Hormones and Animal Social Behavior. Elizabeth Adkins-Regan. Princeton University Press, Princeton, NJ, 2005. 411 pp., illus. $45.00 (ISBN 0691092478 paper).
Thirty years ago, while an undergraduate at Berkeley, I worked as a research assistant for Frank A. Beach, a founder of behavioral endocrinology. On a typical afternoon, I purchased an oxtail bone, cut it to a specified dimension, and drove to a field station to conduct behavioral tests on group-housed beagles. Within each five-dog pack, a social pecking order was established. I knew this because, after gaining the dogs' attention, I tossed the bone into the center of the pack and recorded which dog acquired it. This was designated the “alpha dog.” I then removed the alpha dog, retrieved the bone, and repeated the procedure to determine the beta dog, and so on. There was little or no fighting—an occasional growl or perhaps a tug-of-war among the lower-ranking dogs, but no overt aggressive behavior. This was true whether the packs comprised all males or all females. When two packs of dogs were tested together, a new hierarchy was sorted out very quickly, again with little overt conflict. The dogs seemed to understand one another's behavioral and sensory cues.
Particularly interesting was the behavior of female dogs that had been treated earlier in their lives with testosterone, the primary circulating sex steroid hormone in males. Some had been exposed to testosterone in utero when their mothers were injected with it, some were injected soon after birth, and some had been exposed through both routes. Such hormonal treatments had little effect on the males, as the treatments roughly duplicated male puppies' normal endocrine milieu. However, they had drastic effects on females. Indeed, the female puppies that received testosterone both pre- and postnatally looked very much like males, although their behavior was neither stereotypically male nor female. When tested a year or two later, however, those females not only were more aggressive, they didn't seem to understand the social rules. They would walk up to an alpha dog chewing on its newly attained oxtail bone and try to yank it away. They would contest the higher-ranked animals at every turn. Growls and outright fighting occurred with much higher frequency when these masculinized females were in the pen. What remains to be determined is whether this outcome reflects adjustments in the hormonally treated females' behavior or in the altered social cues emitted, or changes in their decision-making, perceptual abilities, or risk-taking behavior. This study cemented my interest in the effects of hormones on social behavior.
That hormones can have long-lasting effects on social interactions is well known. The mechanisms by which these interactions take place, and the ecological and evolutionary pressures that shape them, are the subject of numerous fascinating studies. However, this literature is spread throughout behavioral, physiological, ecological, and developmental journals, and a concise synthesis has been lacking. Hormones and Animal Social Behavior, written by Elizabeth Adkins-Regan, a professor of psychology and neurobiology at Cornell University, fills this void nicely. I assigned this book for a graduate seminar on hormones, brain, and behavior last term, and the students and I thoroughly enjoyed it.
The book is well written in an informal, entertaining style, and the new data, the novel synthesis, and the effortless glide across multiple levels of analysis make it remarkable for its depth and breadth. It is nearly a perfect behavioral biology book, suitable for graduate and advanced undergraduate students. When reading it, I kept hearing the ghost of Frank Beach's “The Snark Was a Boo-jum” paper as Adkins-Regan gently, but persistently, reminded me that knowing how things work in one species does not mean we understand how things work in other species. She conveys the complexity of comparative biology without overwhelming the reader.
The first chapter reviews basic endocrinology, with the presentation limited to those hormones and their receptors that are best documented as influential in social behavior. The chapter discusses why social behavior requires hormonal regulation, and describes the synthesis and metabolism of major steroid hormones. A description of the actions of neuropeptides and prolactin, and the mechanisms of their action, follows. There are concise and highly integrative sections on plasticity and development, as well as on environmental regulation of hormones.
Chapter 2, the longest, covers the behavioral topics most commonly associated with behavioral endocrinology: mating, fighting, parenting, and signaling. Adkins-Regan does a good job of summarizing decades of research, though she also presents a new synthesis of how hormones alter behavior via interactions with neural circuits, networks, and processes. I enjoyed the presentation of daily and seasonal influences of hormones, but I would have appreciated here an explicit statement about the reason underlying daily or seasonal reductions in testosterone: Males cannot continuously manage the costs of high testosterone (a point the author makes later in the book). In contrast, she does a magnificent job on the role of testosterone signaling, and breaks down the costs of testosterone on far-ranging physiological and behavioral parameters into digestible and testable hypotheses.
In chapter 3, which describes social relationships and organization, Adkins-Regan begins to add function to mechanism. She also brings ecological factors to bear in addressing cause-and-effect relationships.
In chapter 4, a description of the development of sex differences and within-sex morphs, Adkins-Regan reviews the organizational (programming) and activational effects of sex steroid hormones. In chapter 5, she reviews the evidence for endocrine contributions to individual differences in social behavior. These wide-ranging chapters use Tinbergen's four formal questions underlying the study of behavior to present sex and individual differences and the hypothetical reasons for these. Adkins-Regan examines the genetic, molecular, endocrine, and neural mechanisms underlying such differences, as well as their development, phylogeny, and adaptive significance. She encourages more mechanistic studies while emphasizing the desirability of a stronger link between behavioral endocrinology and evolutionary biology.
In chapter 6, life stages and life histories are considered. The author presents the typical species-level and individual-level trade-offs between somatic functions and reproduction that shape the evolution of life histories (for example, survival mechanisms versus growth). She then brilliantly describes the importance of hormones in life stages such as hatching and birth, metamorphosis, puberty, peripubertal dispersal, and the onset of reproductive senescence. The author focuses on trade-offs between mating and parental efforts; I wish there had been more emphasis on the core life history trade-offs, such as that between reproductive effort and immune function, a proxy for survival mechanism. The influences of sex steroid hormones, as well as glucocorticoids, on immune function have profound effects on survival and reproduction, and the trade-offs can vary as a function of time of year.
In the final chapter, Adkins-Regan examines phylogeny in the context of evolutionary conservation and innovation. She notes that whereas genomes, steroid mechanisms, and brain structures are generally conserved across phylogeny, social relationships and organization are quite diverse. Why? The author suggests several possibilities. Hormones allow for diverse social behaviors by allowing the action of a variety of conserved and innovative mechanisms (e.g., changes in the distribution of receptors in various brain regions). She also emphasizes that some developmental mechanisms can be repeated across phylogeny to produce specific behaviors (e.g., vocalization linked to both innate and acquired social cues).
Behavioral endocrinology has matured since I watched beagles form social hierarchies nearly 30 years ago. The field has changed from merely measuring and manipulating circulating hormone concentrations to examining gene transcription, hormone receptors, and other molecular and cellular parameters, as well as the neural circuitry and social environment associated with various behaviors. Researchers would benefit by heeding the overarching message in Adkins-Regan's book: It is always critical to consider the pressures that shape behavioral mechanisms.
Hormones and Animal Social Behavior masterfully achieves Adkins-Regan's goal of integrating behavioral endocrinology with ecological and evolutionary studies. One could quibble with the relative shortage of figures, the lack of detailed referencing of statements in the text, or possibly a slight overemphasis on birds (I would have liked to have seen more mammalian examples, because behavioral endocrinology will be important in future attempts to conserve species as critical conditions change). Nonetheless, I predict that this outstanding book will soon become a classic in behavioral biology.