Animal Personalities: Behavior, Physiology, and Evolution

Overview


Ask anyone who has owned a pet and they’ll assure you that, yes, animals have personalities. And science is beginning to agree. Researchers have demonstrated that both domesticated and nondomesticated animals—from invertebrates to monkeys and apes—behave in consistently different ways, meeting the criteria for what many define as personality. But why the differences, and how are personalities shaped by genes and environment? How did they evolve? The essays in Animal Personalities reveal that there is much to ...
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Animal Personalities: Behavior, Physiology, and Evolution

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Overview


Ask anyone who has owned a pet and they’ll assure you that, yes, animals have personalities. And science is beginning to agree. Researchers have demonstrated that both domesticated and nondomesticated animals—from invertebrates to monkeys and apes—behave in consistently different ways, meeting the criteria for what many define as personality. But why the differences, and how are personalities shaped by genes and environment? How did they evolve? The essays in Animal Personalities reveal that there is much to learn from our furred and feathered friends.
           
The study of animal personality is one of the fastest-growing areas of research in behavioral and evolutionary biology. Here Claudio Carere and Dario Maestripieri, along with a host of scholars from fields as diverse as ecology, genetics, endocrinology, neuroscience, and psychology, provide a comprehensive overview of the current research on animal personality. Grouped into thematic sections, chapters approach the topic with empirical and theoretical material and show that to fully understand why personality exists, we must consider the evolutionary processes that give rise to personality, the ecological correlates of personality differences, and the physiological mechanisms underlying personality variation.
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Editorial Reviews

Jeanne Altmann

“The editors provide a cornucopia full of studies on animal personalities, diverse in biological approaches and levels of investigation as well as in species. Gone are the days, not so long ago, when the intrepid few planted the seeds of research on personalities in animals other than humans and did so despite suspicion of the enterprise.”
Annali dell'Istituto Superiore di Sanit� - Enrico Alleva

“In this timely volume, the first one synthesizing and integrating the research on animal personality, Claudio Carere and Dario Maestripieri, two recognized scholars of behavioral biology, provide a collection of essays diverse in biological approaches and levels of investigation as well as in species—from invertebrates to monkeys and apes, including humans. . . . There is currently no other compilation of papers providing such a broad and updated overview about a subject at the forefront of science. Various research perspectives and approaches . . . have been brought together striving to develop new avenues of research. They include applied areas with an overall holistic approach to the subject, which makes the volume particularly valuable for a wide audience, ranging from undergraduate students uncertain of their future choices, biologists of virtually all disciplines, medical researchers, veterinarians, and psychologists.”
Animal Welfare - Ori Pomerantz

“Fascinating. . . . [and] valuable in promoting our understanding of the specific needs and motivation of different individuals, and consequently to improving their management.”
Choice - B. E. Fleury

“This synthesis of a blossoming area of research is valuable for all academic libraries. Highly recommended.”
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Product Details

  • ISBN-13: 9780226922058
  • Publisher: University of Chicago Press
  • Publication date: 3/8/2013
  • Pages: 520
  • Product dimensions: 9.10 (w) x 6.30 (h) x 1.30 (d)

Meet the Author


Claudio Carere is adjunct professor of animal behavior and animal physiology in the Department of Ecological and Biological Sciences, Tuscia University, Italy. Dario Maestripieri is professor of comparative human development, evolutionary biology, and neurobiology at the University of Chicago.
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Read an Excerpt

ANIMAL PERSONALITIES

Behavior, Physiology, and Evolution

THE UNIVERSITY OF CHICAGO PRESS

Copyright © 2013 The University of Chicago
All right reserved.

ISBN: 978-0-226-92197-6


Chapter One

The Bold and the Spineless

Invertebrate Personalities

JENNIFER A. MATHER AND DAVID M. LOGUE

Introduction

Reviewing the study of personalities of invertebrates offers a series of challenges. First, there is a huge number of invertebrate species, sometimes estimated to represent 98% of the animal species on the planet (Pechenik 2000). Second, invertebrates exhibit a tremendous array of life history strategies, developmental trajectories, modes of reproduction, and physiological bases of behavior, many of which are poorly known. A further challenge arises from the diversity of perspectives and research backgrounds that characterizes invertebrate personality researchers.

One of the goals of this review is to determine the degree to which invertebrates, often viewed as animals of limited behavioral repertoires, exhibit personality as defined in the introduction and throughout this volume. We begin with a survey of reports that relate to personality in invertebrates. We categorize these as (1) descriptive reports, (2) physiological/genetic linkages (see Van Oers et al. 2005), (3) ontogenetic studies (sensu West-Eberhard 2003), and (4) ecological/selection studies (Groothuis and Carere 2005; Smith and Blumstein 2008). There will be some bias toward studies of poorly known taxa, even if their evidence is fragmentary. We then evaluate several particularly thorough and influential research programs in depth. In the final section, we provide recommendations for future research directions and attempt to summarize the current state of the field.

This review does not evaluate the division of labor (polyethism) in colonies of social insects, or the discrete morphologies (polyphenism) found in many invertebrates. Although we recognize that both of these phenomena may relate to personality (e.g., Bergmüller and Taborsky 2010; Bergmüller et al. 2010), we have chosen to focus on subtler forms of personality (i.e., those that form continuous rather than discrete distributions). We refer readers interested in polyethism and polyphenism to reviews by Beshers and Fewell (2001) and Emlen and Nijhout (2000), respectively.

General survey

A literature search of the papers that assess individual differences and/or correlated behavior in invertebrates revealed thirty-two papers. These range widely across taxa, one is on Caenorhabdita worms and one on snails and a small collection on cephalopod mollusks. Arthropods are well represented, with two on crustaceans, eight on spiders, and fourteen on insects, three on individuals in the larval stage, and one spanning developmental stages. The scope of these studies varies extremely widely, and only those on the fruit flies, grass spiders, fishing spider, field crickets, and cephalopods fall into a group of papers that merits further discussion. In Table 1.1 each paper is described as within one of four general categories: descriptive, ecological/ selection, physiological/genetic, and ontogenetic. Next, a brief comment is made about the study design, then major results of the study are summarized, and last, comments are made that allow the reader to understand the study better.

The genetic control of behavior in the fruit fly, Drosophila

Research on the behavior of Drosophila fruit flies has made a considerable contribution to our knowledge of individual differences in behavior, even though the researchers conducting this work did not frame their research in terms of personality. Rather, their work attempted to describe genetic influences on physiology and behavior. Sokolowski's (2001) review of the behavioral genetics of Drosophila is particularly informative to researchers interested in the genetic underpinnings of personality.

Sokolowski (2001) makes it clear that even in flies there are no genes "for" behavior. Rather, genes and the environment interact to determine anatomy and physiology, which, in turn, influence behavior. Variation in individual genes can influence more than one aspect of an animal's phenotype—a phenomenon known as pleiotropy (Cheverud 1996). Variation at pleiotropic loci can result in consistent individual differences across multiple contexts—in other words, personalities (Sih et al. 2004). Much of the investigation of the behavior of Drosophila has focused on linking genetic differences to differences in behavior. Researchers identify a variable locus in the fly genome that covaries with behavior and investigate the physiological pathway that links the genetic variation to differences in behavior. Of the many examples of research along these lines, the following two are particularly good demonstrations of the relationship between genetics and "personality" in fruit flies.

In fruit fly larvae, scientists have found a gene, for, which influences foraging behavior. The R variant of the gene is the dominant allele and the s variant is the recessive one. In the presence of food, rover (Rs or RR) larvae tend to leave a food patch, but sitter larvae (ss) tend to remain (Sokolowski 2001). Natural selection favors rovers in crowded situations and sitters in less crowded ones. In other words, selection for a behavioral strategy is density dependent. Environmental variation can also affect behavior, as food deprivation turns rovers into sitters and other environmental factors can transform sitters into rovers. To define the personality of an individual, its behavior should be consistent through all contexts; so, rovers should be always rovers. This example shows a relevant plasticity of behavioral response, which does not match with personality. The difference between the two behavioral types is mediated by a small difference in cGMP-dependent protein kinase activity—on average, rovers have 12% more activity than sitters. Rovers have better short-term but poorer long-term memory than sitters (Mery et al. 2007). The rover-sitter example elegantly demonstrates how one gene can influence individual differences in an important behavior pattern linked to activity.

Several mutations cause male fruit flies to terminate courtship prematurely. One of the most interesting of these is the dunce mutation, which alters learning (Sokolowski 2001). Normal males that have encountered a mated female suppress courtship for three hours. The mechanism of this courtship suppression is olfactory-based avoidance learning. Dunce males, however, do not exhibit olfactory-based avoidance associative learning and so do not suppress courtship. Learning suppression by this mutation (likely due to alteration in the mushroom bodies of the brain) could have pleiotropic effects. If, as seems likely, these effects influence behavior in more than one context and persist over time, pleiotropy would be causally linked to personality.

Studies of the for and dunce loci illustrate how relatively minor genetic variation can cause persistent, context-general differences in behavior, which might be measured as personality. Findings from such studies, however, should not be taken as evidence that genetic variation, rather than environmental variation or gene-by-environment interaction, is the primary determinant of personality in fruit flies. Higgins et al. (2005) studied "activity" in groups of flies derived from nine isogenic (i.e., genetically identical except for sex) lines. They found that less than 15% of variation in summed activity was due to lineage. A group-within-lineage effect accounted for over 20% of the variation in activity, suggesting an important contribution of social environment to activity. The interaction between genes and the environment explained another 11% of the variation in activity, meaning that various lineages responded differently to different environments. Interestingly, there were significant differences in the specific behaviors that contributed to activity (feeding, grooming, resting, and walking) among different lines, so a summed activity measure may not do justice to the complexity of the problem.

Foraging-predation tradeoffs in the Western grass spider, Agelenopsis aperta

The field of behavioral ecology is defined by its hypothesis-driven, evolutionary approach to behavior. Whereas personality psychologists emphasize holism, behavioral ecologists often focus on specific behavioral traits and develop models that predict an individual's optimal behavior in a given set of circumstances. For example, a well-known optimal foraging model describes optimal prey choice (i.e., the prey type that will maximize a predator's energy intake) given the profitability, search time, and handling time of each potential prey type (Stephens and Krebs 1986). Behavioral ecologists' interest in optimal behavior stems from the fact that natural selection shapes behavior in ways that tend to maximize an individual's fitness over evolutionary time.

Using optimal foraging theory as an example, suppose that foraging preference (for prey A versus prey B) differs among individuals and covaries with boldness in the presence of predators, such that bolder individuals tend to prefer prey A. Optimal foraging theory does not consider individual differences because it assumes that all individuals behave optimally; if A is the optimal prey, all individuals should choose A until it is depleted to the point that B becomes the optimal choice. Further, optimal foraging theory treats foraging as a context-specific behavior, whose fitness consequences are independent of behavior in other contexts. If prey choice is linked (e.g., by pleiotropy, by genetic linkage) to boldness, the fitness consequences of boldness will affect the evolution of prey choice, and vice versa.

The behavioral syndromes paradigm incorporates individual differences and between-context correlations in behavior into an evolutionary framework (Sih et al. 2004; Bell 2007). A series of studies on the Western grass spider, Agelenopsis aperta, is an early example of the behavioral syndromes approach. The Western grass spider is a funnel web spider that occurs in both dry grassland and moist riparian habitats. Grassland dwellers experience lower prey availability, higher competition for webs, and lower predation from birds (Riechert and Hedrick 1990). The authors asked how the very different selection regimes in these two habitats affected spiders' behavior.

Riechert and Hedrick's (1990, 1993) work contributes to the personality literature because it measures multiple behavioral traits and quantifies the relationships between them. The traits that they examined—boldness, latency to forage, success in agonistic contests—might be said to constitute the "shy-bold" axis of personality widely studied in vertebrates (Gosling 2001). The authors, however, call these behaviors manifestations of "aggression" and "fear," which they view as separate but correlated axes (Smith and Riechert 1984). Regardless of the terminology or the underlying mechanisms, these traits are evolutionarily important because they affect predator avoidance, foraging, and other factors that determine fitness.

Riechert and Hedrick (1990) reasoned that natural selection should favor more fearful spiders in riparian habitats, and more aggressive spiders in grasslands. Because riparian spiders experience high predation risk and high food availability, spending a lot of time hiding (an expression of fearfulness) should provide high benefits in the form of reduced risk of predation at a relatively low cost—if they miss a meal because they are hiding, another meal will probably be available soon. In contrast, grassland spiders are under low predation risk, but they must maintain large territories and be vigilant for potential food because prey is scarce. Grassland spiders would benefit from low fearfulness and high aggressiveness if these traits help them to defend large territories and capture more prey. Because predation is relatively uncommon in the grassland population, the costs of being exposed on the web should be lower than in the riparian population. The investigators measured fearfulness by simulating an approaching avian predator and recording whether the resident spider retreated into its funnel and, if so, how long it took to re-emerge. Their predator stimulus was simple but appropriate to their subject's umwelt; experimenters blew puffs of air onto the web sheet with a rubber bulb designed to clean camera lenses. As predicted, free-living spiders from the riparian habitat exhibited significantly longer latencies to re-emerge from the funnel than their grassland counterparts (Riechert and Hedrick 1990). The same pattern was found among second-generation laboratory-raised spiders, showing that genetic factors are responsible for at least part of the difference in latency to emerge between the two populations.

Emergence time was not the only trait that differed between the populations. The researchers deposited standardized prey items into spiders' webs and measured their latency to attack. They found that riparian spiders took longer than grassland spiders to attack prey that had been deposited in their webs (14.1 vs. 6.6 sec, on average; Hedrick and Riechert 1989). The hypothesis that latency to attack and latency to recover from disturbance are constrained to evolve together can be used to generate the prediction that the two traits will covary within a given population. Indeed, recovery from disturbance and latency to attack prey were related among individuals in the riparian population, suggesting such a constraint. Further, when spiders exhibiting short latencies to recover from disturbance were pitted against spiders with long latencies in agonistic contests, the short-latency spiders tended to win (Riechert and Hedrick 1993). Thus, behaviors associated with fighting, recovery from disturbance, and predation all covary in A. aperta. Genetic causes of behavioral syndromes include pleiotropy (i.e., multiple effects attributable to a given genetic variant) or linkage disequilibrium (i.e., when two or more genes tend to be inherited together; Riechert and Hedrick 1990; Sih et al. 2004).

The researchers then asked whether the behavioral differences between the two populations resulted from adaptation to the local environments. Reciprocal transplant experiments revealed that local spiders fared better than transplants, supporting the hypothesis that spiders are adapted to their local environment (Riechert and Hall 2000). A natural experiment on local adaptation occurred at an Arizona site where a riparian zone intersects an arid habitat and migration between habitats resulted in substantial gene flow between the two populations (Riechert 1993). Although selection presumably continued to favor the individuals best suited to each environment, immigrants from the other environment continuously added maladaptive genes to the population. When she eliminated gene flow with experimental enclosures, Riechert (1993) found that the populations rapidly evolved to become more adapted to their environments.

As with most of the behavioral syndromes research that followed it, the Western grass spider project emphasized environmental influences on the evolution of correlated patterns of behavior. This approach offers insights into the fundamental significance of personality in animals: Why do personalities exist? Why is group A different from group B? How does the existence of personality affect the evolution of animal populations? One criticism of the behavioral syndromes approach is that it tends to focus on a small set of specified traits. For example, the Western grass spider project measured a small number of behaviors, and identified only one or two axes of covariation. Measuring more behaviors in more contexts would have allowed the researchers to more fully define these axes and perhaps to discover additional axes relevant to natural selection (see Pruitt et al. 2008; Logue et al. 2009). Such criticisms notwithstanding, the Western grass spider studies represent an important early step toward understanding the evolutionary basis of individual differences in behavior.

(Continues...)



Excerpted from ANIMAL PERSONALITIES Copyright © 2013 by The University of Chicago. Excerpted by permission of THE UNIVERSITY OF CHICAGO PRESS. All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.

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Table of Contents


Contributors
Introduction: Animal Personalities: Who Cares and Why?
Claudio Carere, Dario Maestripieri

Part I: Behavioral Characterization of Personalities across Animal Taxa

Chapter 1. The Bold and the Spineless: Invertebrate Personalities
Jennifer A. Mather, David M. Logue
Chapter 2. Evolutionary Perspectives on Personality in Stickleback Fish
Alison M. Bell, Susan A. Foster, Matthew Wund
Chapter 3. Avian Personality
Kees van Oers, Marc Naguib
Chapter 4. Differential Behavioral Ecology: The Structure, Life History, and Evolution of Primate Personality
Alexander Weiss, Mark J. Adams
Chapter 5. Personalities in a Comparative Perspective: What Do Human Psychologists Glean from Animal Personality Studies?
Samuel D. Gosling, Pranjal H. Mehta

Part II. Genetics, Ecology, and Evolution of Animal Personalities

Chapter 6. The Quantitative and Molecular Genetics of Animal Personality
Kees van Oers, David. L. Sinn
Chapter 7. What Is the Evidence that Natural Selection Maintains Variation in Animal Personalities?
Niels J. Dingemanse, Denis Réale
Chapter 8. Frontiers on the Interface between Behavioral Syndromes and Social Behavioral Ecology
Andrew Sih
Chapter 9. The Evolution of Animal Personalities
Max Wolf, G. Sander van Doorn, Olof Leimar, Franz J. Weissing

Part III. Development of Personalities and Their Underlying Mechanisms

Chapter 10. Ontogeny of Stable Individual Differences: Gene, Environment, and Epigenetic Mechanisms
James P. Curley, Igor Branchi
Chapter 11. Parental Influences on Offspring Personality Traits in Oviparous and Placental Vertebrates
Dario Maestripieri, Ton G. G. Groothuis
Chapter 12. Neuroendocrine and Autonomic Correlates of Animal Personalities
Doretta Caramaschi, Claudio Carere, Andrea Sgoifo, Jaap M. Koolhaas

Part IV. Implications of Personality Research for Conservation Biology, Animal Welfare, and Human Health

Chapter 13. Animal Personality and Conservation Biology: The Importance of Behavioral Diversity
Brian R. Smith, Daniel T. Blumstein
Chapter 14. Personality Variation in Cultured Fish: Implications for Production and Welfare
Felicity Huntingford, Flavia Mesquita, Sunil Kadri
Chapter 15. Behavioral, Physiological, and Health Biases in Laboratory Rodents: A Basis for Understanding Mechanistic Links between Human Personality and Health
Sonia A. Cavigelli, Kerry C. Michael, Christina M. Ragan

Acknowledgments
Index

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