Primer Effects by Murine Pheromone Signaling: Pheromonal Influences on Reproductive Conditions

99 Pages·2016·2.287 MB·English

by  Sachiko Koyama (auth.)

SPRINGER BRIEFS IN ANIMAL SCIENCES
Sachiko Koyama
Primer Effects by
Murine Pheromone
Signaling
Pheromonal
Influences on
Reproductive
Conditions
SpringerBriefs in Animal Sciences
More information about this series at http://www.springer.com/series/10153
Sachiko Koyama
Primer Effects by Murine
Pheromone Signaling
fl
Pheromonal In uences on Reproductive
Conditions
123
SachikoKoyama
Schoolof Medicine, Medical Science
Program
Indiana University
Bloomington,IN
USA
ISSN 2211-7504 ISSN 2211-7512 (electronic)
SpringerBriefs inAnimal Sciences
ISBN978-3-319-13932-6 ISBN978-3-319-13933-3 (eBook)
DOI 10.1007/978-3-319-13933-3
LibraryofCongressControlNumber:2016933470
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Preface
Nowadays the word “pheromone” is well known. However, the popular image of
pheromones usually involves some mysterious, invisible chemicals that make
people attracted to the opposite sex perhaps because of the use of the word in the
names of some perfumes. Pheromones have many functions. Indeed some of them
function as attractants between the sexes, and some stimulate aggression between
membersofthesamesex, especiallyinmales. The functionthatperhaps isnotyet
well known is their affect on the reproductive status of others. In this context,
males’ pheromones stimulate females’ reproductive status and females’ pher-
omones stimulate males’ reproductive status. Although studies in mice have pro-
gressed substantially, mechanistic clarification of these phenomena may provide
valuable applicability to humans as well.
Thestudyofolfactorycommunicationinmiceadvanceddramaticallyduringthe
last half of the twentieth century, beginning with the first observation findings on
physiological changes in females in the 1950s to the chemical identification of the
responsible pheromones that followed in the 1980s. The first observations were
of the influences of conspecific odors on the estrous cycles and establishment of
pregnancy in female mice, effects that came to be called Lee-Boot effect, Whitten
effect, Bruce effect, and Vandenbergh effect (Chap. 3). These influences of con-
specific odors on physiological conditions are called “primer effects,” whereas the
influences of conspecific odors on behaviors are called “releaser effects.” In this
book, I will focus on the primer effects, other than in Chap. 4 Identification of
Pheromones, where I described about some releaser effects in explaining the
pheromones that had been identified so far.
In the 1990s, olfactory neuroscience research produced a transition of the
investigationofolfactorycommunicationfromclassicbehavioralbiologystudiesto
studies usingthetechniques inmolecularbiologyand/orneuroscience,studies that
included the use of transgenic mice. My own studies at college included animal
psychologyandIbecameinterestedinthefieldofethology,theevolutionofanimal
behaviors and their adaptive functions. I subsequently obtained my Ph.D. in
EthologyandIlaterstudiedcellbiologyandthereproductivephysiologyofsperm
v
vi Preface
cells as a postdoctoral fellow at the University of Tokyo in the laboratory of Prof.
ShinjiKamimura (currentlyatChuoUniversity,Japan).Ifoundthatspermdensity
inthemalesexposedtofemale-soiledbeddingisenhancedandthatspermmotility
inthesubordinatemales issuppressed compared todominant males(see Chap.3).
My training in cell biology opened my eyes to microscopic studies of cells, a
major transition from my earlier macroscopic studies of social behaviors in mice
using mazes or encounter boxes. Following that, I expanded my professional
trainingtoneurogenesisandstudiesofmammaryglands.Thatledtotwoadditional
new findings, an enhanced development of mammary glands in female mice by
exposure to a male murine pheromone, and an enhanced cognitive function in the
next generation of these females (both discussed in Chap. 5). I also identified the
pheromones that stimulate adult neurogenesis (Chap. 5). In summary, my studies
and collaborations with the people working in these diverse fields led me to dis-
cover four new primer effects that will be the main topics of this book: effects on
sperm motility, sperm density, mammary glands, and enhanced cognitive function
in the next generation.
Ihaveintentionallyincludedinthisbooktheinformationthatisdifficulttowrite
inacademicpapers.Examplesincludethedetailsofmousebiologythatmayaffect
odorsofmiceandtheirresponsestoodorsofothermice,aswellasthekeystepsin
thescientificendeavorthatledtoexcitingresultsinsuccessfulexperiments,orthat
led to negative results, which sometimes give us important information as well.
This information may be important for students and for junior scientists. I believe
thattheabilitytoincludesuchinformationisoneofthebenefitsinwritingabook.
Acknowledgments
There are many people to whom I would like to express my thanks. First of all, I
would like to express my sincere thanks to Shinji Kamimura of the University of
Tokyo (currently at Chuo University, Japan), who expanded my knowledge and
techniquesfromanimalpsychologyandethologytocellbiologyofspermcells.IfI
did not have the chance to collaborate with him, we could never find the primer
effectsinmalesthatwefound.Hewasgenerousenoughtocombinetheknowledge
fromdifferentstudyfields,whichInowknowthatitisextremelyrare,and,besides,
he enthusiastically used the metaphor of “a fusion of atoms gives off enormous
energy” in explaining our interdisciplinary project to his colleagues at the
UniversityofTokyo.Nothingismoreencouragingthanthisinconductingatotally
new interdisciplinary scientific activity. The pheromone projects on neurogenesis,
mammaryglands,andtrans-generationalinfluencesofpheromoneswereconducted
in collaboration with many people, but especially with Milos V. Novotny and
Helena A. Soini of the Department of Chemistry, and John Foley of the School of
Medicine of Indiana University. Utilization of the synthetic analogues of pher-
omones, which Milos Novotny generated, enabled precise control of exposure to
pheromones, and collaboration with John Foley whose profession is molecular
biologyofmammaryglandsenabledexpansionoftheprojectstoincludemammary
glands and molecular level analyses. I would also like to express my sincere
gratitude to John Watkins, III of the School of Medicine of Indiana University for
allhissupport.AnotherspecialsinceregratitudegoestoRobertKarnofUniversity
of Arizona, who thoroughly edited my English in the Preface and Chap. 1, and
provided many comments on mouse biology from his profession of wild mouse
geneticsandgeographicaldistributionofwildhousemousesubspecies.Iappreciate
Silvia Herold and Claus-Dieter Bachem of SpringerBrief for providing me this
exciting chance to write a book on murine pheromone signaling. And last but not
least, I appreciate my family in Japan for understanding that I am a scientist who
would never stop studying and pursuing my science. It is always exciting to think
about a new hypothesis.
vii
Contents
1 Introduction: The Laboratory Mice . . . . . . . . . . . . . . . . . . . . . . . . 1
1.1 Ethology and the Study Field of Olfactory Communication
in Laboratory Mice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 The Social System and Breeding System . . . . . . . . . . . . . . . . . . 3
1.3 Pregnancy, Delivery, and the Growth and Development
of the Offspring. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
1.4 Mouse Biology, Hormones, Pheromones, and Pheromone
Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
2 The Olfactory Systems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.1 The Olfactory Systems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.2 The Main Olfactory System and Its Pathway in Relation
to Pheromone Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
2.3 Accessory Olfactory System (Vomeronasal System). . . . . . . . . . . 15
2.4 Responses to Pheromone Are not Always the Same. . . . . . . . . . . 17
2.5 Sex Differences in the Responses to Pheromones. . . . . . . . . . . . . 20
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
3 The Primer Effects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
3.1 The Lee–Boot Effect, Whitten Effect, and Vandenbergh Effect . . . 23
3.2 Bruce Effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
3.3 Primer Effect in Males . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
3.3.1 Social Dominance and Sperm Motility. . . . . . . . . . . . . . . 29
3.3.2 Female Odors and Sperm Density . . . . . . . . . . . . . . . . . . 31
3.3.3 Influence of Adult Males’ Odor on Sperm Morphology . . . 35
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
ix
x Contents
4 Identification of Pheromones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
4.1 Pheromones to Induce Primer Effects. . . . . . . . . . . . . . . . . . . . . 39
4.2 Pheromones to Induce Releaser Effects. . . . . . . . . . . . . . . . . . . . 43
4.2.1 Aggression. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
4.2.2 Sexual Behaviors and Pheromones in Tears: The Esps. . . . 44
4.2.3 Kin Recognition, Subspecies Recognition,
and Mate Preference . . . . . . . . . . . . . . . . . . . . . . . . . . . 45
4.2.4 Rooting Behaviors by Neonates: Are There
Pheromones in Mouse Milk? . . . . . . . . . . . . . . . . . . . . . 50
4.2.5 Parental Behaviors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
5 New Primer Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
5.1 From Early Studies to New Studies . . . . . . . . . . . . . . . . . . . . . . 59
5.2 Adult Neurogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60
5.3 Odors of Opposite Sex Stimulate Neurogenesis. . . . . . . . . . . . . . 60
5.4 Identification of Pheromones that Stimulate Cell Proliferation
in the Brain. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
5.4.1 Female Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
5.4.2 Male Studies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66
5.5 Mammary Gland Expansion by Exposure to Male Pheromone. . . . 68
5.6 Trans-generational Influence of Exposure to Pheromones . . . . . . . 70
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
6 Ontogeny. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
6.1 Ontogeny of the Olfactory System. . . . . . . . . . . . . . . . . . . . . . . 75
6.2 Developmental Changes in the Responses to Pheromones. . . . . . . 78
6.3 Epigenetic Changes on the Sensitivity to Smell. . . . . . . . . . . . . . 79
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
7 Adaptive Functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
7.1 What is their Function in Reproductive Success?. . . . . . . . . . . . . 85
7.2 Function of Enhanced Adult Neurogenesis by Exposure to
Pheromones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
7.3 Possible Pheromonal Signaling in Humans and its Function . . . . . 87
Appendix. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90