From Genes to Animal Behavior: Social Structures, Personalities, Communication by Color PDF
Preview From Genes to Animal Behavior: Social Structures, Personalities, Communication by Color
Primatology Monographs Series Editors Tetsuro Matsuzawa Inuyama, Japan Juichi Yamagiwa Kyoto, Japan For further volumes: http://www.springer.com/series/8796 Miho Inoue-Murayama ● Shoji Kawamura Alexander Weiss Editors From Genes to Animal Behavior Social Structures, Personalities, Communication by Color Editors Miho Inoue-Murayama, Ph.D. Alexander Weiss, Ph.D. Professor Senior Lecturer Wildlife Research Center Psychology Kyoto University School of Philosophy, Psychology 2-24 Tanakasekiden-cho, Sakyo-ku and Language Sciences Kyoto, Kyoto 606-8203 The University of Edinburgh Japan 7 George Square, Preface These individual differences are of the highest importance for us, for they are often inherited, as must be familiar to every one; and they thus afford materials for natural selection to act on and accumulate, in the same manner as man accumulates in any given direction individual differences in his domesticated productions. Charles Darwin, On the Origin of Species When one looks at the natural world, one is immediately struck by the diversity within humans as well as other species, including primates, dogs, birds, and even squid. This diversity did not escape the notice of early naturalists, including Charles Darwin, and the biological and genetic bases of variation in behavioral diversity have been subjects of broad interest since the early days of ethology, sociobiology, comparative psychology, and many other fields. Research on behavioral diversity is challenging, and thus many approaches have been devised to address its natural origins. Only relatively recently have attempts been made to bring these different approaches together. We firmly believe that to truly illuminate the pathways from genotypes to behav- ioral phenotypes requires such an interdisciplinary research program. However, we are aware of certain realities, namely, that behavioral research comprises a seem- ingly vast number of disciplines and subdisciplines. This fact can be seen by the wide range of subject areas from which the authors of the chapters within this volume hail. A quick glance at the author affiliations shows that they study animal behavior from the perspectives of, among others, evolutionary biology, genetics, anthropol- ogy, agriculture, and behavioral ecology. One unfortunate consequence of this diversity is that it makes attempts to unify the study of behavior particularly diffi- cult, as the various disciplines and subdisciplines each include several variables, whether they are proximity behaviors, coloration, or personality, that are not well- understood by those in other areas. Another complicating factor arises from the fact that, given the specialization of many journals, it can be difficult for members of one discipline or even subdiscipline to keep up with the literature in other areas. We therefore felt that there was a need for a volume to describe the methods and find- ings of researchers in several subdisciplines. It is our sincere hope that this volume represents an advance in this direction and will help researchers studying the path- ways from the genotypes to behavioral phenotypes learn from and even collaborate v vi Preface with one another. To these ends we divided the book into five sections: kin and sexual selection; personality research; the genetic bases of personality; coloration and color vision; and other biochemical measures. The chapters in each of these sections show how researchers in different areas study a particular question or set of questions about animal behavior. While these chapters do not encompass all pos- sible research questions or methods, they have in common the fact that they all demonstrate how by bridging different research areas one can better understand the complex nature of behavioral diversity. The first section concerns kin and sexual selection, perhaps two of the oldest research areas in modern evolutionary biology. These research areas are essential to understanding the evolution of social behaviors and therefore this section sum- marizes research on kinship analyses using genetic markers and the analyses of genes related to reproductive behavior, which have provided various insights into sexual and kin selection. In summarizing this research area, this section covers diverse taxa, including primates, rodents, birds, and eusocial insects, and its chap- ters focus on topics that reflect taxonomic characters. The first chapter in this sec- tion is a review by Jörns Fickel and Alexandra Weyrich which examines female mate choice in rodents. Their chapter summarizes recent thinking about sexual selection and highlights several factors that may influence female mate choice, including the major histocompatibility complex, oxytocin, and olfactory receptor genes. In the second chapter, Emmi Schlicht and Bart Kempenaers review the effect of extra-pair paternity on sexual selection (mainly) in birds. They first point out the problems in the calculations used to quantify the effect of extra-pair paternity and how these effects are interpreted. They then suggest that multiple matings appear to drive sexual selection in several monogamous avian species. The third chapter in this section is a review from Eiji Inoue which examines male reproductive success and cooperative and affiliative behaviors among paternal relatives in nonhuman primates. The review shows that paternal kin-biased behavior is observed in some conditions, but that the particular conditions and mechanisms underlying paternal kin recognition are unclear. The final chapter in this section is a review from Koji Tsuchida which examines conflict resolution among eusocial wasps in light of kin selection frameworks with particular regard to foundress groups, sex ratio, and male parentage. He shows that kin selection theory is limited in its ability to explain adaptive conflict resolution among nestmates. The second section focuses on animal personality research, an area that is just gaining traction in evolutionary biology and behavioral ecology, sometimes under labels such as temperament or behavioral syndromes. Although it has a well-estab- lished pedigree in human psychology research, much of this rich knowledge is unfamiliar to researchers in these other areas. Similarly, much of the recent work on personality coming from evolutionary biology and behavioral ecology is unfamiliar to psychologists. We hope that this section introduces members of these disciplines to new methods and concepts, which will enable them to better study substantive questions about personality evolution in humans as well as nonhuman animals. To these ends this section begins with a chapter by Sonja Koski, who reviews the meth- ods used by and some findings of psychologists and evolutionary biologists who Preface vii study animal personality. Her chapter synthesizes these areas and should help those who study animal personality in psychology and evolutionary biology better advance their common goals. The second chapter in this section is a theoretical chapter by Mark James Adams which highlights how evolutionary and quantitative genetics can inform the study of personality in nonhuman primates in psychology as well as evolutionary biology, with particular attention being paid to possible evolutionary mechanisms that might maintain variation. In particular, this chapter focuses on illustrating quantitative methods that can be used to study wild populations of non- human primates and other animals, which do not lend themselves to more experi- mental approaches. The third chapter is a review of behavioral genetics research on animal personality by Kees van Oers and David Sinn. Their review focuses on the “phenotypic gambit,” an assumption that the phenotypic structure of personality reflects the genetic structure of personality. They conclude that the literature sup- ports this assumption, although they warn of possible dangers, given that little is known about how well genetic influences generalize across age, sex, and environ- ments. They then point out several useful directions for future researchers who wish to address these unanswered questions. The fourth and fifth chapters in this section highlight how animal personality research can be applied to practical problems. The research described in these chapters can lead to discoveries regarding the role per- sonality plays in social interactions and mating in different species, including those that are difficult to study in the wild or in laboratory conditions. Similarly, these chapters highlight how a genetically influenced phenotype such as personality inter- acts with the environment to bring about positive affect or well-being. In the first of these chapters, Marieke Gartner and David Powell highlight how personality can be applied to improve conservation of zoo-housed animals and maximize their well- being. They then describe in detail how personality data can be used when introduc- ing new animals into existing exhibits, to find pairs that will readily mate and produce offspring, and to devise enrichment programs that respect and cater to the differences among individuals within each exhibit. In the second of these chapters, Simon Turner, Jenny Gibbons, and Marie Haskell describe how they and others have used methods from psychology and biology to develop and validate measures of temperament for agriculturally important species, such as pigs and cattle. Moreover, this chapter highlights the possible practical uses of these measures to improve the conditions of these animals and the safety of their handlers by reducing levels of aggression and fear by selective breeding based on genetic indices. The third section follows closely from the prior section in that it, too, focuses on studies of personality. However, this section highlights molecular genetic research in the area, and, in particular, attempts to relate personality traits to genetic loci. It begins with a summary by Kouta Kanno and Shoichi Ishiura, who review their attempts to find genetic markers for personality traits in humans, and especially their work on the in vitro expression of the dopamine transporter (DAT1) gene. As will become clear to readers, while several candidate genes exist, findings from association studies have been mixed. The next three chapters in this section describe studies of nonhuman animal personality. In the second chapter, Miho Inoue-Murayama, Alexander Weiss, Naruki Morimura, Masayuki Tanaka, Juichi Yamagiwa, and Gen’ichi Idani viii Preface describe studies of the genetics of personality in great apes. The chapter summarizes recent research on candidate genes believed to underlie human personality variation in aggression and affiliation. Their research has demonstrated that differences in the allelic distribution of genes such as the monoamine oxidase and vasopressin receptor genes may explain trait differences at the within- and between-species levels of analy- ses. This chapter is followed by an exciting chapter from Enikő Kubinyi, Mária Sasvári-Székely, and Ádám Miklósi on the genetics of personality in dogs. We think the authors make a convincing case that, because dogs co-evolved with humans and have had their behaviors and other traits shaped by humans via selective breeding, they are an excellent model species for studying the genetics of personality. Their chapter summarizes research in multiple areas, including the means used to measure personal- ity in dogs, the results of genetic association studies, and studies that reveal how gene function differs across breeds. Andrew Fidler’s chapter concludes this section. He describes his work combining classical ethological studies and modern molecular genetic approaches to reveal how neuroendocrine mechanisms and evolution have yielded persistent individual differences in avian behavior. Moreover, he shows how the results of his studies can lead to practical interventions to improve poultry breeding and to protecting endangered avian species such as the kea (Nestor notabilis). The fourth section focuses on the evolutionary and genetic bases of vertebrate body coloration and color vision. Sensory organs and adaptations are fundamental determinants of behavior across the animal kingdom. Animals sense external stimuli through sensory organs and react to stimuli with a variety of behaviors, including foraging for food, escaping predators, navigating their environment, and mating. Of the senses, vision is best understood with respect to its genetic mechanisms and variation. In response to environmental conditions, different species evolved several types of color vision, and animal coloration has evolved and diversified as a signal. The first chapter in this section is by Nicholas Mundy, who discusses research on the evolutionary genetics of coloration in vertebrates. The study of coloration pro- vides an excellent opportunity to illuminate the mechanisms of phenotypic evolution from genetics to behavioral adaptation. Thus, this section introduces the proximate bases of coloration and the types of color variation followed by a discussion on progress in identifying the molecular basis of color variation in wild vertebrates. This progress includes discoveries that suggest considerable convergence in the genetic mechanisms underlying color variation across broad phylogenetic scales. However, genes underlying color variation in many nonhuman primates are still waiting to be uncovered. In the second chapter of this section, Yohey Terai and Norihiro Okada review their exciting work on speciation in the cichlid fish in Lake Victoria. They describe how coloration and sensory adaptations to different light environments led to speciation and how such a study system helps to understand the molecular bases of evolution. In the final chapter of this section Shoji Kawamura reviews recent research on the selective pressures leading to the evolution and diver- sity of vertebrate color vision and aspects of the visual sensory system. The chapter therefore summarizes recent exciting findings on the relationship between opsin genes and behavior. Because patchy and spectrally varying illumination is more common in shallow water and in forests, the review focuses on fish and primate spe- cies that are highly polymorphic with respect to color vision. Preface ix The fifth section focuses on the biochemical and neurological underpinnings of mind, behavior, and social interactions in humans and nonhuman primates. In doing so, the section describes several new technologies that can be used to study behavior. These physiological measures are advantageous in that, as pheno- types, they are closer to the actual genetic influences underlying behavioral traits than responses to a questionnaire or even behavior. In the first chapter, Takamasa Koyama and Akiko Nakagami, review their experimental research showing how endocrine-disrupting chemicals may influence socialization in macaques (Macaca mulatta and Macaca fascicularis). This work is important as it highlights the subtle, although potentially serious, effects that environmental pollutants may have on humans and other species. The next two chapters focus on the use of neuroimaging technologies to better understand mechanisms underlying geneti- cally based individual differences in behavior. In the first of these chapters, Hideki Ohira reviews his group’s studies on the neural basis of individual differ- ences in positive and negative emotional reactivity and postulate hypotheses regarding the genetic regulation of these relationships in humans. Using positron emissions technology (PET) scanning as well as cardiovascular and neuroendo- crine indices, they found that positive and negative emotions lead to coordinated physiological responses, although these responses can be regulated by cognitive appraisal of the situation. In the final chapter, Chihiro Yokoyama and Hirotaka Onoe describe the development of a method that can be used to conduct PET scans on conscious nonhuman primates. They then describe how measures derived via this approach helped to better understand the molecular bases of social behavior and the sensory system in a New World Monkey, the common marmoset (Callithrix jacchus). While the use of these methods in studies of non- human primate behavior is not widespread at present, we expect they might be important in the near future. Although this volume is not comprehensive, we hope that by focusing on a selection of topics it will convey the most cutting-edge research in the study of animal behavior, perception, genetics, and evolution. It is our express wish that researchers in various disciplines will benefit from the chapters herein and possibly be inspired to expand their existing research programs with new technologies, mea- sures, or collaborations with researchers in other areas. For example, PET imaging studies on conscious nonhuman primates could be used to better understand the neural mechanisms underlying personality or kin recognition; studies examining whether coloration is linked to behavioral consistencies or personality may enable researchers to identify personality-related genes; and quantitative genetic studies in wild populations may highlight the genetic bases of phenotypes such as female preference for mates. Such interdisciplinarity will be central to gaining insights into animal and human behavior. We look forward to this new body of research and hope it will be the basis of a new volume at some point in the near future. As should be clear, the authors spent a great deal of time and effort in writing their respective chapters. For this, we offer our most humble gratitude. We would also like to thank Eiji Inoue, who contributed to the book by editing and reviewing chapters, especially those in the first section. In addition, we are also grateful to Nick Mundy and Yohei Terai, who helped review the chapters in the fourth section. x Preface We also offer thanks to Sayaka Kato, who provided invaluable assistance during the editing process and to Aiko Hiraguchi and Kaoru Hashimoto of Springer Japan for their assistance in putting together this volume. This book could not have been completed without the guidance and support of the series editors, Tetsuro Matsuzawa and Juichi Yamagiwa, and three anonymous reviewers who made valu- able comments about an earlier draft. In addition, the work of numerous collabora- tors, post-doctoral researchers, and students was integral to much of the research discussed herein. Finally, we would like to thank our loved ones and family mem- bers for their support throughout. Miho Inoue-Murayama Shoji Kawamura Alexander Weiss Contents Part I Sexual and Kin Selection in Animals 1 Female Mate Choice in Rodents .............................................................. 3 Jörns Fickel and Alexandra Weyrich 2 Extra-Pair Paternity and Sexual Selection ............................................. 35 Emmi Schlicht and Bart Kempenaers 3 Male Reproductive Skew and Paternal Kin-Biased Behavior in Primates ................................................................................ 67 Eiji Inoue 4 Social Structures and Conflict Resolution in Primitively Eusocial Polistes Wasps ............................................................................. 83 Koji Tsuchida Part II E volutionary Bases and Practical Implications of Animal Personality and Temperament 5 How to Measure Animal Personality and Why Does It Matter? Integrating the Psychological and Biological Approaches to Animal Personality ............................................................................... 115 Sonja E. Koski 6 Evolutionary Genetics of Personality in Nonhuman Primates ............. 137 Mark James Adams 7 Toward a Basis for the Phenotypic Gambit: Advances in the Evolutionary Genetics of Animal Personality .............................. 165 Kees van Oers and David L. Sinn xi
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