Table Of ContentPrimatology 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
