75 Reciprocal altruism, 23 Red deer (Cervus elaphus), territoriality in, 216 217, 216f Red Queen effect, 21 Reflex circuits, 41 42, 42f Regan, C. Tate, 187 Releasing factors/hormones, 52 Reproduction associated and disassociated patterns, 129 130, 130f infanticide and, 235236
INDEX
255
insurance hypothesis and overproduction of young, 237238 seasonality in, 130 133 short-day and long-day breeders, 31 Reproductive character displacement, 144146 Reproductive synchronization, 156160 Reptiles, sex determination in, 124 Resource management, migration as mechanism of, 101 Retinal mapping, 68 69 Rice, William, 162 Ringdove, reproductive synchronization in, 157158, 157f Ritualized displays, territoriality and, 217 218 Ritz, Thorsten, 15 Robinson, Gene, 49 Rodents. See also specific species hoarding in, 62 parental behavior in, 191192, 192f, 193, 194195, 195f Rolshausen, Gregor, 96 Rosenthal, Gil, 6, 177 Rowe, Locke, 162 Runaway sexual selection, 21, 172 Ryan, Michael J., 30, 173, 177, 207
S
Sabourin, Patrick, 149 Sage grouse, 219, 219f Sailfin mollies, mate-choice copying in, 56 Sakaluk, Scott, 173 Salmon migration of, 97 98, 99, 106 olfactory imprinting in, 106 107, 107f Savannah sparrows (Passerculus sandwichensis), calibration of navigation compass in, 114 Schartl, Manfred, 177 Schizocosa uetzi (wolf spider), 156 Scholz, Allan T., 107 Searching activities, appetitive behaviors as, 60 Sea slug Aplysia, 124 Seasonality, 130133 environmental triggers, 131133 hormonal mediation of, 133 Sea turtle migration, 115, 116f Secondary sexual characteristics, 52, 163 Seehausen, Ole, 135 Segregation distortion, 24, 25f Selection. See also Sexual selection agent of, 20, 21 direct, 20, 21, 167
indirect, 21 kin, 22 24 sexual, 19 21 target of, 20, 21 Selfish genes, 24 The Selfish Gene (Dawkins), 24, 205 Sensitization, aggression learning and, 232 Sensory exploitation, 172 Sensory processing, 37 41 electroreception, 3941, 40f hearing in mammals, 38 39, 38f Serotonin aggression and, 227, 229230, 230f as neuromodulator, 47, 48 49 as neurotransmitter, 37, 47 in parasite infections of crustaceans, 79 Sessile organisms, 89 Sex, evolution of, 122 Sex chromosomes, 123, 124 Sex determination, 123 124 environmental, 123, 124 genetic, 123 haplodiploid system, 123, 209210, 209f, 211 temperature-dependent, 124, 128 Sex differences, 121130 activational role of hormones, 128130, 130f organizational role of hormones, 125 128, 126f sex determination, 123124 Sex hormones. See Gonadal steroid hormones Sex role reversal, 162 Sexual communication mate recognition, 144156 reproductive synchronization, 156160 Sexual conflict, 162 Sexual differences in mating strategies, 160163 Sexual dimorphism abundance of, 163 examples of, 166f in polygyny and polyandry, 187188 territoriality and, 217218 Sexual fidelity, 188 189 Sexual reproduction, genetic variation generated by, 122 Sexual selection behaviors generating, 163168 described, 19 21 evolution of weapons, 163, 164f165f runaway, 21, 172 sensory exploitation, 173 sexual differences in mating strategies, 160163
256
INDEX
Sexual selection (Continued ) sexual dimorphism examples, 166f signal complexity, favoring of, 173174 Seyfarth, Robert, 139 Sheep, mother infant bonding in, 194 Sherman, Paul W., 23 Sherrington, Charles Scott, 60 Siamese fighting fish (Betta splendens), 223, 224f Siblings cooperation among, 199 siblicide, 235, 236238 Signal reliability, 169 172 Sign-stimulus-evoked fixed action patterns, 66 Silent mutations, 53 Slime mold, 205 206, 206f Smith, John Maynard, 122 Snakes aquatic garter snakes (Thamnophis sirtalis), 76 77, 77f infrared prey sensing by, 71, 7374, 73f Social aggression, 215 222 conditioned defeat behavior, 225, 225f dear enemy phenomenon, 219 222, 221f, 222f dominance hierarchies, 222 223 experience as determinants of winners and losers, 224227, 225f, 226f female, 230 231 juvenile experiences, importance of, 226227, 226f leks and display sites, 219, 219f male, 227230, 228f, 230f mate guarding, 218 neural and hormonal mechanisms of, 227231 in females, 230231 in males, 227 230, 228f, 230f testosterone surge after winning, 231 reproduction, link to, 215, 227, 238 territoriality, 216 218 Social bonding cooperation, 197 204 eusociality, 208 211, 209f kin recognition, 204 207 male female, 183189 parent offspring, 189 197 sexual fidelity versus, 188 189 species recognition, 207 208, 208f Sokolowski, Maria, 86 87 Soltis, Joseph, 236 Somatosensory signals, parental behavior and, 194 Songbirds, song learning in, 151 154, 152f
Sound localization in barn owls, 69 71, 70f, 72f perception of, 38 39, 38f Spalding, Douglas Alexander, 106 Spatial learning/memory, 62 65, 63f Speciation behavioral contributions to, 144 sympatric, 95 96 Species, definition of, 143 Species recognition, 144, 207208, 208f Spencer, Herbert, 19 Spermatophore, 218 Sperm competition, 218 Spotted hyenas, siblicide in, 238 SRY gene, 123, 125, 126, 126f Starling (Sturnus vulgaris), migration of, 108 Star patterns, as compass, 108 Stein, V .W., 96 Steroid hormones. See Gonadal steroid hormones Strassmann, Joan, 205 Stress cross-generational transmission by maternal behavior, 11 13, 12f developmental stress effect on birdsong, 170 171 Stretch reflex, 41 42, 42f Sturnus vulgaris (starling), migration of, 108 Submissive behavior, 223226, 225f Subordinates, 222 226, 225f Sun, as compass, 108 Sunk-costs fallacy, 83 Superb fairy-wren (Malurus cyaneus), 196 Supergenes, 205 Surfperches, 173 Survivorship, 18, 19 Survivorship costs of traits, 169170 Swordtails genetics of body size in, 176179, 178f mate choice in, 6 7, 7f, 173 Sylvia atricapilla (blackcap), 93 96, 94f Sympatric speciation, 95 96 Synapse, 36 37 Syrian hamsters (Mesocricetus auratus), aggression in, 225 227, 225f, 226f Syrinx, morphology of songbird, 2f, 3
T
Tadpoles, kin recognition in, 204 Taeniopygia guttata. See Zebra finch Taste aversion learning, 75 76 T5 cells, 68 TDF (testes-determining factor), 125 Teleogryllus spp., 149, 218
INDEX
257
Temeles, Ethan J., 220 Ten Cate, Carel, 155 Territoriality dear enemy phenomenon, 219 222, 221f, 222f marking, 218 in polygynous systems, 217 in red deer, 216217, 216f ritualized displays, 217 218 in Syrian hamsters, 225 Testes-determining factor (TDF), 125 Testosterone aggression facilitation by, 227230, 228f, 230f bird eggs supplemented with, 160 conversion to estrogen, 125, 126, 227228, 230 elevation in response to conspecific calls in frogs, 159 in females, 230 paternal behavior and, 190, 192193 reproductive synchronization and, 158 seasonality in levels of, 133 sexual differentiation, role in, 125127, 126f, 127f surge after winning, 231 as transcription factor, 53 Tetrodotoxin, 76 77, 77f Thamnophis sirtalis (aquatic garter snake), 7677, 77f Threat displays in dominant subordinate relationships, 223 territoriality and, 217 218 Thryothorus ludovicianus (Carolina wren), dear enemy effect in, 221 Thuman, Katharine A., 188 Thyroxine influence on migration, 103, 104 role in olfactory imprinting, 106107 Tinbergen, Niko four questions of, 1 3, 2f one question of, 4 Toads (Bufo) predator avoidance behavior, 66 tadpole siblings in schools, 199 visual prey capture, 66 69, 67f, 68f Tolerance, neural basis of, 201 204 Torus semicircularis, 147, 149 Touch sensors, in bat wings, 13 14 Tramontin, Anthony D., 50 Transcription factors, 53, 55 Trematode (Dicrocoelim dendriticum), 78 79, 78f Trigeminal temperature nerve endings, 71, 73 Tritonia, swimming in, 43 44, 43f, 48 49 Trophic hormones, 52 Trust, neural basis of, 201204 Trust game, 203204 ngara frogs Tu
call recognition in, 30, 31f, 32, 149, 151, 173 mating calls of, 30, 31f, 32, 137138, 207 208, 208f reproductive synchronization, 159 signal complexity, 174 species recognition, 30, 31f, 32 Turkeys, cooperation among sibling, 199 Turtles, loggerhead sea (Caretta caretta), navigation by, 115, 116f Tyto alba (barn owl), auditory hunting by, 69 71, 70f, 72f
U
Ultrasound. See Echolocation Umwelt, 37 38, 39, 41
V
Van Valen, Leigh, 21 V1a receptor, 184 185, 185f, 186f, 228229 Vasopressin aggression and, 227230, 230f cooperative behavior and, 201203 in monogamous prairie voles, 184185, 185f, 186f as neuromodulator, 48 parental behavior and, 193 Vertebrates motor control in, 41 pattern of sex steroid levels in, 129, 129f polarized light sensed by, 111 112 Vervet monkeys, referential signals in, 139 Verzijden, Machteld, 155 Vision in aphids, 8 10, 9f visual prey capture in toads, 66 69, 67f, 68f Voles monogamy and promiscuity in, 184185, 185f, 186f vasopressin effect on social attachment, 229 von Frisch, Karl, 1 von Uexku ll, Jakob, 37, 41
W
Waldman, Bruce, 204 Walum, Hasse, 185 Weapons, evolution of in animals, 163, 164f 165f Weevils, winged-wingless dimorphism in, 96 97, 97f Weiss, Samuel, 50 Whiptail lizards (Cnemidophoris uniparens), 124, 159 White-crowned sparrows long learning in, 152 response to song variation, 159 160
258
INDEX
Wilczynski, Walter, 173 Williams, George C., 26 Wiltschko, Roswitha, 116 Wiltschko, Wolfgang, 116 Wingedwingless dimorphism, in insects, 96 97, 97f Wingfield, John, 159 Wolffian duct system, 125, 126 Wolf spider (Schizocosa uetzi), 156 Wommack, Joel C., 226
Xiphophorus multilineatus, 176 Xiphophorus nigrensis, 176 179, 178f
Y
Yang, Eun-Jin, 232 Y chromosomes, 123, 125127 Young, Larry, 184
Z
Zahavi, Amotz, 169 Zebra finch (Taeniopygia guttata) aggregation preferences, 201202, 202f optimal foraging theory study in, 86, 86f response to song, 174 song learning in, 153f, 154 Zook, John, 13 Zugunruhe, 93, 98, 101, 103f, 108
X
X chromosomes, 123 Xenopus laevis, 204 Xiphophorus helleri, mate choice in, 6 7, 7f Xiphophorus maculatus, 6, 7f

Animal Behaviour

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Animal Behaviour

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Questions in Animal Behavior

TINBERGENS FOUR QUESTIONS

Males song repertoire size

TINBERGENS ONE QUESTION

Warbler finch Probing bill Cactus eater

Ground finch Crushing bill Seed eater

SYNERGISMS BETWEEN DIFFERENT LEVELS OF ANALYSIS Evolutionary History Informs Function

Mate Choice in Swordtails

Preference favoring sword Indifference Discrimination against sword

Mechanism Informs Function

Autumn Leaves and Aphid Vision

400 500 600 Wavelength (nm)

Acquisition Informs Evolutionary History

Cross-Generational Transmission of Stress by Maternal Behavior

Mother High licking/grooming

Increased serotonin tone and stimulation of 5-HT7 receptor

Demethylation of Nr3c1 exon 1, acetylation of histones around Nr3c1

Function Informs Mechanisms

Bats Listening in the Dark

Pigeons Flying in the Fog

Page references followed by f denote figures; those followed by t denote tables.

Mutation, 18, 18f, 19 Mutualisms, 23

Xiphophorus multilineatus, 176 Xiphophorus nigrensis, 176 179, 178f

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