Rodent Societies: An Ecological and Evolutionary Perspective

by Jerry O. Wolff (Editor), Paul W. Sherman (Editor)

Overview

Rodent Societies synthesizes and integrates the current state of knowledge about the social behavior of rodents, providing ecological and evolutionary contexts for understanding their societies and highlighting emerging conservation and management strategies to preserve them. It begins with a summary of the evolution, phylogeny, and biogeography of social and nonsocial rodents, providing a historical basis for comparative analyses. Subsequent sections focus on group-living rodents and characterize their reproductive behaviors, life histories and population ecology, genetics, neuroendocrine mechanisms, behavioral development, cognitive processes, communication mechanisms, cooperative and uncooperative behaviors, antipredator strategies, comparative socioecology, diseases, and conservation. Using the highly diverse and well-studied Rodentia as model systems to integrate a variety of research approaches and evolutionary theory into a unifying framework, Rodent Societies will appeal to a wide range of disciplines, both as a compendium of current research and as a stimulus for future collaborative and interdisciplinary investigations.

Product Details

ISBN-13:	9780226905372
Publisher:	University of Chicago Press
Publication date:	05/15/2007
Pages:	610
Product dimensions:	8.50(w) x 11.00(h) x 1.30(d)

About the Author

Jerry O. Wolff is professor of biology at St. Cloud State University.

Paul W. Sherman is professor of neurology and behavior at Cornell University.

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Rodent Societies An Ecological & Evolutionary Perspective
The University of Chicago Press Copyright © 2007 The University of Chicago
All right reserved.
ISBN: 978-0-226-90536-5



Chapter One Rodent Societies as Model Systems

Jerry O. Wolff and Paul W. Sherman

The Rodentia is the largest order of mammals, consisting of more than 2,000 species and comprising 44% of all mammals. Rodents come in a variety of body shapes, from cylindrical to spherical, and sizes, from less than 10 g to more than 66 kg. The characteristic that unites this order-and is its most conspicuous trait-is a single pair of razor-sharp incisors, which are used to gnaw food, excavate tunnels, and defend themselves. The name "rodent" derives from the Latin word rodere, which means "to gnaw."

No matter where you live, a rodent is probably not far away. Rodents inhabit all continents except Antarctica, and they occur in terrestrial, subterranean, arboreal, and aquatic habitats-from the high arctic tundra to equatorial rain forests, temperate bogs and swamps to hot, arid deserts, and rocky mountaintops to sandy canyon bottoms. Many species live in close association with humans. With such varied characteristics and expansive ecology, rodents provide a range of attributes that have captivated scientists and annoyed laypersons for hundreds of years.

The diversity of rodents, and the ease with which many species can be maintained in captivity, has led to their choice as model systems for observational and experimental studies in genetics, ecology, demography, physiology, and psychology. The social and reproductive behaviors of rodents also are diverse and intriguing. Although most rodents are nocturnal, a surprising amount of research has been conducted on rodent social biology. As a result, large databases are available, and these can be used to test hypotheses about the ecological and evolutionary forces that mold mammalian social and reproductive behaviors. Many aspects of behavioral ecology are similar across species (e.g., the effects of resource distributions on mating systems [Slobodchikoff 1984; Ostfeld 1990]; the role of ecological factors in favoring group-living [Hoogland 1995; Ebensperger and Cofré 2001]; and the role of kinship in structuring social interactions [Sherman 1981a; Lacey and Wieczorek 2003]). Unifying theories developed from other taxa, such as primates, ungulates, or canids, can be experimentally tested in the field and laboratory with rodents. These options are not so readily available for the larger, wider-ranging taxa. Thus rodents are not only models for testing hypotheses developed from rodents, but they have become models for other taxa as well. The relevant information, however, is widely scattered and sometimes conflicting. Hence this volume.

Our goals were to synthesize and integrate the current state of knowledge about the social behavior of rodents, to provide ecological and evolutionary contexts for understanding rodent societies, and to highlight emerging conservation and management issues to preserve these societies. Thus we attempted to emulate Primate Societies (1987) and Cetacean Societies (2000), the two outstanding preceding volumes in this series published by the University of Chicago Press.

In selecting topics and contributors for the present volume, we first chose areas of behavioral biology and model species that we considered essential for understanding the adaptive significance of rodent social behavior generally. Then we invited contributions from researchers who have demonstrated their preeminence in illuminating these areas and in studying the focal taxa. We urged authors to use the comparative approach, and to discuss not only the behavior of their subjects but also that of ecologically similar and phylogenetically related species. We instructed authors to differentiate proximate (mechanistic) from ultimate (evolutionary) causes of behavioral phenomena, and to emphasize the usefulness of integrating results at different levels of analysis. Finally, we encouraged authors to highlight the roles of experimentation and hypothesis testing in advancing our understanding and in developing the next generation of predictive models.

All chapters were peer reviewed, sometimes by authors of related chapters, in an attempt to enhance integration. The resulting volume attests not only to the authors' expertise, good humor, and willingness to revise and reconsider their work in light of constructive criticisms and new information, but also why these contributors have made studying rodent societies their life's work. We hope that after diving between the covers of this volume, you too will be struck by rodentophilia!

We begin this anthology with a summary of the evolution, phylogeny, and biogeography of rodents, to provide an historical context and a basis for comparative analyses. We divided the subsequent 39 chapters into seven major areas that characterize rodent societies. These include sexual behavior (chaps. 3-7), life history (chaps. 8-15), behavioral development (chaps. 16-19), social behavior (chaps. 20-25), antipredator behavior (chaps. 26 -28), comparative socioecology (chaps. 29-37), and conservation and disease (chaps. 38-41). Although each section focuses on a particular aspect of rodent social biology, several central themes reemerged throughout each chapter and the entire volume, enabling us to identify some universal components of rodent societies.

Universal Components of Rodent Societies

A basic understanding of behavior quickly reveals patterns that recur in various taxa. And in that rodents have been studied extensively in many areas of behavior, ecology, and evolution, authors have been able to synthesize theory with empirical studies to develop conceptual models to explain many aspects of rodent societies. It is these predictable patterns that we attempt to emphasize in this anthology.

Regarding reproductive strategies, we deviated from the conventional approach of chapters on monogamy, polygyny, and promiscuity, in favor of examining sex-specific mating strategies. Thus there are chapters on male mating strategies (Waterman, chap. 3) and female mating strategies (Solomon and Keane, chap. 4), and these focus on individual reproductive behaviors rather than the species- or population-level mating system. Our authors demonstrate how sex-specific mating and reproductive tactics maximize fitness; similar tactics also occur among males and females of other mammalian taxa. Carroll and Potts (chap. 5) use house mice as models to demonstrate the importance of female choice in selecting for genetically compatible mating partners. The ideas, mechanisms, and results are applicable to sexual selection theory in that they provide evidence for the "compatible genes" hypothesis for mate choice. In a phylogenetic analysis of breeding systems in Neotomine and Peromyscine rodents, Kalcounis-Rüppell and Ribble (chap. 6) examine a series of behavioral and ecological parameters to develop a model that predicts mating systems. Koprowski (chap. 7) also uses a comparative approach in describing alternative sexual behaviors in male tree squirrels, which reveals how male tactics are dependent in part on female tactics. All these authors remind readers of the evolutionary arms race between the sexes, and their chapters demonstrate how the behavioral strategy of one sex often is dependent on the behavior of the other sex. Mating systems are thus a consequence of alternative mating tactics used by males and females.

All animals must communicate with each other at some time, especially during intrasexual conflict and for mating and defensive purposes. Important aspects of communication that have been well studied in rodents include chemical factors in urine that accelerate and suppress reproduction (Drickamer, chap. 9), express dominance and territoriality (Roberts, chap. 22), and serve as cues of genetic compatibility in mate choice (Carroll and Potts, chap. 5). Vocal communication, especially alarm calling, has also been well studied in rodents (Blumstein, chap. 27, and Hoogland, chap. 37), as has nepotism (assisting kin) more generally (e.g., Holmes and Mateo, chap. 19).

A major theme that unites this volume is the importance of genetic relatedness in modulating the social behavior of rodents, as showcased, for example, in the chapters on general topics such as social learning (Galef, chap. 18), kin recognition (Holmes and Mateo, chap. 19), parental care (McGuire and Bemis, chap. 20), alarm calling (Blumstein, chap. 27, and Hoogland, chap. 37) as well as in chapters focused on specific taxa, including beavers (Busher, chap. 24), mole-rats (Nevo, chap. 25; Faulkes and Bennett, chap. 36), ground squirrels (Hare and Murie, chap. 29), and marmots (Armitage, chap. 30). Social groups of kin most often result from philopatry of daughters (Solomon and Keane, chap. 4), which in turn creates advantages for males that disperse to seek unrelated females for mating and to avoid inbreeding or reproduction competition in the natal site (Nunes, chap. 13). Coloniality, sociality, and especially eusociality depend on kinship (Lacey and Sherman, chap. 21) and occur in blind mole-rats (Nevo, chap. 25), North American ground squirrels (Hare and Murie, chap. 29), desert rodents (Randall, chap. 31), some groups of South American rodents (Lacey and Ebensperger, chap. 34), and African mole-rats (Faulkes and Bennett, chap. 36).

Experimentation and Hypothesis Testing

Science does not advance by gathering data that support hypotheses, but by conducting "strong inference" tests (Platt 1964) of the alternatives. Such tests involve developing competing, critical predictions from each hypothesis, and then conducting experiments or observations that attempt to falsify these predictions. The hypothesis that is left standing at the end of this process becomes the front-runner as the most likely explanation for the phenomenon at issue.

To meet our primary goals, we asked authors to emphasize their experimental and strong inferential approaches whenever possible. For example, the role of hormones and neural control of behavior (Curtis and colleagues, chap. 16) have been elucidated experimentally. The expression of hormones such as vasopressin and oxytocin are positively correlated with monogamy, which in turn affects mating behavior, paternal care, and juvenile development. Rigorous testing of alternative hypotheses is used by Carroll and Potts (chap. 5) to examine the genetic consequences of mate choice and sexual selection in house mice via the major histocompatibility complex (MHC), by Drickamer (chap. 9) to determine the role of chemical signals in accelerating or suppressing reproduction, and by Sikes (chap. 11) to demonstrate howfield and laboratory experimentationwas used to test hypotheses for facultative sex ratio adjustment. Sikes concludes that the theory for adaptive sex ratio adjustment in rodents has thus far exceeded the data, and that no mechanism for varying the sex ratio adaptively has been discovered. Experimentation is also used to determine what factors contribute to stress and how stress affects fitness and demography (Boonstra et al., chap. 12) and how rodents learn what foods to eat and avoid (Galef, chap. 18). McGuire and Bemis (chap. 20) use cross-fostering experiments to discern the role of paternal care in polygynous and monogamous species of voles. An experimental approach also is used to address mechanisms of reproductive suppression and self regulation (Krebs et al. chap. 15), scent marking (Roberts, chap. 22), antipredator processes (Owings and Coss, chap. 26; Ylönen and Brown, chap. 28), the genetic basis for aggression in mole-rats (Nevo, chap. 25), alarm calls (Blumstein, chap. 27; Hoogland, chap. 37), and behavior conducive to commensal living in rats and mice (Berdoy and Drickamer, chap. 32).

Proximate Mechanisms and Ultimate Causation

Why do animals do what they do? There are multiple, complementary answers to such a question, which lie at different levels of analysis (Tinbergen 1963; Sherman 1988). One type of answer addresses the mechanistic (hormonal, neuronal) causes of a behavioral phenomenon, while another addresses the ontogeny of the behavior in each individual's lifetime, still a third examines the effects of the behavior on the individual's fitness, and the fourth type of answer addresses the evolutionary history of the behavior. The first two levels are known as proximate and the latter two as ultimate explanations. Complete understanding of any behavioral phenomenon requires answers at all four levels and their integration.

Synthesis of mechanism and function is well illustrated in chapters 3 (Waterman) and 4 (Solomon and Keane), which describe how the behavior of one sex becomes a stimulus for the opposite sex to utilize a particular reproductive tactic, such as wandering versus mate guarding, or territoriality versus searching. Alternative reproductive tactics are typically functions of both social and ecological variables, as is also illustrated in chapters 6 (neotomine and peromyscine rodents, Kalcounis-Rüppell and Ribble), 7 (tree squirrels, Koprowski), 30 (marmots, Armitage), and 34 (South American hystrigonath rodents, Lacey and Ebensberger). In chapter 8, Dobson and Oli explain how reproductive effort is tied to altricial and precocial development of offspring. The presence of an opposite-sex parent is the stimulus for sex-biased natal dispersal in mice, which ultimately prevents inbreeding and intrasexual competition with male relatives (Nunes, chap. 13). Male affiliative behavior leading to monogamy can be explained proximately by neuronal and hormonal mechanisms and ultimately by the value of paternal care in contributing to survival of young (Curtis et al. chap. 16). Although density of voles and mice, or more likely number of adult females, seems to be a proximate mechanism to suppress reproduction in young females, the ultimate benefit apparently is to conserve reproductive effort by aborting embryos that would likely be killed by infanticide at birth (Krebs et al. chap. 15). Conversely, Ebensperger and Blumstein (chap. 23) discuss how the act of ejaculation inhibits infanticide by males, which in turn might be a selective factor for multi-male mating by females in some species, to confuse paternity and deter infanticide. Finally, Mateo (chap. 17) uses experimental and observational data from ground squirrels to demonstrate how learning, maturation, and ecological selective pressures intertwine to shape the ontogeny of adaptive behavior. Although we gave each author guidelines and a general subject area to cover, we found that many authors were able to go beyond a summation of data for a particular topic and synthesize two or more disciplines to create new theory with new predictions.

A Synthesis of Disciplines and New Paradigms

Many chapters included in Rodent Societies cover topics that occur in most behavior texts (e.g., Alcock 2005; Dugatkin 2003). However, we encouraged authors to go beyond summarizing current knowledge to develop new paradigms by combining ideas from various disciplines. For example, Kalcounis-Rüppell and Ribble (chap. 6) provide a phylogenetic analysis of life history and physiological correlates of male and female mating strategies in which they conclude that litter mass and distributional range of a species are good predictors of the occurrence of paternal care. Dobson and Oli (chap. 8) present a model of reproductive effort involving "fast and slow" life histories that is ultimately based on demography. The authors attempted to understand if developmental stage at birth might become a constraint on the ontogeny of reproductive effort and other life history variables. Albrecht Schulte-Hostedde (chap. 10) applies sexual selection and parental investment theory to investigate how ecological and energetic constraints might limit sexual dimorphism, independent of the mating system. Schulte-Hostedde presents two alternative hypotheses to illustrate how the energetics of reproduction, sexual selection, and costs of extreme climatic conditions interact to limit sexual dimorphism in chipmunks.

(Continues...)

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Table of Contents

Introduction


1     Rodents Societies as Model Systems
      Jerry O. Wolff and Paul W. Sherman
2     Rodent Evolution, Phylogenetics, and Biogeography
      Rodney L. Honeycutt, Laurence J. Frabotta, and Diane L. Rowe

Sexual Behavior


3     Male Mating Strategies in Rodents
      Jane Waterman
4     Reproductive Strategies in Female Rodents 
      Nancy G. Solomon and Brian Keane
5     Sexual Selection: Using Social Ecology to Determine Fitness Differences
      Lara S. Carroll and Wayne K. Potts
6     A Phylogenetic Analysis of the Breeding Systems of Neotomine-Peromyscine Rodents
      Matina C. Kalcounis-Rüppell and David O. Ribble
7     Alternative Reproductive Tactics and Strategies of Tree Squirrels   
      John L. Koprowski

Life Histories and Behavior

8     Fast and Slow Life Histories of Rodents
      F. Stephen Dobson and Madan K. Oli
9     Acceleration and Delay of Reproduction in Rodents
      Lee C. Drickamer
10    Sexual Size Dimorphism in Rodents 
      Albrecht I. Schulte-Hostedde
11    Facultative Sex Ratio Adjustment 
      Robert S. Sikes
12    The Role of the Stress Axis in Life-History Adaptations
      Rudy Boonstra, J. M Barker, J. Castillo, and Q. E. Fletcher
13    Dispersal and Philopatry
      Scott Nunes
14    Gene Dynamics and Social Behavior
      F. Stephen Dobson
15    Social Behavior and Self-Regulation in Murid Rodents
      Charles J. Krebs, Xavier Lambin and Jerry O. Wolff

Behavioral Development

16    Neural Regulation of Social Behavior in Rodents
      J. Thomas Curtis, Yan Liu, Brandon J. Aragona, and Zuoxin Wang
17    Ontogeny of Adaptive Behaviors
      Jill M. Mateo
18    Social Learning by Rodents
      Bennett G. Galef Jr.
19    Kin Recognition in Rodents: Issues and Evidence
      Warren G. Holmes and Jill M. Mateo

Social Behavior

20     Parental Care
       Betty McGuire and William E. Bemis
21     The Ecology of Sociality in Rodents
       Eileen A. Lacey and Paul W. Sherman
22     Scent Marking 
       S. Craig Roberts
23     Nonparental Infanticide
       Luis A. Ebensperger and Daniel T. Blumstein
24     Social Organization and Monogamy in the Beaver
       Peter Busher
25     Evolution of Pacifism and Sociality in Blind Mole Rats
       Eviatar Nevo

Antipredator Behavior

26    Social and Antipredator Systems: Intertwining Links in Multiple Time Frames 
      Donald H. Owings and Richard G. Coss
27    The Evolution of Alarm Communication in Rodents: Structure, Function, and the Puzzle of Apparently Altruistic Calling
      Daniel T. Blumstein
28    Fear and the Foraging, Breeding, and Sociality of Rodents
      Hannu Ylönen and Joel S. Brown

Comparative Socioecology

29    Ecology, Kinship, and Ground Squirrel Sociality: Insights from Comparative Analyses
      James F. Hare and Jan O. Murie
30    Evolution of Sociality in Marmots: It Begins with Hibernation
      Kenneth B. Armitage
31    Environmental Constraints and the Evolution of Sociality in Semifossorial Desert Rodents
      Jan A. Randall
32    Comparative Social Organization and Life History of Rattus and Mus
      Manuel Berdoy and Lee C. Drickamer
33    Social Organization and Resource Use in Capybaras and Maras
      David W. Macdonald, Emilio A. Herrera, Andrew B. Taber, and José Roberto Moreira
34    Social Structure in Octodontid and Ctenomyid Rodents
      Eileen A. Lacey and Luis A. Ebensperger
35    Socioecology of Rock-Dwelling Rodents
      Karen Nutt
36    African Mole-Rats: Social and Ecological Diversity
      Chris G. Faulkes and Nigel C. Bennett
37    Alarm Calling, Multiple Mating, and Infanticide among Black-Tailed, Gunnison’s, and Utah Prairie Dogs
      John L. Hoogland

Conservation and Disease

38    Issues in Rodent Conservation
      William Z. Lidicker Jr.
39    Conservation of Ground Squirrels
      Beatrice Van Horne
40    Conservation of Prairie Dogs
      John L. Hoogland
41    Social Behavior, Demography, and Rodent-Borne Pathogens
      Richard S. Ostfeld and James N. Mills

Conclusions

42    Conclusions and Future Directions
      Paul W. Sherman and Jerry O. Wolff

Index

Editorial Reviews

"Undoubtedly the most exhaustive and progressive analysis of rodent social behavior to date. Deftly edited . . . this well-organized book . . . [is] a significant compendium of more than 50 years of research."

Integrative and Comparative Biology - Heather Patisaul