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Parallel Miocene dispersal events explain the cosmopolitan distribution of the

Hypogymnioid lichens

Article in Journal of Biogeography middot April 2019

DOI 101111jbi13554

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Taxonomy Phylogeny Biogeography of Megasporaceae Worldwide View project

Outline of Fungi View project

Pradeep K Divakar

Complutense University of Madrid

291 PUBLICATIONS 4956 CITATIONS

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Xinli Wei

Chinese Academy of Sciences


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Paloma Cubas



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Carlos G Boluda



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Journal of Biogeography 20191ndash11 wileyonlinelibrarycomjournaljbi emsp|emsp1copy 2019 John Wiley amp Sons Ltd

Received4June2018emsp |emsp Revised10February2019emsp |emsp Accepted21February2019DOI 101111jbi13554

R E S E A R C H P A P E R

Parallel Miocene dispersal events explain the cosmopolitan distribution of the Hypogymnioid lichens

Pradeep K Divakar1emsp| Xin-Li Wei2 emsp| Bruce McCune3emsp| Paloma Cubas1emsp| Carlos G Boluda1emsp| Steven D Leavitt4emsp| Ana Crespo1emsp| Svetlana Tchabanenko5emsp| H Thorsten Lumbsch6

1DepartamentodeBiologiacuteaVegetalIIFacultaddeFarmaciaUniversidadComplutensedeMadridMadridSpain2StateKeyLaboratoryofMycologyInstituteofMicrobiologyChineseAcademyofSciencesBeijingChina3DepartmentofBotanyandPlantPathologyOregonStateUniversityCorvallisOregon4DepartmentofBiologyampMLBeanLifeScienceMuseumBrighamYoungUniversityProvoUtah5SakhalinBranchoftheBotanicalGarden-InstituteoftheFar-EasternBranchRussianAcademyofSciencesVladivostokRussia6ScienceampEducationTheFieldMuseumChicagoIllinois

CorrespondenceXin-LiWeiStateKeyLaboratoryofMycologyInstituteofMicrobiologyChineseAcademyofSciencesBeijingChinaEmailweixlimaccn

Funding informationNationalNaturalScienceFoundationofChinaGrantAwardNumber31770022theSpanishMinisteriodeEconomiayCompetitividadGrantAwardNumberCGL2013-42498-PMinistryofScienceandTechnologyofChinaGrantAwardNumber2014FY210400

EditorDrVincentMerckx

AbstractAim Contemporaryspeciesrsquodistributionsareshapedbybothgeographyandhistori-caleventssuchasextinctiondiversificationinspecificareasandlong-distancedis-persals In the most diverse family of lichen-forming fungi Parmeliaceae theHypogymnioidcladeisanexampleofanevolutionarylineagecomprisedofspeciesoccurringintemperatetosubpolarregionsinbothhemispheresHereweelucidatethetimingofdiversificationeventsandtheimpactofhistoricaleventsonthespeciesdistributioninthislineageLocation WorldwideTaxon GeneraArctoparmelia Brodoa Hypogymnia and Pseudevernia(Parmeliaceae)Methods OursamplingfocusedonthemostdiversegenusofthecladeHypogymnia includingc70ofthedescribedspeciesWereconstructedphylogeneticrelation-shipsusingamulti-locusdatasetestimateddivergencetimesandinferredancestraldistributionsResults OuranalysessuggestthattheancestoroftheHypogymnioidcladeoccurredintheHolarcticIneachofthefourgeneraallrecoveredasmonophyleticherediver-sificationhaveoccurredlargelyduringtheMioceneandPlioceneAnumberofcur-rentlyacceptedspeciesdidnotformmonophyleticgroupsespeciallyincaseswherespecimens were collected from distinct geographic areas with multiple distinctcladescorrespondingtothegeographicregionoforiginOurresultssuggestthatonlyaveryfewspeciesintheHypogymnioidcladehavecosmopolitandistributionsallofwhichreproducesusingvegetativepropagulesincludingbothsymbioticpartnersMain conclusions WhilethediversificationoccurredpredominantlyintheNorthernHemisphereduringtheMiocenealong-distancedispersaleventfromtheNortherntotheSouthernHemisphereresultedindiversificationofacladeofspecieslargelyrestrictedtotheSouthernHemisphereSimilartoothergroupsinthisdiversefamilyourstudyhighlightstheneedforre-evaluationofspeciesboundariesamongmem-bersoftheHypogymnioidclade

K E Y W O R D S

BiogeographydiversificationHypogymnialichenMiocenemolecularevolutionmolecularsystematicssubstitutionrate

2emsp |emsp emspensp DIVAKAR et Al

1emsp |emspINTRODUC TION

Many lichens have distinctive distribution patterns such as trulycosmopolitan broad and intercontinental distributions includ-ingpantropicalspeciesorspeciesoccurringinthepolarregionsofboth hemispheres (Culberson 1972 Galloway 2007) endemic atsmall geographic scales (Luumlcking etal 2014) or disjunct distribu-tion (Leavitt etal 2013)More andmore biogeographical studiesattempting tounderstand factors influencing thewidelydisparatedistributionalpatternsoflichen-formingfungihaveoccurredinre-cent years (see eg Leavitt Esslinger Divakar amp Lumbsch 2012Nuacutentildeez-Zapataetal2017Weietal2017)

Phylogeny-basedhistoricalbiogeographyaimsatunderstand-ing how past climatological and geological processes shapedcurrent distributional patterns of species richness dealingwithevolutionaryprocessesoccurringovermillionsofyearsonalargescale during which speciation extinction dispersal and vicari-ance are the key processes (MorroneampCrisci 1995VilhenaampAntonelli2015WiensampDonoghue2004)Phylogeneticrecon-structions inferred fromDNA sequence data coupledwith an-cestral rangeestimationarepowerful toolsusedto inferwhichfactorslikelyimpactbiogeographicpatterns(ReeampSmith2008RonquistampSanmartin2011SanmartinampRonquist2004)Whilebiogeographical studies on lichen-forming fungi demonstratethat both vicariance and long- ormid-distancedispersal eventsshapedistributionsofthesesymbioticfungi(AmodePazCrespoCubas Elix amp Lumbsch 2012 Leavitt etal 2012 OtaacuteloraMartiacutenez Aragoacuten amp Molina 2010) species with cosmopolitandistributions are rarer thanearlier assumedThese results haveledtoan increasedinterest inhistoricalbiogeographicalstudiesinlichen-formingfungiespeciallyinmacrolichengroupssuchasthefamilyParmeliaceae(AmodePazetal2012Divakaretal2012 Nuacutentildeez-Zapata etal 2017) which is one of the largestfamiliesoflichen-formingfungiwithc2800currentlyacceptedspecies (JaklitschBaral LuumlckingampLumbsch2016)The familyoriginated during the Cretaceous with diversification of majorcladesduringthePaleogeneandamajor increase indiversifica-tionduringtheMiocene(Kraichaketal2015)Ithasaworldwidedistribution occurring from tropical and temperate rainforeststo deserts and Polar Regions (Divakar etal 2015 Persoh ampRambold2002)

Inspiteofthisprogressourcurrentknowledgeofevolutionaryrelationshipsandbiogeographyofspecieswithcontrastingdistribu-tion patterns is limitedAboutwhy species occurring in a distinctgeographicalareamorecloselyrelatedtoothersinthesameregionthanthoseoccurringonothercontinentseithertheproductofmul-tiplemigrationsintotheseareasorsomeotherreasonsitseemslikeremaininguntested

WithinParmeliaceaetheHypogymnioidcladeincludesfourfo-liosegeneramdashArctoparmelia Brodoa Hypogymnia and Pseudevernia SpeciesintheHypogymnioidcladeoccurinarctic-alpinetotemper-ate regions The saxicolous generaArctoparmelia and Brodoa con-tainanumberofspecieswithwideoftencircumpolardistribution

(Goward1986Hale1986)thecorticolousgenusPseudevernia in-cludestemperatespeciesmostlyrestrictedtoacontinentandadja-centareas(Egan2016Hale1968NashampElix2002)IncontrastHypogymnia has a cosmopolitan distribution occurring in temper-ate regions of both the northern and southern Hemisphere (Elix1979 Elvebakk 2011McCune 2002McCuneMartin ampWang2003) Hypogymnia also comprises species with restricted distri-butionalrangessuchaswesternNorthAmericaeasternAsiaandthesouthernHemisphereorEurasia(Elix1979ElixampJames1982Hawksworth1973Lai1980McCuneampWang2014)

The Hypogymnioid clade represents an interesting lineagefor investigating the origin of species distributions in lichen-forming fungi due to its distinctive distribution patterns So faronly two studies addressed historical biogeography in the genusHypogymniaonestudy focusedonphylogenetic relationshipandbiogeographicstructureofthisgenusinferringthatmajorlineageshave continental-scale distributions (Miadlikowska etal 2011)However thisstudywas largely restricted tospecies fromNorthAmerica (25 spp) and sampled only two genetic markers (ITS ampGPD1) the other study used phenotypic data to address possi-blebiogeographicpatternsofSouthAmerican species (Elvebakk2011)inwhichtheauthorproposedthattheHypogymnioidcladelikelyoriginatedinLaurasia

Herewe assembled amulti-locus data set including five ge-neticmarkers and representing 70 species ie 68 of the totaldescribed species in theHypogymnioid clade to reconstruct thephylogeny The resulting phylogeny was then used to estimatediversification times and ancestral ranges of themajor lineagesSpecificallyweaddressthefollowingquestions(a)Whataretheevolutionary relationships in theHypogymnioid clade (b)Whendid early diversification events happenwithin this clade and (c)Howdidthedistributionalrangesinthecladechangethroughtimeandhowcanweexplainthecurrentwidedistributionofsomespe-ciesandrestricteddistributionalrangesofothertaxaWehypoth-esizethatthemajorHypogymnioidspecieslikelyoriginatedintheHolarctic

2emsp |emspMATERIAL S AND METHODS

21emsp|emspTaxon sampling

Weincludedtotally161specimenscorrespondingto70speciesofthe fourgenera in theHypogymnioid cladeArctoparmelia (twooffivespecies)(Hale1986)Brodoa(allthreespecies)(Goward1986)Hypogymnia(62ofc90species)(Thelletal2012)andPseudevernia (threeof six species) (Egan 2016) In addition five specieswithinParmeliaceaewereselectedasoutgroupsbasedonpreviousstudies(seeTableS11inAppendixS1)

22emsp|emspMolecular methods

TotalgenomicDNAwasextractedfromasmallsectionofthethal-lusor apotheciausing theDNeasyplantMiniKit (QiagenHilden

emspensp emsp | emsp3DIVAKAR et Al

Germany) Fivemarkerswere amplified the nuclear ribosomal in-ternal transcribed spacer region (ITS) nuclear ribosomal largesubunit (nuLSU) mitochondrial ribosomal small subunit (mtSSU)glyceraldehyde-3-phosphate-dehydrogenase(GPD)andDNArepli-cationlicensingfactorminichromosomemaintenancecomplexcom-ponent7 (MCM7) Primers PCR conditions and sequencingwerethesameasdescribedpreviously(Crespoetal2007Schmittetal2009) Newly obtained sequences were aligned with sequencesdownloadedfromGenBank(wwwncbinlmnihgov)withsequencesof each locus aligned separately usingmafft (Katoh Asimenos ampToh 2009) For the ITS nuLSUGPD andMCM7 lociwe appliedthe G-INS-I alignment algorithm ldquo20PAMK=2rdquo scoring matrixandoffsetvalue=00withtheremainingparameterssettodefaultvaluesandforthemtSSUweusedtheE-INS-Ialignmentalgorithmldquo20PAMK=2rdquo scoringmatrix and offset value=00 AmbiguousalignmentpositionsweredelimitedandremovedusingGblocksfol-lowedWeietal(2017)

23emsp|emspPhylogenetic analysis

Phylogenetic analyseswere performed using the five-locus datasetWeusedamaximum likelihood (ML)approach todetectpo-tential conflicts between individual markers with a threshold ofge70 bootstrap support (Lutzoni etal 2004) Since no conflictwas evident it was assumed that the data sets were congruentandcouldbecombinedforsubsequentphylogeneticanalysesThesingle-gene and partitioned matrix were analysed and the genetopologies were reconstructed using the program RaxML 826(Stamatakis 2014) as implemented on the CIPRES Web Portal(httpwwwphyloorgsub_sectionsportal Miller Pfeiffer ampSchwartz2010)withtheGTRGAMMAmodelaparameter(Γ)forrateheterogeneityamongsitesandwithoutaparameterforesti-matingtheproportionofinvariablesites(RodriguezOliverMarinampMedina1990) Supportvalueswereassessedusing the ldquorapidbootstrappingrdquooptionwith1000replicatesAlllociweretreatedasseparatepartitionsOnlycladesthatreceivedbootstrapsupportge70 were considered strongly supported Phylogenetic treeswere drawn using the program FigTree 142 (Rambaut 2009)Alignments are available at TreeBase (httpwwwtreebaseorg)understudynumber22675

24emsp|emspDating analysis

We estimated divergence dates using the program beast 243 (Bouckaertetal2014)Themostlikelytreederivedfromthefive-locusRAxMLphylogenetic analysis as the starting tree for eachdatasetwasusedInbeastthepartitionedalignmentdatasetwasanalysedwithunlinkedsubstitutionmodelsacross the lociandarelaxed clockmodel (uncorrelated lognormal) for each partitionAYulepriorwasassigned to thebranchingprocessTheconcat-enated data setwas partitioned into five partitions correspond-ingtoeachlocususingPartitionfinder111(LanfearCalcottHoamp Guindon 2012) to infer the best-fitting substitution model

TrNef+I+G for ITS nuLSU GPD and MCM7 and TIM+I+G formtSSUallowingunlinkedparameterestimationand independentratevariationSimulationssuggest thatcomplexmodelevolutioninferredfromalimitedsampleofcharactersmaybeheavilybiased(Posada amp Crandall 2001) therefore we did not further parti-tionGPDandMCM7 locibycodonpositionSince thesemodelsare unavailable in beastweusedsimilarmodelstothoseofbest-fittingsubstitutionmodelsieSYM+I+GforITSnuLSUGPDandMCM7 andGTR+I+G formtSSUDue to the lackof appropriatefossilevidencefortheHypogymnioidcladeweusedthemolecularevolutionratesforITSestimatedforMelanelixia (243 times 10minus9sub-stitutionsiteyear)(Leavittetal2012)and070(nuLSU)and069(mtSSU)times10minus9 substitutionsiteyear obtained for Parmeliaceae(AmodePazetal2012)toestimatethetimetothemostrecentcommonancestor(MRCA)forallcladesSubstitutionratesfortheother lociwereco-estimatedalongtherununderauniformnor-mal lognormalandanexponentialpriordistributionExploratoryanalysesprovidedsimilarresultsamongtheseanalyses(resultsnotshown) hencewe selected the lognormal prior for final analysis(Thorne amp Kishino 2002) Additionally a secondary calibrationconstraining the Hypogymnioid clade (Divakar etal 2015) at3167Ma (2385ndash4062Ma95highestposteriordensityHPD)wasimplemented(Divakaretal2017)

To explore the effects of distribution priors and different cal-ibration points on the results we used different schemes (a) thedistributionsofpriorsweremodelledusinguniformnormallognor-malandexponentialpriors (HoampPhillips2009)and(b)thediver-gencetimeestimateswerecomparedbetweenthethreedifferentcalibrationsITSrateversusLSUrateversussecondarycalibrationExploratoryanalysesprovidedhighlysimilarresultsamongdifferentmodelledanalyses(seeAppendixS2fordetailsTableS22)henceweselectedthenormaldistributionpriorandthesethreecalibrationpointsforfinalanalysis

AnalyseswereperformedusingfourindependentMCMCrunsof50milliongenerationswithasamplingtreeevery1000generationsfollowedWeietal(2017)andaredetailedinAppendixS2

25emsp|emspAncestral range estimation

We estimated ancestral range probabilities using the R packagelsquoBioGeoBEARSrsquo(Matzke2014)basedonthedatedtreeobtainedinbeastSpeciesdistributionswereobtainedfromselectedliteratures(Bitter1901Elix1979Lai1980McCuneDivakarampUpreti2012McCuneampWang2014)andunpublishedresultsofthefirstauthorElvebakk (2011) and Miadlikowska etal (2011) reported mainlybased on some Hypogymnia species continental-scale distribu-tionSinceanumberofspeciesoccureitherinnorthernandcentralAsiaorEuropeandadjacentareasweseparatedthoseareasintheanalysisTherangesforeachspecieswereassignedtoeightmajorgeographic regionsNorthAmerica (A)Europeandadjacentareas(B)northernandcentralAsia(C)easternAsiaandIndo-Malayanre-gion(D)Neotropics(E)AfricaandMiddleEast(F)southernSouthAmerica(G)andAustralasia(H)


lsquoBioGeoBEARSrsquo implements likelihoodversionsofthebiogeo-graphic models DEC (dispersalndashextinctionndashcladogenesis) (Clarke2008 Ree amp Sanmartin 2009) DIVA (dispersalndashvicariance anal-ysis) (Ronquist 1997) and BAYAREA (Landis Matzke Moore ampHuelsenbeck 2013) with two free parameters describing ana-genesis therateofdispersal (d rangeexpansion)andtherateofextinction(erangecontraction)(ReeampSmith2008)butdifferedin their treatment of cladogenetic events inwhich ancestral anddaughter distributional ranges overlapWe did not consider thethirdfreeparameter (jorldquojumprdquo)thathasbeencriticizedbyReeampSmith(2018)

Theanalyseswereperformedusingthedatedtreeprunedtocontainonlyonespecimenofeachmonophyletic speciesand incaseswhereanominal taxonwas found tohavewell-supportedphylogeographicsubstructurewetreatedeachlineagecomprisedof specimens from a distinct geographic region as separatespecies-level lineages All rangeswere allowed considering thescenarioofawidedistribution in thepastofanyof thestudiedtaxa and assuming equal rates of dispersal between any tworegions Results were compared using the Akaike information criterionwith correction (AICc) considering the relatively smallsamplesizeinthisstudy(ie68ofthetotaldescribedspecies)which gives a sense of the relative probability of each modelbased on the preferred model corresponding to the minimumAICcvalue

3emsp |emspRESULTS


Atotalof500newsequences(119ITS106nuLSU101mtSSU84GPDand90MCM7)weregeneratedforthisstudy(TableS11)Thealigneddatamatrixwas3228bp in length (ITS442nuLSU726mtSSU759GPD731andMCM7570)TheconcatenatedMLtreehad a LnL (= minus22233) and single locus trees showed no conflicts(datanotshown)IntheMLtopologytheHypogymnioidcladeandallfourcurrentlyacceptedgeneraarestronglysupportedasmono-phyletic (seeAppendixS3FigureS33) The twoNorthAmericanPseudeverniaspeciesincludedherevizP consocians and P intensa didnotformseparatemonophyleticgroups

Within the genusHypogymnia two strongly supportedmono-phyleticgroupsmdashcladeldquoArdquoandldquoBrdquo(FiguresS33Figure1)werere-coveredCladeldquoArdquoincludesspeciesendemictoNEAsia(CladeldquoA1rdquo)and North America clade ldquoA2rdquo Clade ldquoBrdquo consisted of twowide-spread clades (clades ldquoB1rdquo and ldquoB2rdquo) a cladeof species restrictedtotheSouthernHemisphere(cladeldquoB3rdquo)andacladewithspeciesmainlyfromfarEastAsiaandtheHolarctic(cladeldquoB4rdquo)

WithincladeldquoArdquocladeldquoA1rdquoconsistsofNEAsianendemicsAllhave physodic acid and mostly lack physodalic acid (P-) thoughphysodalic-containingchemotypesareknowninthisgroupThere-mainingtwosubcladeshavelowbootstrapsupport(lt70)exceptthemajorclade(CladeldquoA2rdquo79)allofwhichareNorthAmericanen-demicsexceptforH hulteniioccurringinNorthAmericaandnorth-ernEuropeWithincladeldquoBrdquofourstronglysupportedsubcladescanbe distinguished Clade ldquoB1rdquo (bootstrap 87) is geographically di-verseincludingonewidespreadspecies(H tubulosa)Macaronesianislandendemics (H tavaresii and H madeirensis)onenarrowAsianendemic (H fujisanensis)oneNorthAmericanendemic(H wilfiana)andoneEuropeanspecieswithpossibledisjunctsinNorthAmericaandAsia (H farinacea)Clade ldquoB2rdquo (bootstrap100)containsonlyH physodes which is geographically widespread apparently withno close relatives Clade ldquoB3rdquo (bootstrap 100) contains speciesrestricted to the southernhemisphere plusone sorediate speciesmore widespread and occurring in the northern Hemisphere (H pulverata) All of the common Austral species occur in this cladeClade B4 (bootstrap 83) contains mostly Asian endemics withthreewidespreadnorthernspecies (H austerodes H bitteri and H subobscura)andonewidespreadmostlynorthernspecies(H vittata)NoclearmorphologicalorchemicalsynapomorphiesareassociatedwitheitherCladeAorB

Several species fall into poorly supported clades (bootstrapvalues lt70)One clade includesH canadensis H rugosa H affincurvoides 2 and H krogiaeThisgroupofmainlyNorthAmericanspeciesaremorphologicallycoherentinthedichotomousbranchinganddark lobe interiorsbuthadnofurther informationotherthanbelongingtocladeldquoArdquoThespecimenHldquoaffpulverata1rdquoisinanun-resolvedpositionincladeldquoBrdquoandisphylogeneticallydistinctfromotherspecimens identifiedasH pulverata recovered incladeldquoB3rdquoInterestinglyHypogymnialdquoaffincurvoides1rdquoismorphologicallysim-ilartoH ldquoaff incurvoides2rdquobutdistantlyrelatedsincetheyfall indifferentcladesldquoBrdquoandldquoArdquorespectively

32emsp|emspDating and ancestral ranges estimation

Themeannodeagesanddivergencedateranges(95HPD)ofthecladesareshowninTableS44 inAppendixS4andFigure1ThedivergenceofPseudeverniawasestimatedtohaveoccurredduringtheOligocene at 3143Ma (2954ndash3347Ma node Ca) whereasthe stem node of Brodoa was estimated at 2604Ma (2118ndash3025Ma node a) All other diversification events of supportedclades were estimated during the Miocene and early PlioceneThe split of Arctoparmelia from Hypogymnia was estimated at2347Ma (1856ndash2792Ma node b) The separation of the twomajorclades(AampB)withinHypogymniawasestimatedat1886Ma

F IGURE 1emspChronogramderivedfromthemaximumcladecredibilitytreeestimatedforthesampledspeciesoftheHypogymnioidcladeThechronogramwasestimatedfromamultilocusdatawithinacoalescent-basedframeworkinbeastLightgreybarsindicatethe95highestposteriordensity(HPD)intervalforthedivergencetimesestimatesValuesabovebranchesindicateagesandbelowbranchesareBayesianposteriorprobability(PP)fromthebeastanalysisonlycladessupportedinthebeastanalysisarepresentedLettersinsidecirclesreferstonodesasinTableS44Thecalibrationpoint(Ca)isindicatedatthecorrespondingnode



(1449ndash2297Ma node d)with subsequent diversificationwithinthosecladesduringtheMiocene(TableS44)DivergenceanalysisshowsthatdiversificationwithinthefourgenerastartedalsofromtheMiocene(Figure1)

The relative probabilities of three models of the ancestralrange analyses are summarized in Table1 Overall the mostlikely biogeographical model was the BAYAREALIKE model(LnL=minus2656 AICc=thinsp53540 AICc weight=100) This model(Table S44 Figure2) showed a most probable Holarctic ances-tral range for the common ancestor of theHypogymnioid cladeeitherinEuropeandNorthAmerica(ABprob=022)orEuropeNorthAmericaandeasternAsiaand Indo-Malayanregion (ABDprob=018) The most probable ancestral areas for all generaandthetwomaincladeswithinHypogymniaare intheHolarctic(a) Europe (B prob=067) or Europe and North America (ABprob=030)forBrodoa(b)UncertainforPseudevernia(c)EuropeNorthAmericaandnorthernandcentralAsia(ABCprob=056)EuropeandnorthernandcentralAsia(BCprob=017)orEuropeandNorthAmerica(ABprob=011)forArctoparmelia(d)EuropeandNorthAmerica(ABprob=068)andEuropeNorthAmericaandeasternAsiaandIndo-Malayanregion(ABDprob=014)forHypogymnia(e)NorthAmericaforcladesAandA2ofHypogymnia (f)EuropeandNorthAmericaforcladesBB1andB2Thesouth-ernHemispherewas estimated as ancestral range for clade B3whereas eastern Asia and Indo-Malayan region was estimatedas the most probable ancestral area for clade B4 (Table S44Figure2)

4emsp |emspDISCUSSION

Our study provides the most comprehensive insight to-date intophylogenetic relationshipsandbiogeography in theHypogymnioidclade in ParmeliaceaeHere themonophyly of the four currentlyaccepted genera in this cladewas supported as found previouslywith smaller ingroup taxon samplings (Divakar etal 2015 2017Miadlikowska etal 2014) These results also supported thepres-enceofdistinctdistributionalpatternsandclearphylogeographicalstructureinHypogymniaconsistentwithpreviousstudiessuggest-ing continental-scale distribution in the genus (Elvebakk 2011Miadlikowskaetal2014)

The fossil record of Hypogymnioid lichens is relatively poor(Kaasalainen Schmidt amp Rikkinen 2017 Taylor Krings amp Taylor2015) Therefore we used molecular sequence data from extanttaxatoinferthehistoricalbiogeographyoftheHypogymnioidcladewhichhavebeenwidelyused tobetterunderstandbiogeographic

patternsinothercladesofParmeliaceae(Divakaretal2015Leavittetal2012Weietal2017)

In our studywe implemented the divergent timeof 3167Mafor the Hypogymnioid node as a secondary calibration point be-causethisagewasobtainedbasedonthreelichenfossilcalibrationsie Alectoria Anzia and Parmelia (Divakaretal2017) andgot theageatthisnodeas3143Ma(Oligocene)OurstudyindicatesthatearlydiversificationeventsoftheHypogymniacladeoccurredintheNorthernHemisphere especiallyNorth America and Europe andthen dispersed to Australia and Asia The other three genera aremainly restricted to theNorthernHemispherewith a few soredi-atespeciesbeingwidelydistributedandextendingtothesouthernHemisphere

Some species were supported as widely distributed includingH tubulosa and H vittata reproducewithasexualdiasporescalledsorediathatdispersethefungalandphotosyntheticallyactivepart-neratthesametimeTheobservationthatsorediatespecieshavehigher dispersal capacity was reported (Bjerke 2003 Elvebakk2011ElvebakkFritt-RasmussenampElix2007)Somesorediatespe-ciessuchasHypogymnia austerodeshaveawidedistributionintheNorthernHemisphere(Elvebakk2011)whichisalsosupportedbyourstudyInCladeB4(FiguresS33)thesorediatespeciesH aus-terodes and H bitteriarewidespreadHypogymnia austerodes com-mon intheNorthernHemisphere isalsofound insouthernSouthAmericaandAustralasia(Elvebakk2011)OurresultssuggestthatthisgrouporiginatedfromAsia(DFigure2)orAsiaandEurope(BDFigure2) during the late Miocene (Figure1) then extended andspreadsouthwardsAsshowninFigureS33theothertwostronglysupportedcladesB1andB2arealsocomposedofsorediatespecieswithworldwidedistribution

TwomajordisjunctionsdistributionintheHypogymnia clade can befound (a)European-NorthAmericanvseasternAsiaandIndo-Malayan region species and (b) amphitropical disjunctions (northand south of tropical climates but notwithin except at high ele-vations) The latter disjunctions have been proposed of relativelyrecentoriginasaresultoflong-distancedispersaloccurringduringthe latePlioceneorPleistocene in lichens (Fernaacutendez-MendozaampPrintzen2013GallowayampAptroot1995MyllysStenroosThellampAhti2003WirtzPrintzenampLumbsch2008)andduringMiocenein plants (Ickert-Bond Rydin amp Renner 2009 Lia ConfalonieriComas amp Hunziker 2001 Simpson Tate amp Weeks 2005) Ourstudy suggests a long-distancedispersal event from theNorthernto the Southern Hemisphere happened during theMiocene Thisunderlines that similar contemporary distribution patterns can becaused by different processes at different times (Donoghue BellampLi2001)Sobasedoncurrentevidenceitappearsthatasingle

LnL No of parameters d e AICc AICc_wt

DEC minus2902 2 00120 000000 58440 000

DIVALIKE minus2963 2 00130 000000 59660 000

BAYAREALIKE minus2656 2 00064 003000 53540 100

TABLE 1emspParameterinferencelog-likelihoods(LnL)andrelativeprobabilitiesusingAICcandAICc_wt(modelweight)ofeachofthreeBioGeBearsmodelsdrateofdispersal(rangeexpansion)erateofextinction(rangecontraction)


F IGURE 2emspMaximumlikelihoodestimationsofgeographicrangeevolutionintheHypogymnioidcladeaccordingtotheBAYAREALIKEmodelinalsquoBioGeoBEARSrsquoanalysisPiechartsatthenodesshowtherelativeprobabilitiesofpossiblegeographicranges(seeTableS44inAppendixS4forancestralareasdetails)


long-distancedispersaleventduringtheMioceneledtotheoriginofaSouthernHemispherecladeofHypogymnia

A number of lineages in Hypogymnia have more restricteddistributional ranges being restricted toAsia (clade ldquoA1rdquo)NorthAmerica (clade ldquoA2rdquo) or the Southern Hemisphere (clade ldquoB3rdquo)(Figure S33) with the exception of H pulverata which is alsoknown from Japan China and easternmost Russia (Elix 1979Galloway2007)OurstudyshowedthatbothcladesldquoA1rdquoandldquoA2rdquooriginatedinNorthAmerica(ldquoArdquoFigure2)withancestorsofldquoA1rdquodispersingintoAsiaduringthemiddleandlateMiocene(Figure1)Clade ldquoB3rdquo (FigureS33)consistingofSouthernHemispherespe-cies originated in North America and Europe (AB Figure2) orNorth America Europe and Asia (ABD Figure2) and dispersedto the southernHemisphereduring themiddle and lateMiocene(Figure1) Althoughmost species of clade ldquoB4rdquo (Figure S33) ini-tially originated in North America and Europe (AB Figure2) orNorthAmericaEuropeandAsia(ABDFigure2)EastAsiabecamethemaindistributionalareasofthiscladeduringthelateMioceneStrikinglyHypogymnia species restricted toeasternAsia and theIndo-MalayanregionbelongtotwodistantlyrelatedcladesA1andB4(FigureS33)andhencespeciesrestrictedtothisareaarecom-posedoftwodifferentelementsthatreachedeasternAsiaandad-jacentregionsduringtheMiocenewhichisconsistentwithotherdisjunctNorthernHemispheredistributionsstudiedrecently(WenampIckert-Bond2009Nuacutentildeez-Zapataetal2017)

The Hypogymnioid clade initially radiated during the earlyOligocenethensuccessivelydiversifiedduringtheearlyMiocene(Figure1)TheearlyMiocene isacrucial timeperiodwithmajorpaleoclimatic events (Zachos Pagani Sloan Thomas amp Billups2001 Zachos Shackleton Revenaugh Palike amp Flower 2001)and the terrestrial climate became coolerwith remarkable ther-mal seasonality (Mosbrugger Utescher amp Dilcher 2005)Majortectonic activity and orogeny also happened in the NorthernHemisphereduringthisperiod(PaganiFreemanampArthur1999Ramstein Fluteau Besse amp Joussaume 1997) Global shifts invegetation are seen during this time period for example alpineconiferous deciduous forests emerged (Ramstein etal 1997)which are knownas very common substrates forHypogymnioidlichensmeanwhilemoreopenhabitats alsooccurred (Ramsteinetal1997)AllthoseconditionsiethesuitableclimateterrainhabitatandsubstratemayhavecontributedtothediversificationoftheHypogymnioidclade

In this study we were able to infer novel perspectives intobiogeographical patterns in Hypogymnioid lichens (a) TheHypogymnioid clade including four genera ie Arctoparmelia Brodoa Hypogymnia and Pseudevernia isawell-supportedmono-phyleticcladeamongwhichPseudeverniaistheearliestdiverginglineage and Hypogymnia the sister group (b) Hypogymnioid li-chensoriginatedduringtheearlyOligocenebutthemaindiversi-ficationhappenedduringtheMioceneand(c)theHypogymnioidcladeoriginatedintheHolarcticandexperiencedalong-distancedispersal event from theNorthern to the SouthernHemisphere

during theMiocenewhichgave rise toacladeof species in theSouthernHemisphere

Besides inthisstudywefoundseveraldistinctspecies-levellineages may be masked within a single nominal taxon withoutreadily observed phenotypical characters (Appendix S3) Whileourtaxonsamplingwasnotspecificallydesignedtoaddressspe-cies delimitation in members of the Hypogymnioid clade it isworthunderliningwhetherthereexistcrypticspeciesinthenearfuture

ACKNOWLEDG EMENTS

XLWthankstheChineseAcademyofSciencesforsupportinghervisiting scholars research at the FieldMuseum (Chicago) SupportbyNationalNatural ScienceFoundationofChina (31770022) theSpanish Ministerio de Economia y Competitividad (CGL2013-42498- P) and Ministry of Science and Technology of China(2014FY210400)aregratefullyacknowledgedSequencingwascar-riedoutattheUnidaddeGenoacutemica (ParqueCientiacuteficodeMadridUCMSpain) thePritzkerLaboratoryforMolecularSystematicsatTheFieldMuseum(ChicagoILUSA)andStateKeyLaboratoryofMycology(BeijingChina)BMthanksMarcCurtisJosephDiMeglioConradSchochandAlishaQuandtforassistancewithDNAextrac-tionandsequencing

DATA ACCE SSIBILIT Y

TheMaterialsareavailableasAppendixS1Allsequencedatagen-eratedforthisstudy(AppendixS1)canbeaccessedviaGenBankhttpswwwncbinlmnihgovgenbankAlignmentsareavailableatTreeBase(httpwwwtreebaseorg)Thecomparisonofthedi-vergencetimeestimatedforHypogymniawithapartitioneddataset of fivemarker loci and a secondary calibration constrainingthecrownoftheHypogymnioidcladeat3167MaisavailableasAppendixS2

ORCID

Xin-Li Wei httpsorcidorg0000-0001-5470-9590

R E FE R E N C E S

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Bitter G (1901) Zur Mophologie und Systematik von Parmelia UntergattungHypogymnia Hedwigia 40171ndash274

Bjerke J W (2003) Menegazzia subsimilis a widespread soredi-ate lichen Lichenologist 35 393ndash396 httpsdoiorg101016jlichenologist200308001

BouckaertRHeledJKuumlhnertDVaughanTWuC-HXieDhellipDrummondAJ(2014)BEAST2asoftwareplatformforBayesian


evolutionary analysis PLoS Computational Biology 10 e1003537httpsdoiorg101371journalpcbi1003537

ClarkeA(2008)AntarcticmarinebenthicdiversityPatternsandpro-cessesJournal of Experimental Marine Biology and Ecology 366 48ndash55httpsdoiorg101016jjembe200807008

Crespo A LumbschH TMattsson J-E BlancoO Divakar P KArticusKhellipWedinM(2007)Testingmorphology-basedhypoth-eses of phylogenetic relationships in Parmeliaceae (Ascomycota)usingthreeribosomalmarkersandthenuclearRPBIgeneMolecular Phylogenetics and Evolution 44812ndash824httpsdoiorg101016jympev200611029

CulbersonWL (1972)Disjunctivedistributions inthe lichen-formingfungiAnnals of the Missouri Botanical Garden 59165ndash173httpsdoiorg1023072394751

DivakarPKCrespoAKraichakELeavittSDSinghGSchmittIampLumbschHT(2017)Usingatemporalphylogeneticmethodtoharmonizefamily-andgenus-levelclassificationinthelargestcladeof lichen-forming fungi Fungal Diversity 84 101ndash117 httpsdoiorg101007s13225-017-0379-z

DivakarPKCrespoAWedinM LeavittSDHawksworthDLMyllysLhellipLumbschHT(2015)Evolutionofcomplexsymbioticre-lationshipsinamorphologicallyderivedfamilyoflichen-formingfungiNew Phytologist 2081217ndash1226httpsdoiorg101111nph13553

Divakar P K Del-Prado R Lumbsch H TWedinM Esslinger TL Leavitt SDampCrespoA (2012)Diversificationof thenewlyrecognized lichenformingfungal lineageMontanelia (ParmeliaceaeAscomycota)and its relationtokeygeologicalandclimaticeventsAmerican Journal of Botany 992014ndash2026httpsdoiorg103732ajb1200258

DonoghueMJBellCDampLiJH(2001)PhylogeneticpatternsinNorthernHemisphereplantgeographyInternational Journal of Plant Sciences 162S41ndashS52httpsdoiorg101086323278

EganRS(2016)PseudeverniainMexicoBibliotheca Lichenologica 110 437ndash448

ElixJA (1979)AtaxonomicrevisionofthelichengenusHypogymnia in Australasia Brunonia 2 175ndash245 httpsdoiorg101071BRU9790175

ElixJAampJamesPW(1982)HypogymniaceaeFlora of Australia 54 208ndash246

Elvebakk A (2011) A review of the genus Hypogymnia (Parmeliaceae) in Chile Bryologist 114 379ndash388 httpsdoiorg1016390007-2745-1142379

ElvebakkAFritt-RasmussenJampElixJA(2007)TheNewZealandlichenPannaria leproloma (Nyl) PM Joslashrg and its panaustral rela-tive P farinosa nom nov Lichenologist 39 349ndash359 httpsdoiorg101017S0024282907006913

Fernaacutendez-Mendoza F amp Printzen C (2013) Pleistocene expansionof the bipolar lichen Cetraria aculeata into the Southern hemi-sphereMolecular Ecology 22 1961ndash1983httpsdoiorg101111mec12210

GallowayDJ(2008)Flora of New Zealand lichens Revised second edition including lichen-forming and lichenicolous fungiLincolnNewZealandManaakiWhenuaPress

Galloway D J amp Aptroot A (1995) Bipolar lichens A reviewCryptogamic Botany 5 184ndash191

Goward T (1986) Brodoa a new lichen genus in the ParmeliaceaeBryologist 89219ndash223httpsdoiorg1023073243288

Hale M E Jr (1968) A synopsis of the lichen genus Pseudevernia Bryologist 71 1ndash11 httpsdoiorg1016390007-2745(1968)71[1ASOTLG]20CO2

HaleM E Jr (1986)Arctoparmelia a new genus in the Parmeliaceae(Ascomycotina)Mycotaxon 25 251ndash254

Hawksworth D L (1973) Two new species of Hypogymnia (Nyl) NylLichenologist 5452ndash456httpsdoiorg101017S0024282973000502

HoSYWampPhillipsM J (2009)Accounting forcalibrationuncer-taintyinphylogeneticestimationofevolutionarydivergencetimesSystematic Biology 58 367ndash380 httpsdoiorg101093sysbiosyp035

Ickert-BondSMRydinCampRennerSS(2009)Afossil-calibratedre-laxedclockforEphedraindicatesanOligoceneageforthedivergenceofAsian andNewWorld clades andMiocenedispersal intoSouthAmericaJournal of Systematics and Evolution 47444ndash456httpsdoiorg101111j1759-6831200900053x

Jaklitsch W M Baral H O Luumlcking R amp Lumbsch H T (2016)Syllabus of plant families - Adolf Englers syllabus der Pflanzenfamilien GebrStuttgartGermanyBorntraegerVerlagsbuchhandlung

KaasalainenUSchmidtARampRikkinenJ(2017)Diversityandeco-logical adaptations in Palaeogene lichensNature Plants 3 17049httpsdoiorg101038nplants201749

KatohKAsimenosGampTohH (2009)MultipleAlignmentofDNASequenceswithMAFFTMethods in Molecular Biology 537 39ndash64 httpsdoiorg101007978-1-59745-251-9_3

Kraichak E Divakar P K Crespo A Leavitt S D Nelsen M PLuumlckingRampLumbschHT(2015)Ataleoftwohyper-diversitiesDiversification dynamics of the two largest families of liche-nized fungi Scientific Reports 5 e10028 httpsdoiorg101038srep10028

LaiMJ (1980)NotesonsomeHypogymnia (Parmeliaceae) fromEastAsiaQuarterly Journal of the Taiwan Museum 33 209ndash214

LandisM JMatzkeN JMooreBRampHuelsenbeck JP (2013)BayesiananalysisofbiogeographywhenthenumberofareasislargeSystematic Biology 62 789ndash804 httpsdoiorg101093sysbiosyt040

LanfearRCalcottBHoSYampGuindonS(2012)PartitionFinderCombinedselectionofpartitioningschemesandsubstitutionmodelsforphylogeneticanalysesMolecular Biology and Evolution 29 1695ndash1701httpsdoiorg101093molbevmss020

Leavitt S D Esslinger T L Divakar P K amp LumbschH T (2012)Miocene and Pliocene dominated diversification of the lichen-formingfungalgenusMelanohalea (ParmeliaceaeAscomycota)andPleistocene population expansions BMC Evolutionary Biology 12 176httpsdoiorg1011861471-2148-12-176

Leavitt S D Fernaacutendez-Mendoza F Peacuterez-Ortega S Sohrabi MDivakar P K ampVondraacutek J hellip St Clair L L (2013) Local repre-sentationofglobaldiversityinacosmopolitanlichen-formingfungalspecies complex (Rhizoplaca Ascomycota) Journal of Biogeography 401792ndash1806httpsdoiorg101111jbi12118

Lia V V Confalonieri V A Comas C I amp Hunziker J H (2001)Molecular phylogeny of Larrea and its allies (Zygophyllaceae)ReticulateevolutionandtheprobabletimeofCreosotebusharrivalto North AmericaMolecular Phylogenetics and Evolution 21 309ndash320httpsdoiorg101006mpev20011025

Luumlcking RDal-FornoM SikaroodiMGillevet PM Bungartz FMoncada B hellip Lawrey J D (2014) A singlemacrolichen consti-tuteshundredsofunrecognizedspeciesProceedings of the National Academy of Sciences of the United States of America 111 11091ndash11096httpsdoiorg101073pnas1403517111

LutzoniFKauffFCoxCMcLaughlinDCelioGDentingerBhellipVilgalysR(2004)AssemblingthefungaltreeoflifeProgressclassification and evolution of subcellular traits American Journal of Botany 91 1446ndash1480 httpsdoiorg103732ajb91101446

Matzke N J (2014) BioGeoBEARS BioGeography with Bayesian(and likelihood) evolutionary analysis in R scripts Retrieved fromhttpcranrproject orgpackage=BioGeoBEARS CRAN TheComprehensiveRArchiveNetwork

McCune B (2002) Lichen flora of the Greater Sonoran Desert Region TempeAZLichensUnlimitedArizonaStateUniversity


McCune B Divakar P K ampUpreti D K (2012)Hypogymnia in theHimalayasofIndiaandNepalLichenologist 44595ndash609httpsdoiorg101017S0024282912000321

McCune B Martin E P amp Wang L S (2003) Five new speciesof Hypogymnia with rimmed holes from the Chinese HimalayasBryologist 106226ndash234httpsdoiorg1016390007-2745(2003)106[0226FNSOHW]20CO2

McCune B amp Wang L S (2014) The lichen genus Hypogymnia in southwest China Mycosphere 5 27ndash76 httpsdoiorg105943mycosphere

MiadlikowskaJKauffFHoumlgnabbaFOliverJCMolnaacuterKFrakerE hellip Stenroos S (2014) Multigene phylogenetic synthesis for1307 fungi representing 1139 infrageneric taxa 312 genera and66 families of the class Lecanoromycetes (Ascomycota)Molecular Phylogenetics and Evolution 79 132ndash168httpsdoiorg101016jympev201404003

MiadlikowskaJSchochCLKageyamaSAMolnarKLutzoniFampMcCuneB(2011)HypogymniaphylogenyincludingCavernularia reveals biogeographic structureBryologist 114 392ndash400 httpsdoiorg1016390007-2745-1142392

Miller M A PfeifferW amp Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic treesNewOrleansLAhttpsdoiorg101109GCE20105676129

MorroneJJampCrisciJV(1995)HistoricalbiogeographyIntroductiontomethodsAnnual Review of Ecology Evolution and Systematics 26 373ndash401httpsdoiorg101146annureves26110195002105

MosbruggerVUtescherTampDilcherD (2005)Cenozoic continen-talclimaticevolutionofCentralEuropeProceedings of the National Academy of Sciences 102 14964ndash14969 httpsdoiorg101073pnas0505267102

MyllysLStenroosSThellAampAhtiT(2003)PhylogenyofbipolarCladonia arbuscula and Cladonia mitis(LecanoralesEuascomycetes)Molecular Phylogenetics and Evolution 27 58ndash69 httpsdoiorg101016S1055-7903(02)00398-6

NashTHIIIampElixJA(2002)Pseudevernia Lichen llora of the Greater Sonoran Desert RegionTempeAZLichensUnlimitedArizonaStateUniversity

Nuacutentildeez-Zapata J Alors D Cubas P Divakar P K Leavitt S DLumbschHTampCrespoA (2017)Understandingdisjunctdistri-bution patterns in lichen forming fungi ndash insights from the genusParmelina (Parmeliaceae Ascomycota) Botanical Journal of the Linnean Society 184238ndash253httpsdoiorg101093botlinneanbox022

Otaacutelora M A G Martiacutenez I Aragoacuten G amp Molina M C (2010)Phylogeographyanddivergencedateestimatesof a lichen speciescomplex with a disjunct distribution pattern American Journal of Botany 97216ndash223httpsdoiorg103732ajb0900064

PaganiMFreemanKHampArthurMA(1999)LateMioceneatmo-sphericCO2concentrationsandtheexpansionofC4grassesScience 285876ndash879httpsdoiorg101126science2855429876

PersohDampRamboldG (2002)Phacopsis - a lichenicolousgenusofthefamilyParmeliaceaeMycological Progress 143ndash55httpsdoiorg101007s11557-006-0004-0

PosadaDampCrandallKA(2001)Selectingthebest-fitmodelofnu-cleotide substitution Systematic Biology 50 580ndash601 httpsdoiorg10108010635150118469

RambautA(2009)FigTree122Retrievedfromhttptreebioedacuksoftwarefigtree

Ramstein G Fluteau F Besse J amp Joussaume S (1997) Effect oforogenyplatemotionandland-seadistributiononEurasianclimatechangeoverthepast30millionyearsNature 386788ndash795httpsdoiorg101038386788a0

ReeRHampSanmartin I (2009)Prospectsandchallenges forpara-metric models in historical biogeographical inference Journal of

Biogeography 361211ndash1220httpsdoiorg101111j1365-2699 200802068x

Ree R H amp Smith S A (2008) Maximum likelihood inferenceof geographic range evolution by dispersal local extinctionand cladogenesis Systematic Biology 57 4ndash14 httpsdoiorg10108010635150701883881

ReeRHampSmithSA(2018)Conceptualandstatisticalproblemswiththe DEC+J model of founder-event speciation and its comparisonwithDECviamodelselectionJournal of Biogeography 45741ndash749httpsdoiorg101111jbi13173

Rodriguez FOliver J LMarinAampMedina J R (1990) The gen-eral stochastic-model of nucleotide substitution Journal of Theoretical Biology 142 485ndash501 httpsdoiorg101016S0022-5193(05)80104-3

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Sanmartin I amp Ronquist F (2004) Southern Hemisphere bio-geography inferred by event-based models Plant versus an-imal patterns Systematic Biology 53 216ndash243 httpsdoiorg10108010635150490423430

Schmitt I Crespo ADivakar P K Fankhauser J Herman-SackettENelsenMPhellipLumbschHT (2009)Newprimersforsingle-copy protein-coding genes for fungal systematics Persoonia - Molecular Phylogeny and Evolution of Fungi 23 35ndash40 httpsdoiorg103767003158509X470602

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Thell A Crespo A Divakar P K Kaumlrnefelt I Leavitt S DLumbsch H T amp Seaward M R D (2012) A review of the li-chen family Parmeliaceae - history phylogeny and current tax-onomy Nordic Journal of Botany 30 641ndash664 httpsdoiorg101111j1756-1051201200008x

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WeiXLLeavittSHuangJPEsslingerTLWangLSMoncadaBhellip LumbschHT (2017) ParallelMiocene-dominateddiversifi-cationof the lichen-forming fungalgenusOropogon (ParmeliaceaeAscomycota)indifferentcontinentsTaxon 661269ndash1281httpsdoiorg10127056661

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BIOSKE TCH

Pradeep K Divakar isaprofessorofUniversidadComplutensedeMadrid SpainHis research focuseson the lichenized fungiParmeliaceae and related lichenicolous fungi including taxon-omybiodiversityphylogenyecologyclimatechangebiogeog-raphypopulationgeneticsmolecularsystematicsandevolution

AuthorcontributionsPKDXLWBMandHTLconceivedthestudyXLWBMandSTprovidedsamplesPKDXLWBMPCandCGBcollectedthedataXLWandPCgener-atedtheDNAsequencesPKDXLWBMandPCanalysedthedataHTLledandPKDXLWandBMjoinedthewritingAllauthorsdiscussedthepaperandgavecomments

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleDivakarPKWeiX-LMcCuneBetalParallelMiocenedispersaleventsexplainthecosmopolitandistributionoftheHypogymnioidlichens J Biogeogr 2019001ndash11 httpsdoiorg101111jbi13554

View publication statsView publication stats

Journal of Biogeography 20191ndash11 wileyonlinelibrarycomjournaljbi emsp|emsp1copy 2019 John Wiley amp Sons Ltd

Received4June2018emsp |emsp Revised10February2019emsp |emsp Accepted21February2019DOI 101111jbi13554

R E S E A R C H P A P E R

Parallel Miocene dispersal events explain the cosmopolitan distribution of the Hypogymnioid lichens

Pradeep K Divakar1emsp| Xin-Li Wei2 emsp| Bruce McCune3emsp| Paloma Cubas1emsp| Carlos G Boluda1emsp| Steven D Leavitt4emsp| Ana Crespo1emsp| Svetlana Tchabanenko5emsp| H Thorsten Lumbsch6

1DepartamentodeBiologiacuteaVegetalIIFacultaddeFarmaciaUniversidadComplutensedeMadridMadridSpain2StateKeyLaboratoryofMycologyInstituteofMicrobiologyChineseAcademyofSciencesBeijingChina3DepartmentofBotanyandPlantPathologyOregonStateUniversityCorvallisOregon4DepartmentofBiologyampMLBeanLifeScienceMuseumBrighamYoungUniversityProvoUtah5SakhalinBranchoftheBotanicalGarden-InstituteoftheFar-EasternBranchRussianAcademyofSciencesVladivostokRussia6ScienceampEducationTheFieldMuseumChicagoIllinois

CorrespondenceXin-LiWeiStateKeyLaboratoryofMycologyInstituteofMicrobiologyChineseAcademyofSciencesBeijingChinaEmailweixlimaccn

Funding informationNationalNaturalScienceFoundationofChinaGrantAwardNumber31770022theSpanishMinisteriodeEconomiayCompetitividadGrantAwardNumberCGL2013-42498-PMinistryofScienceandTechnologyofChinaGrantAwardNumber2014FY210400

EditorDrVincentMerckx

AbstractAim Contemporaryspeciesrsquodistributionsareshapedbybothgeographyandhistori-caleventssuchasextinctiondiversificationinspecificareasandlong-distancedis-persals In the most diverse family of lichen-forming fungi Parmeliaceae theHypogymnioidcladeisanexampleofanevolutionarylineagecomprisedofspeciesoccurringintemperatetosubpolarregionsinbothhemispheresHereweelucidatethetimingofdiversificationeventsandtheimpactofhistoricaleventsonthespeciesdistributioninthislineageLocation WorldwideTaxon GeneraArctoparmelia Brodoa Hypogymnia and Pseudevernia(Parmeliaceae)Methods OursamplingfocusedonthemostdiversegenusofthecladeHypogymnia includingc70ofthedescribedspeciesWereconstructedphylogeneticrelation-shipsusingamulti-locusdatasetestimateddivergencetimesandinferredancestraldistributionsResults OuranalysessuggestthattheancestoroftheHypogymnioidcladeoccurredintheHolarcticIneachofthefourgeneraallrecoveredasmonophyleticherediver-sificationhaveoccurredlargelyduringtheMioceneandPlioceneAnumberofcur-rentlyacceptedspeciesdidnotformmonophyleticgroupsespeciallyincaseswherespecimens were collected from distinct geographic areas with multiple distinctcladescorrespondingtothegeographicregionoforiginOurresultssuggestthatonlyaveryfewspeciesintheHypogymnioidcladehavecosmopolitandistributionsallofwhichreproducesusingvegetativepropagulesincludingbothsymbioticpartnersMain conclusions WhilethediversificationoccurredpredominantlyintheNorthernHemisphereduringtheMiocenealong-distancedispersaleventfromtheNortherntotheSouthernHemisphereresultedindiversificationofacladeofspecieslargelyrestrictedtotheSouthernHemisphereSimilartoothergroupsinthisdiversefamilyourstudyhighlightstheneedforre-evaluationofspeciesboundariesamongmem-bersoftheHypogymnioidclade

K E Y W O R D S

BiogeographydiversificationHypogymnialichenMiocenemolecularevolutionmolecularsystematicssubstitutionrate





























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Parallel Miocene dispersal events explain the cosmopolitan ... · Parallel Miocene dispersal events...

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