Gene-Environment Interplay

131 Pages·2012·1.674 MB·2-128\131

by  Marla B. Sokolowski and Stephen F. Goodwin (Eds.)

Advances
in
Genetics, Volume 77
Serial Editors
Theodore Friedmann
University of California at San Diego, School of Medicine, USA
Jay C. Dunlap
The Geisel School of Medicine at Dartmouth, Hanover, NH, USA
Stephen F. Goodwin
University of Oxford, Oxford, UK
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Contributors
Numbersinparenthesesindicatethepagesonwhichtheauthors’contributionsbegin.
JadeAtallah(59) DepartmentofBiology,UniversityofTorontoatMississauga,
Mississauga, Ontario,Canada
GuyBloch(1) DepartmentofEcology,EvolutionandBehavior,TheAlexander
Silberman Institute of Life Sciences, The Hebrew University of
Jerusalem, Jerusalem, Israel
Frances A. Champagne (33) Department of Psychology, Columbia University,
NewYork,USA
Ada Eban-Rothschild1 (1) Department of Ecology, Evolution and Behavior,
The Alexander Silberman Institute of Life Sciences, The Hebrew
UniversityofJerusalem, Jerusalem, Israel
Joel D. Levine (59) Department of Biology, University of Toronto at
Mississauga, Mississauga, Ontario,Canada
O¨zge O¨zkaya (79) Department of Genetics, University of Leicester, Leicester,
UnitedKingdom
Ezio Rosato (79) Department of Genetics, University of Leicester, Leicester,
UnitedKingdom
Jonathan Schneider (59) Department of Biology, University of Toronto at
Mississauga, Mississauga, Ontario,Canada
1Currentaddress:DepartmentofPsychiatryandBehavioralSciences,StanfordUniversity,
Stanford,California,USA
vii
Preface
Thereareanumberofcommonthemesthathaveemergedinrecentyearsfrom
bothanimalandhumanresearchongenesandbehavior.Theconceptofgene–
environment interplay is one of the most exciting. Our thinking about how
individualdifferencesinbehaviorarisehascomealongwayfromthedayswhen
psychologists answered this question by saying it is the environment and bi-
ologists attributed it to genes. Fortunately, this nature–nurture dichotomy has
finally been put to rest. Even the question of what proportion of phenotypic
variation is genetic compared to environmental (genes þ environment) makes
littlesensewithourcurrentunderstandingabouthowgenesareabletolistento
the environment. The concept of gene–environment interactions (G (cid:2) E)
emerged from the inadequacies of broad sense heritability measures. Initially
G(cid:2)Eweredeterminedbystatisticalinteractionsbetweenbehavioralmeasures
of two or more genotypes measured in two or more environments. With the
advent of genetic technologies, research moved onto measuring G (cid:2) E effects
arising from allelic variation in single genes in individuals exposed to different
environments.Morerecently,G(cid:2)Ehavebeenmeasuredatthegenomelevel.
Theconcept ofgene–environment interplay encompasses bothG(cid:2) E
andepigenetics.Epigeneticsoffersanothersetofbiologicalmechanismswhereby
theenvironmentcangetunderourskinwithoutthenecessityoftherebeingDNA
sequence variation. It provides biological mechanisms for why identical
twins with the same DNA sequences nevertheless differ in their phenotypes.
Like G (cid:2) E, changes in the epigenome are responsive to many interesting
environmental factors within and around the individual including the social
environment. We now know that our genome is listening to our environment
andrespondstoitwithchangesintheexpressionofourgenes.
Gene–environmentinterplaychangesduringdevelopment.Thereisan
active interplay during prenatal and postnatal development and adulthood
between our genome and the environments we experience. What happens at
onedevelopmentstagesignificantlyaffectsthedevelopmentaleventsthatfollow.
Researchhascomealongwayfromthenowdebunkedconceptofnature–nurture.
This volume provides a sampling of some of the new and elegant
researchbeingperformedongene–environmentinterplay.
Chapter 1 is from Ada Eban-Rothschild and Guy Bloch; they review
studies in Drosophila melanogaster and the bee Apis mellifera, which suggest that
social influences on the clock are more important than previously recognized.
Studying social behavior in Drosophila has all the advantages of advanced
ix
x Preface
molecular genetics with anatomical, physiological, and behavioral approaches,
andthebeecanbestudiedandmanipulatedinanecologicallyrelevantcontext.
Thesestudieswillbeasteppingstonetoimportantbreakthroughsinourunder-
standingofthemechanismsunderlyingsocialinfluencesonsleepandcircadian
rhythms.
Chapter 2 is from Frances A. Champagne. The relatively new field of
epigenetics, the study of how a gene’s function or expression can be changed
withoutalterationstothegeneticcode,haschangedthewaywethinkaboutour
geneticmakeup.InChampagne’sfascinatingreview,shediscussestheepigenetics
ofsocialexperience,emphasizingtheroleofepigeneticmechanismsinshaping
variation in social behavior and the implications of epigenetics for our under-
standingofthetransmissionoftraitsacrossgenerations.
Chapter 3 is from Joel D. Levine’s lab. Levine’s group has pioneered
studies in Drosophila by observing fly social interactions. They have noted that
in group situations flies engage in complex social interactions that influence
learning, circadian clocks, aggression, and mating. This systems-level network
approach to the study of Drosophila groups will be key to understanding the
regulationandmodulationofsuchgroupsocialbehaviorsandtheimportanceof
contextinregulatingthem.
Chapter 4 is from Ezio Rosato’s lab. This fresh perspective on the
circadian clock in the fly provides a uniquely deep understanding of the topic
under discussion amenable to all readers, while at the same time bringing in
those papers that challenge the current notion of how the molecular clock
operates atthecellular level,and provides anew view on theorganization and
theevolutionofcircadianclocks.
MARLAB.SOKOLOWSKI
STEPHENF.GOODWIN
1
Social Influences on Circadian
Rhythms and Sleep in Insects
Ada Eban-Rothschild1 and Guy Bloch
Department of Ecology, Evolution and Behavior, The Alexander Silberman
InstituteofLifeSciences,TheHebrewUniversityofJerusalem,Jerusalem,Israel
I. Introduction
II. TheCircadianSystemofInsects
III. SocialInfluencesonCircadianRhythmsinInsects
A. Socialsynchronization
B. Socialinfluencesontheontogenyofcircadianrhythms
C. Socialmodulationofplasticityintheexpressionofcircadian
rhythms
D. Additionalsocialinfluencesoncircadianrhythms
IV. Sleep
A. Sleepininvertebrates
B. Sleepinhoneybeeswithandwithoutcircadianrhythms
V. SocialInfluencesonSleepinInsects
VI. Conclusions
Acknowledgments
References
1Currentaddress:DepartmentofPsychiatryandBehavioralSciences,StanfordUniversity,
Stanford,California,USA
AdvancesinGenetics,Vol.77 0065-2660/12$35.00
Copyright2012,ElsevierInc.Allrightsreserved. http://dx.doi.org/10.1016/B978-0-12-387687-4.00001-5
2 Eban-Rothschild and Bloch
ABSTRACT
Thediversesociallifestyleandthesmallandaccessiblenervoussystemofinsects
make them valuable for research on the adaptive value and the organization
principles of circadian rhythms and sleep. We focus on two complementary
modelinsects,thefruitflyDrosophilamelanogaster,whichisamenabletoexten-
sivetransgenicmanipulations,andthehoney beeApismellifera,which hasrich
andwell-studiedsocialbehaviors.Socialentrainmentofactivityrhythms(social
synchronization)hasbeenstudiedinmanyanimals.Socialtimegiversappearto
be specifically important in dark cavity-dwelling social animals, but here there
are no other clear relationships between the degree of sociality and the effec-
tiveness of social entrainment. The olfactory system is important for social
entrainment in insects. Little is known, however, about the molecular and
neuronalpathwayslinkingolfactoryneuronstothecentralclock.Inthehoney
bee, the expression, phase, and development of circadian rhythms are socially
regulated, apparently by different signals. Peripheral clocks regulating phero-
mone synthesis and the olfactory system have been implicated in social influ-
ences on circadian rhythms in the fruit fly. An enriched social environment
increasesthetotalamountofsleepinbothfruitfliesandhoneybees.Infruitflies,
thesechangeshavebeenlinkedtomolecularandneuronalprocessesinvolvedin
learning, memory, and synaptic plasticity. The studies on insects suggest that
socialinfluencesontheclockarericherthanpreviouslyappreciatedandhaveled
toimportantbreakthroughsinourunderstandingofthemechanismsunderlying
socialinfluencesonsleepandcircadianrhythms. (cid:1)2012,ElsevierInc.
I. INTRODUCTION
Thesocialenvironment,whichwedefineasthesumofsocialinteractions,cues,
andsignalsencounteredbyananimal,hasaprofoundinfluenceonitsdevelop-
ment,physiology,andbehavior.Inthecurrentreview,wefocusontheinfluences
of the social environment on two fundamental biological systems, circadian
rhythms and sleep, in insects. Circadian rhythms are biological rhythms that
cycle with a daily period of roughly 24h (see Section II). Sleep is a complex
behavioralstatethatischaracterizedbyreducedactivityandresponsiveness(see
Section IV). These two systems interact in various ways. For example, the
circadianclockinfluencesthetimingofsleepandwakefulness,andclockgenes
areimplicatedintheregulationofdifferentaspectsofsleep,suchassleepquality
and homeostasis (Andretic et al., 2005; Sehgal and Mignot, 2011). Circadian
rhythms and sleep are sensitive to environmental variables such as light and
temperature(forarecentreviewseePeschelandHelfrich-Forster,2011).There
is also evidence that circadian rhythms and sleep are influenced by the social
1.SocialInfluencesonCircadianRhythmsandSleep 3
environment,butlittleisknownaboutthefunctionalsignificanceorthemech-
anismsunderlyingtheseinteractions(DavidsonandMenaker,2003;Mistlberger
and Skene, 2004). Insects provide an excellent system for addressing these
questionsbecausetheirnervoussystemisrelativelysmallandaccessible.Insects
are very diverse in terms of their activity phase and include species that are
diurnal,nocturnal,orcrepuscular,aswellasthosethatcanswitchbetweenthese
statesorbeactivewithnocircadianrhythms.Importantly,insectsshowabroad
rangeofsociallifestyles,rangingfromsolitarytohighlystructuredsocieties.
Highly eusocial insects such as ants, honey bees, and termites are
characterized by the restriction of reproduction to a single or a few individuals
(e.g.,queens),bythefactthatindividualsfromoldergenerationscooperatively
carefortheyoung,andbyanelaboratecommunicationsystem(Wilson,1971).
Thesocialenvironmentinfluencesalmosteveryfacetofthelifeofhighlysocial
insects, including their patterns of activity and sleep (see below). The social
environment is also important for many animals living in simple societies, and
forsolitaryanimalsaswell.Thesocialenvironmentoftheseanimalsmayinclude
interactions with potential mates, offspring, or conspecifics with which they
compete for resources such as territory, shelter, or mates. We focus mainly on
the highly social honey bee and the fruit fly, which is commonly considered
solitary or facultatively gregarious. The honey bee provides an excellent model
foridentifyingandstudyingthesocialsignalsinfluencingcircadianrhythmsand
sleep in an ecological context. The arsenal of genetic and transgenic toolkits
available for Drosophila make it an excellent model for studying the molecular
mechanismsunderlyingtheinteractionbetweensocialfactorsandthecircadian
andsleepsystems.
II. THE CIRCADIAN SYSTEM OF INSECTS
Circadianrhythmsaredefinedasbiologicalrhythmsthatmeetthefollowingthree
criteria:(1)theypersist,or“free-run,”withaperiodofabout24hintheabsenceof
external time cues, (2) they are reset, or entrained, by environmental cues, in
particular,lightandtemperature,and(3)theyexhibit“temperaturecompensation”;
in other words, their period length is stable over a wide range of physiological
temperatures. The circadian clock influences many physiological and behavioral
processesininsects.Theseincludeactivity,thesleep-wakecycle,feeding,mating,
oviposition,egghatching,andpupaleclosion.Thecircadianclockisalsoinvolved
inmeasuringdaylength,andinfluencesphotoperiodismandannualrhythms,such
asdiapauseandseasonalreproduction(Dunlapetal.,2004;Saunders,2002).
The circadian system has been traditionally described as having
three functional components, although today this description is regarded as a
useful conceptual framework rather than a strict description of the system
4 Eban-Rothschild and Bloch
(Zhang and Kay, 2010). The core of the clock is composed of pacemakers,
cell-autonomousrhythmgeneratorsthatcycleapproximatelywitha24-hperiod.
The central pacemaker is entrained by input pathways in which environmental
signals are detected, converted to sensory information, and transmitted to the
centralpacemakers.Outputpathwayscarrytemporalsignalsawayfrompacemak-
er cells to various biochemical, physiological, and behavioral processes (Bell-
Pedersenetal.,2005;Dunlapetal.,2004;Saunders,2002).Themolecularbases
ofrhythmgenerationinpacemakersoforganismsasdiverseasfungi,plants,fruit
flies, and mammals consist of interlocked autoregulatory transcriptional/ trans-
lational feedback loops with positive and negative elements. The pacemaker
cells of animals are interconnected in a circadian network that couples
their activities and orchestrates normal rhythms in physiology and behavior
(Bell-Pedersenetal.,2005;Dunlapetal.,2004).
The insect for which the circadian clockwork has been best charac-
terized is the fruit fly Drosophila melanogaster (see Peschel and Helfrich-Forster
(2011) for a recent review, and Zhang and Kay (2010) for an updated list of
clock genes). The transcription factors Clock (Clk) and Cycle (Cyc) (the
positive elements) form a dimer and activate the transcription of the transcrip-
tion factors Period (Per) and Timeless (Tim1) (the negative elements). Per and
Tim1 are translated into proteins that enter the nucleus where they interfere
with the transcriptional activity of the CLK:CYC complex and concomitantly
shut down their own expression. Par Domain Protein 1 (Pdp1), Vrille (Vri), and
Clockwork Orange (Cwo) act together with Clk in an interlocked feedback
loop that is thought to stabilize the Per/Tim1 loop. Additional proteins
including several kinases and phosphatases fine tune this cell-autonomous
rhythm generation machinery by modulating the stability of the canonical
clock genes. Drosophila-type Cryptochrome (Cry-d, also known as insect Cry1)
has a photic input function. Although the genes and the organizational
principles of the molecular clockwork of mammals and Drosophila are similar,
there are some important differences between them. For example, mammals
do not have orthologs for Tim1 and Cry-d, but have three paralogs for Per.
They also have two paralogs for Cry (mammalian-type Cry, their insect
orthologs are also known as insect Cry2) that act together with the Per
genes in the negative loop of the clock.
The recent sequencing of the genomes of several insects and other
invertebrates indicates that there is notable variation in the molecular organi-
zationoftheinsectclock.Forexample,thegenomeofthehoneybeeandother
speciesoftheorderHymenopteradoesnotencodeorthologstoCry-dandTim1
genes, but does encode the mammalian-type transcriptional repressing Cry-m
(Ingram and BloIngram et al. submitted; Rubin et al., 2006; Yuan et al., 2007).
The functional significance of this variability in the molecular organization of
thecircadianclockworkininsectsisunknown(Rubinetal.,2006).
1.SocialInfluencesonCircadianRhythmsandSleep 5
There is also considerable variation in the anatomical organization of
thecircadiannetworkintheinsectbrain(Helfrich-Forsteretal.,1998;Sehadova
et al., 2003; Zavodska et al., 2003). The clock network of Drosophila comprises
about150neurons/brainhemispherethataretypicallyclassifiedintosevenmajor
neuroanatomicalgroups.Therearethreegroupslocatedinthedorsalpartofthe
brain, termed dorsal neurons 1–3 (DN ). The other four groups are located
1–3
morelaterallyandventrallyandarecalledlateralneurons(LN ,l-LN ,LPN,and
d v
s-LN ).Clockproteinsarealsoexpressedinafewhundredgliacells,butlittleis
v
knownabouttheirimportanceforchronobiologicalfunctions(Helfrich-Foerster
et al., 2007; Nitabach and Taghert, 2008). Immunostaining with antibodies
directed against clock proteins suggests that there is a wide range of species-
specific variation in the anatomical organization of the circadian network in
insects(e.g.,Helfrich-Forsteretal.,1998;Sehadovaetal.,2003;Zavodskaetal.,
2003).Forexample,inthehoneybee,boththePERandPigmentDispersingFactor
(PDF,apeptideinthecircadiansystemofinsects)-immunoreactiveclustersare
located in brain areas that have been implicated in the regulation of circadian
rhythmsinDrosophila,butcurrentlythereisnoevidenceforcellsexpressingboth
PERandPDFasinDrosophila(Blochetal.,2003;Sehadovaetal.,2004).
III. SOCIAL INFLUENCES ON CIRCADIAN RHYTHMS IN INSECTS
The social environment of insects consists of conspecific individuals at all life
stages(i.e.,eggs,larvae,pupae,andadults),whichtheymaycontactdirectlyor
indirectly by sensing cues and signals they release to the environment (such as
volatilepheromonesoracousticsignals).Suchsocialfactorsintheenvironment
mayinfluencethephase(entrainment),strength,expression,ordevelopmentof
circadianrhythms.
A. Social synchronization
Social synchronization, or “social entrainment” is the best studied social influ-
ence on the circadian clock. Social synchronization in animals experiencing
various social interactions (including courtship, aggression, and caging with
conspecifics) has been tested for diverse species and experimental protocols
(Table 1.1). These studies, mainly with mammals, suggest that animals differ
considerably in their entrainment by social time givers. Some species are
entrained well even by cues such as volatile odorants and sounds that do not
requiredirectcontact(e.g.,GoelandLee,1997;Levineetal.,2002;Rajaratnam
and Redman, 1999; Southwick and Moritz, 1987), while other species fail to
show social entrainment even after forceful social interactions such as overt
aggression or sexual experience (e.g., Gattermann and Weinandy, 1997;