!
1!
Nick!Edward!Dillon!
Colorado!State!University!
[email protected]
!
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The$Heredity$of$Behavior$in$Insects:$Divergent$Evolution$in$Action$
$
Abstract:$
This!review!will!examine!the!heredity!of!behavioral!traits!in!insects!and!how!the!
inheritance!of!behavioral!predispositions!may!lead!to!divergent!evolution.!Insects,!like!most!
organisms,!demonstrate!phenotypic!plasticity!as!a!result!of!gene!by!environment!(‘GxE’)!
interactions.!GxE!may!lead!to!speciation!through!reproductive!isolation!when!a!discontinuous!
distribution!of!phenotypes!results!(Campbell!&!Reece!2011).!In!several!species!of!insects,!the!
environment!experienced!by!a!progenitor!has!been!observed!to!influence!the!phenotype!of!
progeny!(Caillaud!&!Via!2012)(Rebar!&!Rodríguez!2015).!!Specifically,!how!might!phenotypic!
plasticity!as!a!result!of!genotype!x!environment!variation!lead!to!reproductive!isolation!and!
eventually!speciation!in!sympatric!populations!of!insects?!Evidence!that!extant!species!evolved!by!
such!phenomenon!is!examined.!!Finally,!I!propose!a!molecular!cladistics!analysis!of!the!species!
(and!potential!subspecies)!E.#binotata#as!a!followTup!experiment!to!further!support!the!likelihood!
that!inherited!behavioral!traits!contribute!to!genetic!divergence.!!
!
Introduction:$
!
There!exist!multiple!working!definitions!of!a!‘species’.!The!Morphospecies!Concept!(MC)!
hypothesis!largely!defines!species!based!on!common!physical!traits;!the!Phylogenetic!Species!
Concept!hypothesis!divides!life!into!‘monophyletic!units’!(or!genetically!isolated!groups!of!
organisms),!and!finally!the!Biological!Species!Concept!(BSC)!hypothesis,!the!legal!definition!of!a!
!
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species!under!the!United!States!Endangered!Species!Act,!defines!a!species!as!a!group!of!
reproductively!isolated!organisms!which!do!not!regularly!mate!with!nonTconspecifics!(and!
produce!infertile!offspring!if!they!do!so)(Herron!&!Freeman!2014).!For!the!purposes!of!this!
review,!I!will!be!operating!primarily!under!the!BSC!hypothesis!of!speciation,!although!all!three!
species!hypotheses!involve!the!limiting!of!gene!flow!between!species!and!thus!similar!implications!
when!examining!the!processes!of!speciation!(Herron!&!Freeman!2014).!The!reduction!of!gene!
exchange!between!populations!is!the!working!definition!of!isolation!under!the!BSC!hypothesis!
(Herron!&!Freeman!2014).!Genetic!isolation!is!important!to!consider!when!evaluating!systems!
were!speciation!might!be!in!action!or!may!have!already!occurred.!
!
Many!of!the!bestTstudied!cases!of!apparent!evolutionary!divergence!are!based!on!
geographical!mechanisms!of!isolation.!I!believe!this!is!simply!because!geographic!isolation!is!the!
most!obvious!mechanism!for!the!prevention!of!genetic!exchange,!however!any!factor!which!limits!
gene!flow!may!lead!to!speciation!(Herron!&!Freeman!2014).!Here,!potentially!isolating!behaviors!
in!insect!systems!are!discussed!and!evidence!for!prior!speciation!by!this!mechanism!is!evaluated.!I!
will!also!attempt!to!distinguish!genetically!heritable!behavior!from!simple!predispositions!to!
certain!behaviors!(such!as!a!sapTsucking!insect!having!a!genetic!preference!to!a!specific!host!plant!
versus!having!been!born!on!a!particular!host!plant!and!choosing!to!parasitize!it!as!a!matter!of!
convenience).!The!potential!role!of!behavior!in!other!mechanisms!of!isolation!and!speciation!is!
also!discussed.!When!appropriate,!the!‘molecular!evolutionary!clock’!(the!evaluation!of!nucleic!
acid!sequence!variation!as!a!predictor!of!time!in!evolutionary!divergence)!will!be!used!as!a!tool!for!
evaluating!patterns!of!divergence!in!the!genomes!of!these!various!insect!models!(Ho!2014).!
!
Insects!perform!relatively!complex!behaviors!as!the!cumulative!product!of!multiple!simple!
instinctual!behaviors!(such!as!taxis!toward!a!physical!stimulus).!Despite!their!apparent!simplicity,!
!
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the!cellular,!molecular!and!electrophysiological!mediators!of!insect!behaviors!are!highly!
conserved!between!many!orders!of!life,!including!humans.!Insects!are!good!model!organisms!for!
studying!evolution!due!to!their!short!generation!times!and!high!fecundity!(not!to!mention!the!ease!
of!keeping!them!in!a!lab).!Understanding!evolutionary!mechanisms!in!insects!will!not!only!shed!
light!on!to!the!evolution!of!the!species!we!share!the!planet!with,!but!also!our!own,!H.#sapiens.#
!
Discussion:$
Assumptions$for$Behavior>Based$Speciation$Hypotheses$
Snail#Chirality:#Genotypic#Determination#of#a#Behavior#Resulting#in#Isolation#
Japanese!land!snails!of!the!genus!Euhadra,!while!not!insects,!provide!an!obvious!example!of!
how!genetic!variation!at!a!single!locus!can!determine!an!animal’s!behavioral!phenotype!and!cause!
genetic!isolation.!Unlike!most!snail!species,!Euhadra#shells!come!in!two!chiral!polymorphisms!
(like!dexB!and!levoB!isomers!of!a!chemical,!or!your!left!and!right!hand)!and!the!direction!of!chirality!
is!determined!by!a!single!locus!(Davison!et!al.!2005).!Snails!of!opposite!chirality!can!only!mate!
with!extreme!difficulty!and!mating!attempts!usually!prove!futile!(Davison!et!al.!2005).!The!
implication!for!the!snail!is!that!sexual!behavior!is!largely!determined!by!this!locus!controlling!
chirality!(Davison!et!al.!2005).!Mitochondrial!DNA!analysis!indicates!that!his!discrepancy!in!
chirality!has!led!to!isolation!of!populations,!derived!from!a!common!ancestor,!which!are!
morphologically!unique!enough!to!categorize!as!separate!species!(Davison!et!al.!2005).!Gene!flow!
studies!of!the!species!in!Euhadra#confirm!genetic!isolation!(an!assumption!of!the!BSC!hypothesis)!
(Davison!et!al.!2005).!The!heritability!of!behavior!is!a!fundamental!assumption!of!behaviorT
mediated!speciation!hypotheses!and!this!example!is!strong!evidence!in!support!of!that!assumption!
(Herron!&!Freeman!2014).!However,!genetic!influence!on!behavior!is!almost!never!as!simple!as!
!
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chirality!and!sex!in!snails;!behavioral!traits!are!typically!multifactorial!and!thus!much!more!
complicated!to!study!(Campbell!&!Reece!2011).!
#
The$Implications$of$Host$Preference$in$Divergent$Evolution$of$Insects$
Assortative#Mating#
!
Many!species!of!insects!have!evolved!elaborate!‘mating!rituals’!for!recognition!of!
conspecifics!and!mediation!of!sexual!selection!(Campbell!&!Reece!2011).!Some!species!of!sapT
sucking!insects!involve!their!plant!hosts!in!their!mating!rituals!in!an!integral!manner!by!sending!
messages!through!the!plant!to!potential!mates!in!the!form!of!vibrations!(Cocroft!et!al.!2010).!The!
mating!signals!of!one!such!species,!the!treehopper!Enchenopa#binotata#have!been!studied!
exhaustively!(Cocroft!et!al.!2010)(Rebar!&!Rodríguez!2015).!This!species!is!found!throughout!
much!of!the!United!States,!but!the!phylogeny!of!E.#binotata!is!not!well!understood!(Rodriguez!et!al.!
2008).!Particular!E.#binotata!populations!have!a!preferred!host!plant!species,!but!host!plant!
preference!varies!depending!on!location!(often!because!the!range!in!which!E.#binotata#is!found!is!
wider!than!that!of!the!host!plant)!(Cocroft!et!al.!2010).!These!observations!indicated!to!the!
research!nucleus!of!Rodriguez,!Cocroft!and!Rebar!that!binotata#likely!had!colonized!novel!host!
plant!species!during!the!course!of!its!evolutionary!history!(yet!apparently!remains!a!tight!enough!
clade!for!different!populations!to!hybridize!and!produce!fertile!offspring;!the!definition!of!a!
species!under!the!BSC!hypothesis)!(Rodriguez!et!al.!2008).!To!examine!the!possibility!of!sexual!
selectionTmediated!phenotypic!divergence!in!binotata,!this!group!of!researchers!has!studied!
mating!signals!and!mate!preference!phenotypes!in!different!host!plantTspecific!populations!(Rebar!
&!Rodríguez!2015).##
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Vibrational!mating!signals!depend!both!on!the!activity!of!the!insect!and!the!physical!
characteristics!of!the!host!plant,!which!acts!as!a!medium!for!the!signal!(Rodriguez!et!al.!2008).!
Subtle!differences!in!mating!signal!variation,!such!as!frequency,!intensity!and!duration!have!been!
observed!across!populations!isolated!both!geographically!and!by!host!plant!specificity!(Cocroft!et!
al.!2010).!!The!selective!response!of!conspecifics!to!a!mating!signal!is!variable!and!depends!both!
on!the!activity!of!the!signal!caller!and!the!acoustic!properties!of!the!plant!(Rodriguez!et!al.!2008).!
Mating!signal!characteristics!and!preferences!have!been!shown!to!be!heritable!in!E.#
binotata!and!an!individual!insect’s!signaling!or!preference!traits!are!multifactorial!(Rebar!&!
Rodríguez!2015)!(Rodriguez!et!al.!2008).!Multifactorial!traits!are!determined!by!multiple!genes!
and!influenced!by!the!organism’s!environment!(Campbell!&!Reece!2011).!!Quantitative!trail!loci!
(QTL)!analysis!has!been!used!to!identify!genes!contributing!to!these!mating!behaviors!(Rebar!&!
Rodríguez!2015).!Interestingly,!but!not!surprisingly,!genes!that!determine!signal!qualities!are!
linked!to!genes!that!predispose!individuals!to!be!receptive!to!those!same!qualities!(these!sets!of!
QTLs!covary)!(Rebar!&!Rodríguez!2015).!This!is!not!an!isolated!phenomenon;!linkage!of!QTL!
genes!contributing!to!mating!signal!traits!in!the!Hawaiian!cricket!Laupala!appear!to!be!linked!with!
genes!for!preference!to!those!same!traits!(Wiley!et!al.!2012).!!
BehaviorTdriven!isolation!and!speciation!hypotheses!predict!more!variation!across!
populations!using!different!resources!in!the!same!geographic!area!than!variation!across!
populations!using!the!same!resources!in!different!areas!(Cocroft!et!al.!2010).!!This!is!precisely!
what!Cocroft!et!al.!(2010)!found!in!host!plant!specific!populations!of!E.#binotata.!At!a!given!local,!
binotata!mating!signals!(and!signal!preference)!vary!significantly!between!populations!using!
different!plant!species!as!hosts!and!there!exists!significantly!lesser!variation!between!
geographically!isolated!populations!of!the!same!host!plant!species!(Cocroft!et!al.!2010).!This!
!
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pattern!is!indicative!of!behaviorally!mediated!speciation!in!action:!phenotypes!within!a!species!
diverge!as!populations!become!genetically!isolated!via!behavioral!segregation.!
!
Parasitism#
Caillaud!and!Via!(2012)!assert!that!the!colonization!of!novel!hosts!is!a!major!contributor!to!
the!diversity!seen!in!parasitic!insects.!The!researchers!analyzed!two!different!‘races’!of!the!pea!
aphid!Acyrthosiphon#pisum!in!an!attempt!to!quantify!their!unique!feeding!behaviors!(each!endemic!
to!either!alfalfa!or!clover!plants)!(Caillaud!&!Via!2012).!These!aphid!‘races’,!while!technically!the!
same!species!under!the!BSC!hypothesis,!exhibit!distinct!divergence!in!feeding!behavior!dictated!
(but!not!determined!entirely)!by!genetic!variation!(Caillaud!&!Via!2012).!Feeding!preference!is!
thus!heritable!is!Acyrthosiphon#pisum#(Caillaud!&!Via!2012).!
Expansion!of!niche!by!the!colonization!of!a!new!host!species!is!not!unique!to!sapTsucking!
insects;!experiments!published!in!2009!by!Malenke!et!al.!shed!light!on!how!the!bird!louse!
Columbicola#macrourae!might!have!colonized!novel!host!species!in!the!recent!evolutionary!past!
and!is!currently!undergoing!a!speciation!event.!Mitochondrial!DNA!analysis!of!25!C.#macrourae#
from!either!WhiteTwinged!Doves!or!Mourning!Doves!(as!well!as!some!historical!samples)!was!
performed!and!five!distinct!haplotypes!were!identified!(Malenke!et!al.!2009).!Transplantation!of!
haplotype!lice!on!to!nonTnative!host!bird!species!resulted!in!a!significant!reduction!of!fitness!in!
both!lice!species!tested!(Malenke!et!al.!2009).!This!result!suggests!that!C.#macrourae!populations!
have!been!isolated!by!host!species!long!enough!for!populationTspecific!selection!to!occur,!
improving!the!fitness!of!each!population!on!their!respective!host!while!genetically!distancing!
them.!!
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Oviposition#
Gravid!plantTdwelling!insects!within!the!same!species!often!show!variable!host!plant!
preference!(Rodriguez!2008).!In!many!cases,!the!host!preference!of!a!mother!insect!is!correlated!
with!performance!in!the!larvae!(that!is,!larvae!perform!significantly!better!on!their!mother’s!
preferred!host!plant)!(Fox!1993).!This!trend!has!been!documented!in!aphids,!lice,!and!beetles!
(Caillaud!&!Via!2012)(Malenke!et!al.!2009)(Fox!1993).!
!
The#Role#of#Epigenetics#in#the#Heritability#of#Behavior#
!
The!emerging!field!of!epigenetics!implicates!another!way!in!which!behavioral!preferences!
may!be!inherited.!I!have!thus!far!examined!studies!in!which!behaviors!are!associated!with!QTL!loci!
and!inherited!with!the!nucleic!acid!sequences!passed!from!progenitor!to!offspring.!Epigenetic!
effects!involve!the!heritable!chemical!modification!of!genes!(such!as!methylation!of!DNA!or!
acetylation!of!histones)!that!may!occur!during!the!lifetime!of!a!progenitor!and!be!passed!on!to!
progeny!(Herron!&!Freeman!2014).!This!pattern!of!inheritance!has!significant!consequences!in!the!
models!previously!discussed;!the!implication!is!that!founders!of!insect!populations!on!new!hosts!
could!undergo!modification!of!their!DNA!during#the#life#of#the#insect!and!pass!on!those!characters!
to!offspring!(Yan!et!al.!2014).!This!process!could!act!as!a!potentiating!factor!of!host!
expansion/colonization!events,!although!specific!research!on!this!possibility!is!lacking.!
#
Positive#Feedback:#Reinforcement#of#Phenotypic#Divergence#
Flavinoids,!secondary!compounds!commonly!synthesized!by!plants,!appear!to!play!
important!roles!in!the!recognition!of!specific!host!plants!by!parasitic!species!and!gravid!insects!
(Simmonds!2000).!The!documented!effects!of!flavonoid!compounds!on!insects!are!numerous!and!
!
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often!act!by!complex!mechanisms,!but!there!are!two!main!ways!flavonoids!exert!their!effects!
(Simmonds!2000).!First,!a!flavonoid!compound!can!act!as!a!phagostimulant!or!antifeedant!in!a!
speciesTdependent!manner!(Simmonds!2000).!For!example,!the!flavonoid!rutin!stimulates!feeding!
behavior!in!locusts,!but!inhibits!the!growth!of!gypsy!moth!and!European!corn!borer!larvae!
(Simmonds!2000).!!Second,!gravid!insects!use!flavonoids!to!identify!their!preferred!hosts!
(Simmonds!2000).!It!is!not!hard!to!picture!how!unique!flavonoid!profiles!in!a!newly!colonized!host!
plant!species!could!contribute!to!the!isolation!of!a!new!population.!In!the!case!of!the!treehopper!E.#
binotata,#secondary!selection!pressures!from!flavonoids!in!new!host!plant!species!might!act!as!a!
positive!feedback!mechanism!further!facilitating!isolation.!
!
Future$Directions:$
The!aforementioned!research!group!led!by!Rodriguez!and!Cocroft!generally!operate!under!
the!same!research!question;!can!phenotypic!plasticity!as!a!result!of!genotype!x!environment!
variation!lead!to!reproductive!isolation!and!eventually!speciation!in!sympatric!populations!of!
parasitic!insects!(treehoppers!of!the!species!E.#binotata)!(Rodriguez!et!al.!2008;!Cocroft!et!al.!
2010)?!Specifically,!Rodriguez!et!al.!(2008)!tests!the!hypothesis;!‘colonizing!of!a!novel!
environment!may,!through!phenotypic!plasticity,!change!sexual!traits!in!a!way!that!could!alter!the!
dynamics!of!sexual!selection’.!Building!on!Rodriguez’s!work,!Cocroft!primarily!examines!the!
hypothesis!that!‘(mating)!signals!vary!between!populations!using!different!resources!to!a!larger!
extent!than!between!populations!using!the!same!resource!at!different!localities’!(Cocroft!et!al.!
2010).!Evidence!for!either!of!these!hypotheses!would!also!support!Cocroft!and!Rodriguez’s!
research!question!(indicating!that!yes,!a!species!can!show!phenotypic!plasticity!as!a!result!of!G!x!E!
interaction,!which!may!lead!to!speciation!through!reproductive!isolation).!!
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To!further!test!these!hypotheses,!I!propose!a!molecular!cladistics!analysis!of!the!species!in!
question.!Enchenopa#binotata,!which!inhabits!a!wide!range!across!the!Eastern!United!States,!has!
not!been!formally!described!(Cocroft!et!al.!2010).!Cocroft!et!al.!(2010)!simply!classify!subspecies!
based!on!which!plant!host!they!inhabit.!As!a!consequence!of!spatial!and!behavioral!segregation!
discussed!previously,!these!subspecies!infrequently!interbreed!although!they!are!physiologically!
capable!of!doing!so!(Cocroft!et!al.!2010).!!Populations!of!E.#binotata#certainly!experience!genetic!
isolation!to!one!extent!or!another,!yet!remain!phylogenetically!close!enough!so!that!they!may!still!
produce!fertile!offspring!in!the!infrequent!instances!in!which!populations!interbreed!(Cocroft!et!al.!
2010).!As!such,!this!is!an!excellent!candidate!species!for!the!study!of!divergent!evolution!in!action.!
These!subspecies!of!E.!binotata!have!already!adopted!mating!signals!that!are!unique!to!
populations!living!on!each!respective!plant!host!(Cocroft!et!al.!2010).!Assuming!Cocroft’s!
hypothesis!is!correct,!I!would!expect!these!subspecies!to!have!recently!diverged!from!a!common!
ancestor!and!for!the!population!associated!with!the!oldest!evolutionary!divergences!to!have!
accumulated!the!greatest!number!of!derived!nucleic!acid!sequences!(Campbell!&!Reese!2011).!I!
would!expect!subspecies!derived!from!the!oldest!evolutionary!(isolation)!events!to!have!
experienced!the!most!sexual!selection!pressure!on!matingTsignal!traits!exhibiting!G!x!E!variation!
and!as!such!the!least!amount!of!phenotypic!variation,!assuming!novel!directional!selection!for!the!
trait!(as!is!the!likely!the!case!when!an!insect!species!colonizes!a!novel!host!plant!when!expanding!
its!range).!I!hypothesize!that!variance!in!mating!signals!within!a!subspecies!is!positively!
correlated!with!time!since!colonization!of!a!novel!host!plant!(which!in!our!cladistics!analysis!is!the!
point!at!which!the!subspecies!became!genetically!isolated!from!a!common!ancestor).!Specifically,!
if!the!answer!to!Rodriguez!and!Cocroft’s!research!question!is!‘yes’,!and!divergent!mating!signal!
!
10!
phenotypes!do!lead!to!speciation!in!treehoppers,!I!would!expect!the!number!of!novel!mutations!to!
be!correlated!with!mating!characteristics!observed!by!Cocroft!et!al.!2010.!
!
To!perform!a!molecular!cladistics!analysis,!I!would!first!sequence!the!genomes!of!each!
subspecies.!Novel!sequences!may!be!identified!using!a!computer!program!and!potential!
subspecies!may!be!ordered!by!‘time!since!host!plant!colonization’!and!evaluated!for!genetic!inT
groups/outTgroups,!which!may!indicate!that!a!subspecies!had!at!one!time!inhabited!a!different!
host!plant!(Campbell!&!Reese!2011).!By!assessing!the!number!of!random!mutations!in!nucleic!acid!
sequences!shared!amongst!subspecies,!we!may!infer!the!time!since!divergence!from!a!common!
ancestor!(which!we!are!defining!here!as!‘time!since!host!plant!colonization’,!according!to!Cocroft’s!
definition!of!these!subspecies)!(Ho!2014).!We!may!infer!taxonomical!proximity!of!these!E.!
binotata!subspecies!to!each!other!on!a!cladistics!map!by!identifying!combinations!of!derived!
(novel)!sequences!between!subspecies!(Campbell!&!Reese!2011).!A!statistical!analysis!examining!
the!correlation!between!‘time!since!host!plant!colonization’!and!variation!in!mating!signal!
behavior!may!provide!evidence!for,!but!not!prove,!Cocroft’s!hypothesis!that!‘differences!in!
resource!use!contribute!to!the!evolution!of!reproductive!isolation!by!altering!the!nature!of!sexual!
selection’!(Cocroft!2010).!!
!
If!Rodriguez!and!Cocroft’s!hypotheses!are!true!and!their!calculations!valid,!there!are!likely!
implications!for!the!treehoppers!in!these!studies.!Rodriguez!concludes!in!his!study!that!GxE!
influence!on!existing!phenotypes!on!new!hosts!can!cause!mating!signals!to!diverge!within!the!
same!species!inhabiting!different!host!plants!and!that!is!almost!certainly!what!is!happening!in!this!
species!of!treehoppers!(Rodriguez!et!al.!2008).!Populations!within!this!species!have!become!
behaviorally!and!phenotypically!isolated!via!host!preference!(Cocroft!et!al.!2010).!!Because!
speciation!may!occur!due!to!reproductive!isolation!and!these!subspecies!rarely!interbreed,!these!
!
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treehoppers!are!likely!undergoing!an!evolutionary!splitting!event.!!Evidence!for!this!assertion!
would!also!support!the!Rodriguez!and!Cocroft!hypotheses.!A!cladistics!mapping!result!in!support!
of!these!hypotheses!would!indicate!speciation!in!action.!!
!
!
References:$
!
Caillaud,!M.!C.,!and!S.!Via.!"Quantitative!genetics!of!feeding!behavior!in!two!!
!
ecological!races!of!the!pea!aphid,!Acyrthosiphon!pisum."!Heredity!108,!no.!3!!
!
(2012):!211T218.!
!
Campbell,!Neil!A.,!and!Jane!B.!Reece.!"Phylogeny!and!the!Tree!of!Life."!Biology.!9th!!
!
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