Evolutionary Biology of Harvestmen (Arachnida, Opiliones)

23 Pages·2015·3.21 MB·English

EN60CH09-Giribet ARI 27November2014 14:47
Evolutionary Biology of
Harvestmen (Arachnida,
Opiliones)
g
s.or Gonzalo Giribet1,∗ and Prashant P. Sharma2
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evi 1MuseumofComparativeZoology,DepartmentofOrganismicandEvolutionaryBiology,
alr HarvardUniversity,Cambridge,Massachusetts02138;email:[email protected]
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2015.60:zalo Giri Annu.Rev.Entomol.2015.60:157–75 Keywords
mol. Gon FOicrtsotbpeurb9li,sh2e0d14onlineasaReviewinAdvanceon daddylong-legs,evo-devo,biogeography,phylogeny,paleontology
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Ent b TheAnnualReviewofEntomologyisonlineat Abstract
v. ento.annualreviews.org
e Opilionesareoneofthelargestarachnidorders,withmorethan6,500species
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u. Thisarticle’sdoi: in50families.Manyofthesefamilieshavebeenerectedorreorganizedin
Ann 10.1146/annurev-ento-010814-021028 the last few years since the publication of The Biology of Opiliones. Recent
Copyright(cid:2)c 2015byAnnualReviews. years have also seen an explosion in phylogenetic work on Opiliones, as
Allrightsreserved
well as in studies using Opiliones as test cases to address biogeographic
∗Correspondingauthor andevolutionaryquestionsmorebroadly.Acceleratedactivityinthestudy
ofOpilionesevolutionhasbeenfacilitatedbythediscoveryofseveralkey
fossils,includingtheoldestknownOpilionesfossil,whichrepresentsanew,
extinctsuborder.Studyofthegroup’sbiologyhasalsobenefitedfromrapid
accrual of genomic resources, particularly with respect to transcriptomes
andfunctionalgenetictools.TherapidemergenceandutilityofPhalangium
opilioasamodelforevolutionarydevelopmentalbiologyofarthropodsserve
asdemonstrativeevidenceofanewareaofstudyinOpilionesbiology,made
possiblethroughtranscriptomicdata.
157
EN60CH09-Giribet ARI 27November2014 14:47
INTRODUCTION
Opiliones (harvestmen or daddy long-legs) are the third-largest order of arachnids, after Acari
(mitesandticks)andAraneae(spiders).Theorderencompassesmorethan6,500describedextant
species in about 1,500 genera, 50 families, and four suborders (58), with an additional extinct
suborderrecentlydescribed(36)(Figure1).Harvestmenconstituteanimportantcomponentof
manyterrestrialecosystems,especiallyinthesoil,wheretheyarescavengersorpredatorsofsmall
arthropodsandworms,butalsoonshrubsandtrees.Severalharvestmanspeciesarewellknown
inruralareasaroundtheworld,especiallyintemperateandtropicalclimates.Fossilharvestmen
firstappearintheDevonianRhyniecherts(ca.405Ma)(28),makingOpilionesoneoftheoldest
terrestrialanimalgroups.TheorderhadalreadydiversifiedbytheCarboniferous(Montceau-les-
Minesfossilsfromca.310Ma)(35,36).
Broad interest in harvestman phylogenetic relationships and biogeographic history has ad-
vancedthefieldofopilionologygreatly.Theadventoftranscriptomicdataforallmajorlineages
g
or ofOpilioneshasprecipitatedtheinclusionofharvestmenasmodelsforevolutionarydevelopmen-
s.
w talbiology(evo-devo)(94,95,97),onlycomparablewiththebetter-studiedspidersamongthe
e
vi arachnidorders.Someharvestmangroupsarealsomodelsystemsforbehavioralecology,andmore
e
alr specificallyreproductivebehavior,astheyexhibitbothindirectanddirectspermtransfer,andmul-
ww.annuuse only. tinipvleesltimneeangteisnhsaovmeedesvpeelcoiepsed(1p1a,r6e1n,ta6l2c,a1r2e2,w,1it2h5)b.oTthhemyattherunsacloannsdtiptuatteerannalu,napnadreavlleenlebdipgaroreunptaolf,
m wnal terrestrialarthropodsintermsofintegratinganatomical,behavioral,biogeographic,ecological,
nloaded fro5. For perso datrceicvguegmleorupelmdatefeundrttauhl,netrpialinl2eto0e0nre6tostwloiangsicOcaolp,milaipnoindleedps.hiDynloeavgelealnonepdtmmiceaknrnktsobwsoilnoecdkegoe2n.00Ihn6adrievneedtsht,memaaunrcehbasiooolfoftgphyhey(k7lon3go),ewnwleehtdiiccgshe,
w1 genomics,andevo-devoaresubstantialandconstitutethefociofthisreview.
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175. n 01/
57-et o
1b SYSTEMATICSANDEVOLUTIONARYHISTORY
2015.60:zalo Giri OpilionesandArachnidPhylogeny
mol. Gon ThepositionofOpilionesinthearachnidtreeoflifehasbeenhotlydebatedoverthelastdecades.
v. Ento by TSchoerpmioonsetsr,efcoernmticnlgadtihsteicclaandaelySsetosmofotmheocrapthao(l1o0g6ic)a.lPdraiotarsmuoggrpehstoalosgiisctaelr-wgororkupharedlastuiogngeshstiepdtoa
Re sister-group relationship to a clade composed of Scorpiones, Pseudoscorpiones, and Solifugae
u. (41,104,121),constitutingthetaxonDromopoda,ortoacladecomposedofRicinuleiandAcari
n
n
A (120),tomentionjustmoderncladisticstudies,butmanyotherhypotheseshavebeenpublished
(reviewedin121).Molecularsequencedataforarachnidshavebeeninplayfortwodecades,but
theyhavenotsatisfactorilyresolvedthepositionofOpilionesinthearachnidtreeoflife(41,67,
121),evenwhenusingupto62protein-encodinggenestoinfertheirphylogeneticposition(76,
77).Thefewcombinedanalysesofmoleculesandmorphology(41,121)largelyagreewiththe
morphologicaldatasetstheyencompass.
Morerecently,systematistshavestartedusingexpressedsequencetags(ESTs)andtranscrip-
tomestoelucidatephylogeneticrelationshipsamonganimals(31),includingarachnids(92).This
latterstudyre-examinedarachnidrelationshipsbasedonalargedatasetofupto3,644lociand
identifiedpossiblesourcesofconflictinresolvingthearachnidtree.Amongtheseareaccelerated
evolutionary rates in certain lineages (e.g., a diphyletic Acari, Pseudoscorpiones); so, when the
fastestgeneswereexcluded,amoreplausiblesetofrelationshipswasrecovered,includingaclade
composedofOpiliones,Ricinulei,andSolifugae,whereasScorpioneswerethesistergrouptothe
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Figure1
ExemplarsofmajorOpilioneslineages:(a)3-DreconstructionofHastocularisargus(Tetrophthalmi),fromtheCarboniferous,(b)Aoraki
longitarsa(Cyphophthalmi,Pettalidae),(c)Acropsopilioneozealandiae(Dyspnoi,Acropsopilionoidea,Acropsopilionidae),(d)Taracussp.
(Dyspnoi,Ischyropsalidoidea,Taracidae),(e)Anelasmocephaluscalcaneatus(Dyspnoi,Troguloidea,Trogulidae),(f)Forsteropsalispureora
(Eupnoi,Phalangioidea,Neopilionidae),(g)Calugan.sp.(Eupnoi,Phalangioidea,Sclerosomatidae),(h)Triregiafairburnigrata
(Laniatores,Triaenonychoidea,Triaenonychidae),(i)Protimesiuslongipalpis(Laniatores,Stygnidae),(j)Phareicranausmanauara
(Laniatores,Gonyleptoidea,Gonyleptidae),and(k)Fissiphalliusmartensi(Laniatores,Zalmoxoidea,Fissiphalliidae).
www.annualreviews.org • Harvestmen(Arachnida,Opiliones) 159
EN60CH09-Giribet ARI 27November2014 14:47
other orders with book lungs (Tetrapulmonata, which include spiders and their allies). To our
knowledge,nopriorphylogenyhadsupportedthisparticularpositionofOpiliones,andonlya
handfulofstudiesproposedasimilarclade,buttheyincludedAcari(124)orAcari,Palpigradi,and
Pseudoscorpiones(33).
TheputativecladecomprisingOpiliones,Ricinulei,andSolifugaeissupportedbythepresence
ofhighlybranchingtracheae,astheseorganismsareamongthelargestmembersoftherejected
cladeApulmonata(arachnidsthatlackbooklungs).However,thishypothesisoftrachealhomology
doesnotfollowthosepreviouslysuggested,andtherespiratorysystemofRicinuleiisparticularly
poorly understood (33, 106). Other major characters used in arachnid phylogeny, such as the
numberofcheliceralsegments(seediscussionbelow),aredemonstrablylabile.Thesethreeorders
transferspermoraspermatophoredirectlyintothefemale’sgenitalopening,withoutplacingit
ontheground—withlegIIIinRicinulei(60),withthecheliceraeinSolifugae(75),orthrough
directcontactinthebasalOpilionessuborderCyphophthalmi(85)—butthisbehaviorhasbeen
g modifiedinPhalangida,whichcopulate.Morphologicalandbehavioralevidenceforthiscladeis
or
s. thereforelimited,andthisrelationshiprequiresfurthertesting.
w
e
vi
e
w.annualre only. OHaprivleiostnmeasnSpyhsytloegmenaytihcassarencdeiPveadleboronatdoaltotegnytioninpastdecades(e.g.,7,41,43,46,50,64–66,
d from wwpersonal us 8do8ifs,Oc1op0vie5lir,oy1no0e7fs)n(,3ea6wn),dCaaanrdcboponhnsyieflneorsgoueusnsiesftoifcossraimnlsaihnlyagssiossnuogfsgluaebrsogteerddmitnhoaelleercexulilasattreiondnacstehaoispfesats(fiFhfiatghsuraraneddi2cea)x.lltHyinrocewtoserugvbeaorn,rizdtheeder
nloade5. For fraemoriglya-nleizvaetliorenlaotfioDnyshspipnsoainadndcoEmupponsoiitiwonas,ersepceecnitallylyporofpLoasneidat(o4r9e)s.(72,88,93).Likewise,amajor
w1
Do11/ The suborder Cyphophthalmi comprises three infraorders and six families whose interrela-
175. n 01/ tionshipshavebeenbroadlystudiedusingmorphology,molecules,orboth(7,39,43,101).Major
57-et o cladesarereadilyrecognizableintermsofanatomicalsynapomorphies,suchassternalopistho-
2015.60:1zalo Girib s((eWonmdeaesltmAgilcfarnticodasNadneedwfitnChineaglNedtehooentiraco)lpa,diOcesg)S.oItvenertinedroanepah(lrtrheesaltlarmtiiciot,enwdshhtiiopcshtraoinnpdciclbuaidloeWgseoethsgteraAfpafhrmiiccialip)e,asattnTedrrnoNsgeoloofsgtihrooevneciioddnaaee-
mol. Gon stituentfamilieshavereceivedconsiderableattention:Neogoveidae(5),Pettalidae(8,9,21,22,
v. Ento by 3si8n)c,eStihroentuidraneo(f2t3h,e4t4w,e7n0t)y,-Sfitrysltocceenlltiudrayei(n1c3l–u1d6e)d,easncdriTptrioognloofsi7r2onoifdtahee(18867).kMnoawjonrecoxtnatnrtibsupteicoiness
Re (38.5%).
u. ThesuborderEupnoiisdividedintothesuperfamiliesCaddoidea(2species)andPhalangioidea
n
An (∼1,800species),thelatterincludingfourill-definedfamilies(Neopilionidae,Phalangiidae,Pro-
tolophidae, and Sclerosomatidae), plus the Metopilio group; all are in urgent need of revision.
Caddoideainclude2speciesinthefamilyCaddidae,butuntilrecentlytheyalsoincludedAcrop-
sopilionidae,mostlyfoundinthesouthernhemisphere(asthesubfamilyAcropsopilioninae)(100)
andnowtransferredtoDyspnoi(49).Anothersouthernclade,Hesperopilio,waslateraddedtoCad-
didae (102) but is now placed within Phalangioidea (49). The families and relationships within
Phalangioidea have been only partially addressed in some recent studies (46, 49, 51, 54, 112),
andonlyonestudyhasprovidedasomewhatbroadanalysisofthesuperfamily,albeitfocusingon
Sclerosomatidae from East Asia and North America (51) and demonstrating nonmonophyly of
traditionalsubfamilies.PhylogeneticrelationshipsandhighertaxonomyofPhalangioidearemain
theleast-understoodaspectsofOpilionessystematics.
ResolvingthephylogeneticrelationshipsofthesuborderDyspnoihasbeenafocusofattention
in the last decade as well (46, 49, 82). A major emendation to the systematics of the suborder
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160 Giribet Sharma
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Pettalidae I.o. Scopulophthalmi
S.o. CYPHOPHTHALMI
Troglosironidae
Ogoveidae I.o. Sternophthalmi
Neogoveidae
Sironidae
I.o. Boreophthalmi
Stylocellidae
Acropsopilionidae S.f. Acropsopilionoidea
S.o. DYSPNOI
Ischyropsalididae
Sabaconidae S.f. Ischyropsalidoidea
Taracidae
Nipponopsalididae
PALPATORES
Nemastomatidae
S.f. Troguloidea
Trogulidae
Dicranolasmatidae
Caddidae S.f. Caddoidea
g Neopilionidae
or
s. Phalangiidae
ew S.o. EUPNOI Protolophidae S.f. Phalangioidea
vi
ww.annualreuse only. PHALANGIDA S.o. Insidiatores MTSScyreilnaetteorhonpesioltoinoomyn gcayrhctoiihdduiapaideeae S.f. “Triaenonychoidea”
m wnal Sclerobunidae
d froperso S.o. LANIATORES TCrlaadvuonniyidchaeiidae* S.f. Travunioidea
nloade5. For BPhriaglgasnigdoaedidae S.f. Phalangodoidea
ow1/1 Sandokanidae
175. Dn 01/1 GRASSATORES EPpeterdoabnuindiadeae S.f. Epedanoidea
57-et o Podoctidae
2015.60:1zalo Girib TAStigtyhogarniesoitdpeanseiiddaaee
omol. y Gon STtryicgonmidmaeatidae S.f. Gonyleptoidea
Ent b Gerdesiidae
v. Cosmetidae
Re Metasarcidae
u. Gonyleptidae
n
An Pyramidopidae
S.f. Assamioidea
Assamiidae
Biantidae
Stygnommatidae* S.f. Samooidea
Samoidae
Escadabiidae
Guasiniidae
Kimulidae
S.f. Zalmoxoidea
Icaleptidae
Fissiphalliidae
Zalmoxidae
Figure2
SummarytreeofthephylogeneticrelationshipsoftheextantOpilionesfamilies.Abbreviations:I.o.,infraorder;S.f.,superfamily;S.o.,
suborder.Unrankedcladesareindicatedtofacilitatediscourse.Asterisksindicatepossibleparaphyleticgroups.
www.annualreviews.org • Harvestmen(Arachnida,Opiliones) 161
EN60CH09-Giribet ARI 27November2014 14:47
consistedoftheidentificationofAcropsopilionidaeasthesistergrouptotheremainingDyspnoi
(49).Thesuborderpresentlyincludes305describedspeciesinthreesuperfamilies:Acropsopil-
ionoidea (19 species in the single family Acropsopilionidae; 49), Ischyropsalidoidea (76 species
inthefamiliesIschyropsalididae,Sabaconidae,andTaracidae;82),andTroguloidea(210species
in the families Dicranolasmatidae, Nemastomatidae, Nipponopsalididae, and Trogulidae; 82).
RelationshipswithinIschyropsalidoideaarenowwellestablisheddespiteseveralrecentfamilial
reassignments(46,83).ThenewfamilyTaracidaewasestablishedforCrosbycus,Hesperonemastoma,
andTaracusinaccordancewiththephylogenyofthesegenera,whereasCeratolasmawastransferred
toIschyropsalididaeandthefamilyCeratolasmatidaewasdismantled(82).WithinTroguloidea,
the sister-group relationship of Trogulidae and Dicranolasmatidae is well established, but the
relativepositionsofNipponopsalididaeandNemastomatidaearelessclear(46,83,107).
RelationshipsandfamiliesofLaniatores(4,138species;59)havechangeddrasticallysince2007
(73),asmultiplelarge-scaleanalysesofLaniatores(12,46,72,88,89)havemodifiedourunder-
g standing of the suborder with reference to the unpublished thesis of A.B. Kury (57). Recently
or
s. Kury(59)continuedtodivideLaniatoresintotwoinfraorders,Insidiatores(568species;59)and
w
vie Grassatores(3,570species;59),theformerwiththesuperfamiliesTravunioideaandTriaenony-
e
alr choidea,andthelatterdividedintoAssamioidea,Epedanoidea,Gonyleptoidea,Phalangodoidea,
w.annue only. SphamyloyooidfeIan,siadnidatoZraelsm,oasxoSiydnetah.eHtoonwyecvheiird,apeh,yalofgamenielyticenadneamlyiscistoofNmeowleZcuelaalrandda,taapspuegagreesdtsapsatrhae-
d from wwpersonal us sfwoisirttheIrnTgsirrdaoivuautpnotrioiedsaalfelroaontmhdeaernlLeuvaanntpiianutgbolrtihessheietnrditatwehoneosrienscy(ec6nh8ti)d,stisunudcbilfeuasdm(i4ni6lgi,ef8su8Ns)i.nipSgpimBonrilioagrnglysyic,dhKaienuraayenfadonCldlolPawdasroaannpyorconhpyiicodhsaaie-l
nloade5. For nonaeItnosifdaimatiolireess,atrsaanwsfherorlien.gthelattertwotoTravunioidea.Littlephylogeneticworkhasfocused
w1
Do11/ Within Grassatores, the largest clade of Opiliones, the first taxonomic change since 2007
175. n 01/ was a replacement name for Oncopodidae, now Sandokanidae (71). Additionally, phylogenetic
57-et o workhasresultedinothertaxonomicchanges.Sharma&Giribet(88)proposedthenewfamilies
2015.60:1zalo Girib Pdanae-dtRropobrcouhvnaiideditanaegla.n(n7ed2wT)ffioatmchuaiselyeiddsatoean,tuatnshdetosSpMheaceritmeassa-arerictchiadlG.ae(o9bn3u)ytlfeodpromtowaindligezarea,ddretihnstegofrMainmagnilTayorPsicbyoriiamdmameidaaotnipddiadCeatero.aPnfaaimnidtioalye-
mol. Gon tosubfamiliesofGonyleptidae.ThesystemproposedbyKurymostlyfollowsthephylogenetic
v. Ento by pmraoipnotasianlsbEyscSahdaarbmiiada&eaGndiriKbeimtu(8li8d)a,ewwitihthtihneSaemxcoeopitdioena(o5f9)Z,aallmthooxuogihdethaeasnedtwSoamfaomoiildieesaa;pKpuerayr
Re inZalmoxoidea,closelyrelatedtoGuasiniidae,inphylogeneticanalyses(88,89).Thecrypticfamily
u. SandokanidaeistentativelyregardedasamemberofthesuperfamilyEpedanoidea,althoughits
n
n
A phylogeneticplacementremainssensitivetoalgorithmicapproach(46,58,88).
The fossil record of Opiliones is relatively rich and well preserved, with several Paleozoic
representatives(27).Modern-lookingmembersofthesubordersEupnoiandDyspnoiarealready
presentintheCarboniferous(35).TheoldestOpilionesfossil,Eophalangiumsheari,isfromthe
DevonianRhyniechertsandwaspreviouslyplacedinEupnoi(28,29).Thisfossilhasbeenusedin
moleculardatingtoconstraintheageofEupnoi(46)orPalpatores(50),basedoninterpretation
ofparticularcharacters.TherecentdiscoveryofanewOpilionesbodyplanintheCarboniferous
Montceau-les-Mines(36)(Figure1a)andofthesister-grouprelationshiptotheDevonianEopha-
langiumnecessitatedreevaluationoftheharvestmandatedphylogeny(36),specificallybecauseof
theunexpectedplacementofthisfossilcladeassistergrouptoCyphophthalmi,notEupnoior
Palpatores.Nodedatingofa279-taxondatasetinthatstudysuggestedaverydifferentscenario,
withCarboniferousdiversificationinallfoursuborders(36).
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EN60CH09-Giribet ARI 27November2014 14:47
TheMesozoicrecordofOpilionesnowincludesMiddleJurassicEupnoi(inthefamilyScle-
rosomatidae)fromChina(45,52),inadditiontoCretaceousCyphophthalmiandDyspnoi(40,
74) and a poorly understood Lower Carboniferous species (56). All major lineages are already
representedinCenozoicamberdeposits,especiallyDominican,Baltic,andBitterfeldamber,orin
themudstonesandshalesfromtheFlorissantformationintheUnitedStates(26,27,30).Thisrich
fossilrecord,accompaniedbyasolidphylogeneticbackgroundbasedoncombinedmorphological
andmoleculardata,contributestoanunparalleledtestcaseforstudyingdiversificationofancient
lineagesofterrestrialarthropods(90).
DiversificationandBiogeography
Opilioneshavebeenconsideredextraordinarymodelsystemsforthestudyofhistoricalbiogeog-
raphybecauseoftheirevolutionaryoldage(27)andlimiteddispersalabilities(42).Themajority
g ofOpilionesspeciesexhibitnarrowdistributions,andcasesoftype-localityendemismarecom-
or
s. moninthegroup.Thesecharacteristics,togetherwiththeprofusionofmorphologicaldiversity
w
vie inharvestmen,facilitatetheidentificationofconstituentspeciesandutilityofmanyharvestman
e
alr lineagesforbiogeographicstudy.
w.annue only. harBveystfmarenth.eTbheesstm-uanldleesrtsstuoboodrdlienreoagfehairnvethstims erengiasrrdenisowCnyepdhofoprhetxhcaelmptii,onoarltfihdeeslioty-coafllpehdymloigtee--
d from wwpersonal us nittheientigdcfirsoecrlomavtieeorrnlyysohcfoipsnestvitgeourgaoeluoksgetyrearfproahsniscielsdhoiasftrtrvhiebesutstmuiopenenr,cswoinintchteina2lel0nc0ty7spG(h3oo5np,dh3wt6h,aa4nl5ma,ai5nd2df,aL7ma4iu)l,rieaessffieoaxr(ct7ls,u1tso6iv,de7al0yte)i.nOWhpaiibtlh--
nloade5. For isopnoensdpehnycelobgeetnwyeewnitdhivreerlagxeendc-ectliomckesaopfptraoxaacahnedsehsatvimearetevdeaalgeedsaonfluannpdrmeacsesdfernatgemdednetgarteioeno(f3c6o,r4r3e)-.
w1
Do11/ IllustrativeofthispatternareseveralgeneraofthefamilyPettalidaethatareendemictoNew
175. n 01/ Zealand and whose distributions and clade ages bear directly on the debate over the character
57-et o of the New Zealand biota, namely, whether this biota retains relicts of Gondwana or whether
2015.60:1zalo Girib ittthhaecloommldipewrsiitstmhesoosntoholeeprlhysyuplecohtsitce-gnOrdloeiugmopicsceinncleNadceeowsloiZnneitsahtlsiasn(8adr,ca9hn,idp2te1hl)ae.gCoonohlmyaskpnashroiowsownnnaonthfimaNtaetlhwgerZopueepattlsaatnlhiddatgCreeyntpeahrinoaptahhree-
mol. Gon signatureofZealandia’sfragmentationfromAustraliaintheCretaceous(98).Thecontingency
v. Ento by obfydmisotrdieblu-btiaosnedonangaeloylsoegsiocfpdriovceersssiefiscaintiopnoorraltyesd.isFpoerrseixnagmhpalrev,easctmceelenrahtaisonbeoefndfiuvretrhseifircealtuicoindartaetde
Re inthegenusCyphophthalmusiscorrelatedwiththetimingofthecollisionoftwoMediterranean
u. microplatesintheEocene(70).Similarly,shortinternodesatthebaseofthephylogenyofSty-
n
n
A locellidae,theoldestknowncladeinmanyfragmentislandsofWallaceaandSundaland(14,16,
110),coincidewithaperiodofgeologicdynamismandmarkedsealeveloscillationsinSoutheast
Asia(16).
Thecorrespondencebetweengeologicalterranesandphylogeneticrelationshipsisalsostrongly
observedinthesuborderLaniatores.Inparticular,superfamilieswithintheinfraorderGrassatores
arefrequentlycontainedwithintraditionalzoogeographicprovinces,suchastheNeotropics(e.g.,
Gonyleptoideaanditssistergroup,Stygnopsidae)andtheAfrotropics(e.g.,Assamioidea),andone
superfamilyspansbothofthese(Samooidea)(42,48).WithintheNeotropics,muchbiogeographic
efforthasfocusedontheuseofsubfamiliesofGonyleptidaetodefineareasofendemism,with
emphasisonendemicsoftheBrazilianAtlanticRainforest(e.g.,20,123).Relatedapproachesin
SoutheastAsiahaveinvestigatedtheinfluenceofgeologyondiversificationinpoorlydispersing
Laniatores,suchasSandokanidae,inconcertwithmolecularphylogenies,butlimitationspersist
www.annualreviews.org • Harvestmen(Arachnida,Opiliones) 163
EN60CH09-Giribet ARI 27November2014 14:47
in taxonomic sampling of small and cryptic species in this geographically complex region (87).
The comparative lack of knowledge of Southeast Asian opiliofauna is highlighted by the 2011
discoveryofanewLaniatoresfamilythatincludessomeofthesmallestmembers(1–2mm)ofthe
suborder(88).
NumerousharvestmanlineageswithSouthernHemispheredistributionssuggestiveofvicari-
ancemayconstituteopportunetargetsforfuturestudyofhistoricalbiogeographyusingmulti-
locusphylogeniesandfossil-calibratedmoleculardating;suchlineagesincludeTriaenonychidae
(excludingFumontanadeprehendor;69),Neopilionidae(49,54,112),andAcropsopilionidae(49).
Nevertheless,earliercharacterizationsofOpilionesasgenerallypoordispersersanddefactoex-
cellentmodelsforstudyofhistoricalbiogeographyareatoddswithcasestudiesofdispersalamong
harvestmen.OneofthemostextremecasesisthesuperfamilyZalmoxoidea,whichoccursinthe
Neotropics,saveforasinglenestedAustralasiancladewithhighdispersalcapabilities(42).Inthis
case,phylogeneticrelationshipsofZalmoxoidea,togetherwithmoleculardatingandmodel-based
g reconstructionsofancestralranges,supportcolonizationofAustralasiaviatransoceanicdisper-
or
s. saloutoftheNeotropics(89).Thispatternconstitutesanuncommonbiogeographicsignalthat
w
vie contrastswiththestronglyPaleotropicalcharacterofAustralasianarthropodfaunas(37).Other
e
alr groups of temperate harvestmen, such as Sironidae, Caddidae, and Sabaconidae, exhibit classic
w.annue only. Hforolsaarbcatcicodniisdtsri(b8u3t)ioannsd,bcaudtdinidtesr(c1o0n8t)i.nAenntoatlhdeirspneortsaabllaeceroxcsseplatniodnbtroidtgheeslhoawsbveageniliitnyfeorfrOedpailtiolenaesst
d from wwpersonal us i(s18thG,e3i4vge,en4n7ut,hs1eA0ic3nr,ocpi1ds0oe9pni,lci1eo1,o1kf)n,eoaxwlttrnheomfruoegmhopiCtpsohmsilietoe,nNboipeohwgyeZloyegrarelaampnhadii,cnVssiuegnnnetaezlssuteienldat,phNheyoglrortoghueApn—metietcrhaiecllayc,o.anngdruJaepnacne
nloade5. For oPfacCifiypchdoispphetrhsaallminiZphalymloogxeonidyeaan—dtdhievecrhgaernaccetetriimzaetsiownitohfcOopnitliinoennetsaalsdarimfto,jduexltsaypsotesemdfworitshtutrdaynos-f
w1
Do11/ vicariancebiogeographyrequiresgreaterscrutinyandpossiblycallsformethodicalevaluationof
175. n 01/ family-levelgroupsonacase-by-casebasis,especiallywithinPhalangioidea.Althoughdiversifica-
57-et o tiondrivenbygeologicprocessesmaybethepredominantexplanatoryhypothesisforharvestman
2015.60:1zalo Girib ddthiissetjurLinbacunttiaidotionstrsre,istbhfuaetmiporinleisevsa(elPe.gno.cd,eoAcoctfridodapisespoaepnrisdlaiolSnraeimdmaoaeiid;na4se9t;)o8a8bn,ed8in9s)pv.eesctiiegsateendd,epmarictictoulaorcleyafnoircliisnleaangdess(we.igth.,
mol. Gon
oy
Ent b GENOMICSANDTRANSCRIPTOMICS
v.
Re Untilrecently,fewgenomicresourcesexistedforOpiliones,causingmajorgapsinknowledgeof
u. harvestmangenetics.AbodyofliteraturehasaddressedcytogeneticsofOpiliones(118),including
n
n
A observationofchromosomenumbersinhybridzones(48)andcorrespondencewithgeography
(119). Population genetics of harvestmen remains in its infancy, with exclusive application to
phylogeography(6,32,116).Beyonddescriptiveapproaches,littleexperimentalgeneticworkhas
beenconductedonthegroup.
TranscriptomicresourcesforOpilioneshavegrownsteadilyinthelastfewyears.Presently,
transcriptomes are available for 14 species in all major clades (50, 79, 92). The first published
harvestman transcriptome was that of the cyphophthalmid Metasiro americanus (79), sequenced
using Illumina short-read technology. This species and its transcriptome were instrumental in
demonstratingtheincidenceofparalogyingenescommonlyregardedassingle-copyorthologs
andfrequentlyusedinSanger-basedphylogenetics.Specifically,twoormorecopiesofhousekeep-
inggenessuchasthoseencodingmethionineadenosyltransferaseandelongationfactor-1αwere
demonstrated to occur in M. americanus, with immediate implications for phylogenetic studies
(17).
·
164 Giribet Sharma
EN60CH09-Giribet ARI 27November2014 14:47
AhandfuloftranscriptomeswassubsequentlyusedtoassesssubordinalrelationshipsinOpil-
iones(50,92),recoveringunambiguoussupportforthetraditionalrelationshipof(Cyphophthalmi,
(Laniatores,(Eupnoi+Dyspnoi))).However,thesamplingofallfoursuborderstodateomitskey
lineagesthatcorrespondtotheearliestdivergencesineachgroup.Specifically,Pettalidae(sister
group to the remaining Cyphophthalmi; 43), Caddidae (sister group to the remaining Eupnoi;
46),Acropsopilionidae(sistergrouptotheremainingDyspnoi;49),andSynthetonychiidae(sister
grouptotheremainingLaniatores;88)allremaintobesampled.Althoughtheseomissionsdonot
affectinferenceofsubordinalrelationships,theyprecludecertaindownstreamapplications,suchas
moleculardatingandinferenceofphylogeneticinformativeness,whichinturnrequiresultrametric
(dated)trees(117).Thishasnotpreventedsomeauthorsfromattemptingtheseapproaches(50),
butmisapplicationoffossilcalibrationstoipsofactoderivednodesmakestheresultinginferences
unreliable. Apropos, discovery of new fossils and concomitant reinterpretations of fossil place-
ments,togetherwithtotal-evidencedating,haveyieldeddifferentestimatesforbasaldivergences
g ofsomesuborders,asdiscussedabove(36,90).
or
s. Oftheexistingharvestmantranscriptomicdatasets,themostheavilyutilizedisadevelopmental
w
vie transcriptomeoftheeupnoidPhalangiumopilio,atractablelaboratoryspeciesrecentlydeployedin
e
alr thestudyofevolutionarydevelopmentalbiology(discussedbelow)(91,94,95,97).Intriguingly,
w.annue only. mP.aonpyilitor,aansswcreiplltaiosninfamcittoersanindvtoiclvkegdeinnoemmebsr(y9o4n,i9c5d).eBveylcoopnmtreanstt,odcucuprlicaastseisnogflem-caonpyydoervtehloolpomgsenin-
d from wwpersonal us ts9ac6lo)r.gpTeinoheness,m,pweacirththiacdnuiilfsafmerrlyeonfHtpioaalxreaalxonpgdryeasipsniposenpnioddfaepgrsaerapanladotgtsecpronariiprnsigoinngdsein(cweasthi,enatghreseurkbbn-yoowwrnhnoetoolef-uognceccnutoirominnealsdipzuaipdtileoircnsat(ai8on4nd,
nloade5. For ogerndoumpleicsahtiaosnnsootfsbpeeecnifiecstgimenaotmedictoredgaioten,s)thisenaobtskennocewno.fAplatrhaolouggshitnhehraerlvaetsivtmesainzetroafnhsacrrvipetsotmmaens
w1
Do11/ for surveyed developmental genes suggests smaller genome size, because of either the absence
175. n 01/ of duplication events or the loss of paralogs if duplication had occurred. The case of paralogy
57-et o inM.americanusappearstobespecifictocertaingenomicregions(e.g.,housekeepinggenes),as
2015.60:1zalo Girib manadrTkehevreosltudrtuainposlniccarariyptetidonmfineerssepnoicdfeeh.raSsrpavenecdsitfimscceoanlrlpyhi,oatnvheseoaMclsc.ouarpmirneorvsicienanngulteosclbiobeprayerfifynechtthaisviserOetvopeoiallliseodfnoearssgsipennegceleiedosirsactshowoveleorllgy.
mol. Gon of hemocyanin, an oxygen-binding pigment in mollusks and some arthropods (e.g., horseshoe
v. Ento by corfatbhse,escigohrptihoenms,otceytarnapinulsmubounnaittesaorfaCchhneildicse;r7a8ta).iTndhiecaptleadceamdeivnetrgoefnthceispsreiqouretnocteheindaivperhgyelongceenoyf
Re theHc2/fandHc5A/dsubunitsofScorpiones+Tetrapulmonata(99),lendingcredencetothis
u. proposedrelationship(76,92).Nootherharvestmantranscriptomesequencedtodatehasrevealed
n
n
A hemocyaninorthologs,althoughsomeimmunochemicalanalyseshavelongsuggestedtheexis-
tenceofhemocyanininharvestmen(63,butsee78).Thediscoveryofthecyphophthalmidhemo-
cyaninmaybeattributabletothesamplingofalargenumberofsequencedindividuals,including
several postembryonic (juvenile) stages, in the transcriptome of M. americanus (79). However,
hemocyaninswerenotobtainedinthedevelopmentaltranscriptomeoftheeupnoidP.opilio.
ManyquestionsconcerningthegenomicarchitectureofOpilionesrequirethesequencingof
completegenomes.Suchadatasourceisrequiredtoobservepseudogenesand/ortranscription-
allyrepressedparalogs(e.g.,ofdevelopmentalgenes),facilitategenediscovery(e.g.,harvestman
hemocyanins),andunderstandgeneregulation.Inaddition,aharvestmangenomehasthepoten-
tialtoelucidatetheevolutionaryhistoryofOpilionesandtheirphylogeneticplacementamong
arachnids.Analysesofgeneorderincasesofpotentialwhole-genomeduplicationhaveprovided
effectiveconstraintsonphylogenetictreetopologiesandinferenceofevolutionaryhistoryinother
organisms(e.g.,25,80,81).
www.annualreviews.org • Harvestmen(Arachnida,Opiliones) 165
EN60CH09-Giribet ARI 27November2014 14:47
OPILIONESASANEMERGINGMODELINEVOLUTIONARY
DEVELOPMENTALBIOLOGY
Althoughmostworkindevelopmentalbiologystillfocusesonmodelorganisms,theavailabilityof
genomicandtranscriptomicresourceshasnarrowedthegapbetweenmodelandemergingmodel
systems.Onedisciplinethathasbenefitedgreatlyinthisregardisevolutionarydevelopmentalbi-
ology.Inferringtheevolutionofdevelopmentalmechanismsrequirescomparisonsacrossmultiple
species.Historically,comparisonsofdevelopmentalgeneexpressioninarthropodshaveutilizeda
handfulofmodels,withmanyoftheseconcentratedwithininsects(e.g.,53).By2010,onlythree
tractablespeciesintwoordersrepresentedarachnidswithrespecttoreliablegeneexpressionpro-
tocolsandfunctionalapproaches:thespidersCupienniussaleiandParasteatodatepidariorum,and
themiteTetranychusurticae(1,19,24).Asecondmite,Archegozeteslongisetosus,hasplayedakey
roleinthedevelopmentalliterature(113–115),butfunctionaltechniqueshavenotbeenachieved
inthespecies,limitingitsutility.
g
or ThefirstappearanceofOpilionesintheevolutionarydevelopmentalliteratureoccurredre-
s.
w cently,withP.opilioemergingasanewexperimentalmodelforharvestmandevelopment(94,95,
e
vi 97).Thiseupnoidprovedanaturalchoicetorepresenttheorder:Itisoneofthefewharvestman
e
alr speciestohaveabroaddistribution,andithasoneoftheshortestknowndevelopmentalcycles
ww.annuuse only. saymnocnhgroOnopuilsiolyndese.vIenlocpoinntgraesgtgtoclmutacnhyetse(m50p–e2ra5t0epmeermclbuetrcsho)fthEautpdnooin,oPt.uopnidlieorlgaoysdmiauplatuipslee,,wlahrigceh,
m wnal greatlyenhancesitstractabilityforstudyofembryonicdevelopment(2).Recentsuccessofinsitu
nloaded fro5. For perso hdaytbaTrifhdoeirzatinhticioslnussptieeoccnhienosifq(FuOiegpsuiwlrioietnh3e)es.mabmroyonsgoafrPac.hopniildiohdaesvelelodptmoreanptaidlpmrooldiefelsrautinoinquoeflgyenfaecielxitparteesssiionn-
w1 vestigationofgeneticmechanismsunderlyingmorphologicalevolutionincheliceratearthropods
o1/
175. Dn 01/1 boercmauitseesh.aCrovemstpmareinsornetoafindkeevyelpolpemsioemntoalrpphroiecse,sosresprinimtihteivseecthharreaecaterarsc,htnhiadtdoordneorts,owccituhrirnefsepriednecres
57-et o to mandibulate arthropod outgroups, enables the polarization of characters, a requirement for
1b
mol. 2015.60:Gonzalo Giri emtyvpooAirlcupnathliiloolyllnuoaasgsrtyhryaoodtrfievttvehaepeelpoxcaephmnmedlpieaclngeeteroaaclf.oaiTnnnfhseeievrsetoninlnaucmgteioe.osfnatakwreiolaytnosdifgsonouilfirecsseaygnnmtappelonemstsiootmrhpaohtryipsohifnyCvroehltevaleiindceeidrnaiftneae,Odthpineilgcio,haneleltihscioesrutaghihes
oy
Ent b sexuallydimorphiccheliceraeoccurinmanyarachnidgroups,includingOpiliones(Figure1f).
v. The number of segments and morphology of the chelicerae have played an important role in
e
u. R arachnid phylogeny (106), with character optimizations supporting a three-segmented, chelate
nn (i.e., articulated) chelicera in the ancestral arachnid and a larger number of segments in fossil
A
pycnogonidsandhorseshoecrabs(nonterrestrialchelicerates;3,10).Two-segmentedchelatetypes
areobservedinsuchlineagesasSolifugaeandPseudoscorpiones.Tetrapulmonatesbearatwo-
segmentedcheliceraofjackknifeshape(nonchelate).Investigatingthegeneticbasisofevolutionary
transitionsincheliceralmorphologywaspreviouslynotpossible;oftheheretoforeavailablemodel
systems,thespidercheliceraisgreatlyderivedandthemitechelicera(two-segmented,chelate)
representsanintermediatestate(Figure4).
Phalangium opilio represents the first tractable chelicerate developmental model with three-
segmented chelicerae. By comparing the expression of genes patterning the proximodistal
appendage axis in P. opilio and multiple spider species, Sharma et al. (94) demonstrated the
presenceofadachshundexpressiondomainintheproximalsegmentofthedevelopingharvestman
chelicera;neitherthissegmentnortheexpressiondomainisobservedindevelopingspiderche-
licerae(Figure4).AnembryonicRNAinterferenceapproachtosilencingthisgenesubsequently
·
166 Giribet Sharma