Phylogeny, historical biogeography, and diversification of angiosperm order Ericales suggest

21 Pages·2017·0.77 MB·English

by  Jeffrey P. Rose

Molecular Phylogenetics and Evolution 122 (2018) 59–79
ContentslistsavailableatScienceDirect
Molecular Phylogenetics and Evolution
journal homepage: www.elsevier.com/locate/ympev
fi
Phylogeny, historical biogeography, and diversi cation of angiosperm order
T
Ericales suggest ancient Neotropical and East Asian connections
Jeffrey P. Rosea,⁎, Thomas J. Kleistb, Stefan D. Löfstrandc, Bryan T. Drewd, Jürg Schönenbergere,
Kenneth J. Sytsmaa
aDepartmentofBotany,UniversityofWisconsin-Madison,430LincolnDr.,Madison,WI53706,USA
bDepartmentofPlantBiology,CarnegieInstitutionforScience,260PanamaSt.,Stanford,CA94305,USA
cDepartmentofEcology,EnvironmentandBotany,StockholmUniversity,SE-10691StockholmSweden
dDepartmentofBiology,UniversityofNebraska-Kearney,Kearney,NE68849,USA
eDepartmentofBotanyandBiodiversityResearch,UniversityofVienna,Rennweg14,AT-1030,Vienna,Austria
A R T I C L E I N F O A B S T R A C T
Keywords: InferringinterfamilialrelationshipswithintheeudicotorderEricaleshasremainedoneofthemorerecalcitrant
Ericaceae problemsinangiospermphylogenetics,likelyduetoarapid,ancientradiation.Asaresult,nocomprehensive
Ericales time-calibratedtreeorbiogeographicalanalysisoftheorderhasbeenpublished.Here,weelucidatephyloge-
Longdistancedispersal netic relationships within the order and then conduct time-dependent biogeographical and diversification
Supermatrix
analyses by using a taxon and locus-rich supermatrix approach on one-third of the extant species diversity
Theaceae
calibratedwith23macrofossilsandtwosecondarycalibrationpoints.Ourresultscorroboratepreviousstudies
Vicariance
andalsosuggestseveralnewbutpoorlysupportedrelationships.Newlysuggestedrelationshipsare:(1)holo-
parasitic Mitrastemonaceae is sister to Lecythidaceae, (2) the clade formed by
Mitrastemonaceae+Lecythidaceae is sister to Ericales excluding balsaminoids, (3) Theaceae is sister to the
styracoids+sarracenioids+ericoids,and(4)subfamilialrelationshipswithEricaceaesuggestthatArbutoideae
issistertoMonotropoideaeandPyroloideaeissistertoallsubfamiliesexcludingArbutoideae,Enkianthoideae,
andMonotropoideae.OurresultsindicateEricalesbegantodiversify110Mya,withinIndo-Malaysiaandthe
Neotropics,withexchangebetweenthetwoareasandexpansionoutofIndo-Malaysiabecominganimportant
areainshapingtheextantdiversityofmanyfamilies.Rapidcladogenesisoccurredalongthebackboneofthe
orderbetween104and106Mya.Jumpdispersalisimportantwithintheorderinthelast30My,butvicarianceis
themostimportantcladogeneticdriverofdisjunctionsatdeeperlevelsofthephylogeny.Wedetectbetween69
and81shiftsinspeciationratethroughouttheorder,thevastmajorityofwhichoccurredwithinthelast30My.
Weproposethatrangeshiftingmayberesponsibleforoldershiftsinspeciationrate,butmorerecentshiftsmay
bebetterexplainedbymorphologicalinnovation.
1. Introduction datahavebeenused(deQueirozandGatesy,2007;Janiesetal.,2013).
Such studies have generated novel insights into the phylogeny, bio-
Therelative contributions oftaxonomic versuscharacter sampling geography,diversification,andcharacterevolutioninlandplantgroups
toimprovedestimationofphylogenetichistorieshaslongbeendebated. where phylogenetic inference based on few taxa and relatively few
Ontheonehand,increasingcharactersamplingallowsformoredatato characters has been problematic (Givnish et al., 2015; Hinchliff and
infer relationships, and is especially useful in the case of rapid radia- Roalson,2013;Roseetal.,2016;Smithetal.,2011;Soltisetal.,2013;
tions where branch lengths are short. On the other hand, increasing TestoandSundue,2016;WurdackandDavis,2009).Wepresentherea
taxonomic sampling may “discover” phylogenetically informative supermatrixanalysisofthespecioseasteridorderEricalesandusethe
characters and may also break up spurious, long branches (Wiens, resultingphylogeneticframeworktoevaluatespeciesdiversificationin
2006).Recently,“supermatrix”approachesthatinferthephylogenetic the context of biogeographical vicariance and dispersal across con-
historyoflargenumbersoftaxainthepresenceofhighlevelsofmissing tinents.
⁎Correspondingauthor.
E-mailaddresses:[email protected](J.P.Rose),[email protected](T.J.Kleist),[email protected](S.D.Löfstrand),[email protected](B.T.Drew),
[email protected](J.Schönenberger),[email protected](K.J.Sytsma).
https://doi.org/10.1016/j.ympev.2018.01.014
Received25August2017;Receivedinrevisedform8January2018;Accepted18January2018
Available online 02 February 2018
1055-7903/ © 2018 Elsevier Inc. All rights reserved.
J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
Fig.1.RepresentativereproductivediversitywithintheorderEricales.(A)Impatienspallida(Balsaminaceae)(B)Primulaveris(left)andP.meadia(right)(Primulaceae)(C)Ardisiacrenata
(Primulaceae)(D)Lysimachialancifolia(Primulaceae)(E)Leptosiphonmontanus(Polemoniaceae)(F)Fouquieriasplendens(Fouquieriaceae)(G)Eschweilerasagotiana(Lecythidaceae)(H)
Synsepalumdulciferum(Sapotaceae)(I)Camelliasinensis(Theaceae)(J)Halesiacarolina(Styracaceae)(K)Sarraceniaflava(Sarraceniaceae)(L)Diospyrosvirginiana(Ebenaceae)(M)Clethra
alnifolia(Clethraceae)(N)Gaultheriaprocumbens(Ericaceae)(O)Rhododendroncalendulaceum(Ericaceae)(P)Monotropsisreynoldsiae(Ericaceae).
1.1. FamiliesandknownrelationshipswithinEricales inferring relationships among families in the order has been difficult
(Anderberg et al., 2002; Geuten et al., 2004; Lens et al., 2007;
Ericales is a largely woody, economically important order of Schönenbergeretal.,2005).Asinotherhigher-levelcladesofproble-
∼12,000speciesdistributed in21or22families(APGIV,2016), de- matic angiosperm groups (e.g., rosids, placement of Caryophyllales,
pending on if Sladeniaceae is recognized asdistinct fromPentaphyla- Malphigiales,Saxifragales),thisdifficultyhasbeenattributedtoarapid
caceae. Families now recognized in theorder exhibit a wide range of radiationinthespanofseveralmillionyears(Davisetal.,2005;Soltis
floral diversity, particularly in the androecium, but also in perianth etal.,2010;2013)whichmayexplainincongruencebetweengenomic
fusion and various other floral characters (Chartier et al., 2017; regionsobservedbyGeutenetal.(2004).Inaddition,inthosecladesof
Schönenbergeretal.,2005;Fig.1).Therefore,itisnotsurprisingthat Ericales where the relationships among families have been well-re-
basedonmorphologyalone,membersbelongingtothisorderhadbeen solved, the relationships often are at odds from a morphological per-
thought to be distantly related (Cronquist, 1981). However, the spective and necessitate comparative anatomical studies to determine
monophylyoftheorderhasbeenclearlydemonstrated(Albachetal., bothputativesynapomorphiesandfacilitateanunderstandingoffloral
2001;Anderbergetal.,2002;Bremeretal.,2002;Chaseetal.,1993; evolution in the order (Löfstrand and Schönenberger, 2015a;
Ruhfel et al., 2014; Soltis et al., 2000, 2011; Schönenberger et al., Schönenberger, 2009; Schönenberger et al., 2010; von Balthazar and
2005). Within the order, monophyly of families has generally been Schönenberger,2013).
substantiatedwiththeexceptionofTheaceae(Anderbergetal.,2002; The most recent molecular phylogeny of the order is that of
now largely broken up into Theaceae and Pentaphylacaceae) but Schönenberger et al. (2005) which used 11 molecular markers (two
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J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
ribosomal, two mitochondrial, and seven chloroplast) from 59 ex- subfamilies of Lecythidaceae, with the Neotropics as apparently an
emplarsoftheorder.Whileprovidingsomefurtherresolutionalongthe “apomorphic”areacomplicates thishypothesis (Mori etal.,2007).In
backbone of the phylogeny from the prior study of Anderberg et al. addition,thepantropicaloramphi-Pacificdistributionpatternsofmany
(2002), several relationships were still unresolved. Nevertheless, families (Lecythidaceae, Primulaceae subf. Myrsinoideae, Sapotaceae)
Schönenberger et al. (2005) found support for seven major supra-fa- beg the question of whether long distance dispersal or vicariance has
milial clades (informally named here and referred to throughout the playedaroleinshapingtheircurrentdistributionpatterns,and,ifboth,
text): (1) “balsaminoids” (Balsaminaceae, Marcgraviaceae, Tetra- whattherelativecontributionsofeachhasbeen.Specifically,withre-
meristaceae),(2)“polemonioids”(Fouquieriaceae,Polemoniaceae),(3) gardtowidespreadtropicalclades,thequestionhasbeenwhethertheir
“primuloids” (Ebenaceae, Primulaceae, Sapotaceae), (4) “styracoids” distributions are explained by vicariance following the breakup of
(Diapensiaceae, Styracaceae,Symplocaceae), (5)acladecomprisedof Gondwana, boreotropical land bridges, or long distance dispersal
Actinidiaceae, Clethraceae, Cyrillaceae, Ericaceae, Roridulaceae, Sar- (Givnishand Renner,2004; Nie etal., 2012; Pennington et al., 2006;
raceniaceae, which has since been divided into the “ericoids” (Cle- Thomasetal.,2015).Intheiranalysisoftheamphi-PacificSymploca-
thraceae, Cyrillaceae, Ericaceae) and “sarracenioids” (Actinidiaceae, ceae, Fritsch et al. (2015) suggested boreotropical migration for the
Roridulaceae,Sarraceniaceae)(LöfstrandandSchönenberger,2015a,b; familywithanorigininSoutheastAsia,spreadtoNorthAmerica,and
Schönenberger et al., 2012), (6) “theoids” (Theaceae, ericoids, sarra- then later spread to South America. Overall, studies on angiosperms
cenioids,andstyracoids),and(7)“coreEricales”(allcladesexcluding have largely suggested that, at least at the family level, clades are
balsaminoids,polemonioids,andLecythidaceae) generally too young to have their distributions explained by the
The holoparasitic family Mitrastemonaceae, consisting of twospe- breakupofGondwanabutmaybeexplainedbyvicariancethroughland
cies in the genus Mitrastemon (Meijer and Veldkamp, 1993; Reveal, bridges(eithernorthernorsouthernhemisphere)orlongdistancedis-
2010),wasnotincludedbySchönenbergeretal.(2005),despiteaclear persal (Berger et al., 2016; Cardinal-McTeague et al., 2016; Ruhfel
affinity to the order based on mitochondrial matR, atp1, and cox1 se- et al., 2016; Thomas et al., 2015). As many families within Ericales
quence data (Barkman et al., 2004, 2007). Unfortunately, studies in- haveapantropicaloramphi-Pacificdistribution,simultaneousanalyses
cluding Mitrastemon have lacked enough sampling within Ericales to ofthesegroupsallowsforconcurrenttestingtoseeiftheprocessesthat
confidently hypothesize its exact placement (APG IV, 2016). The ledtothepresent-daydistributionsaresimilarand/oroccurredwithin
polystemonous condition with connate filaments (Meijer and thesametimeframe.
Veldkamp,1993)andunusualplacentationsuggestpotentialaffinities TherecentexplosioninthenumberofdiscoveredCretaceousfossils
to Lecythidaceae (Mori et al., 2007; Mori et al., 2015), although the of ericalean affinity (Crepet et al., 2013; Martínez et al., 2016;
familyappearsfairlyremotefromotherEricalesbasedonoverallfloral Schönenberger and Friis, 2001; Schönenberger et al., 2012) from
form(Chartieretal.,2017). EuropeandNorthAmericaindicatesanorthtemperateoriginofatleast
The recent emphasis on whole-plastome sequencing has provided the ericoid clade of Schönenberger et al. (2005). Not only does this
additional information on phylogenetic relationships in Ericales. recentlyenrichedfossilrecordprovidecluesastotheoriginoftheorder
Unfortunately,onlyahandfulofplastomesfromfewericaleanfamilies or certain clades within the order (which can be recapitulated with
have been sequenced and these families belong to the well-supported biogeographical analyses of extant tips), but also provides numerous
clades of Schönenberger et al. (2005). Nevertheless, phylogenetic re- fossilstocalibrateamolecularphylogeny.
constructionsbasedoncodinggenes(Joetal.,2016;Yanetal.,2016)
recapitulate the findings of Schönenberger et al. (2005) but also pro- 1.3. DiversificationshiftswithinEricales
vide support for a relationship of Theaceae as sister to the ericoids,
sarracenioids,andstyracoids. Within Ericales, the occurrence of several large genera (Impatiens
(Balsaminaceae), ∼1,000 spp.; Rhododendron (Ericaceae), ∼1,000
1.2. BiogeographicaldistributionsofEricales spp.;Diospyros(Ebenaceae),∼700spp.;Erica(Ericaceae),∼700spp.;
Primula (Primulaceae) ∼400 spp.; Symplocos (Symplocaceae), ∼300
Biogeographically, Ericales is widespread with both pantropical spp.)suggeststhepossibilityofmultiple,temporallyandgeographically
(Lecythidaceae, Sapotaceae) and cosmopolitan (Ericaceae, widespreadshiftsindiversification.Evidenceforshiftsinthesegroups
Primulaceae) clades. Because classifications based on morphology has been presented for Erica and Rhododendron (Bouchenak-Khelladi
differsodramaticallycomparedtothecircumscriptionoftheorderas etal.,2015;Schweryetal.,2015;putativelyassociatedwiththeriseof
currently recognized, no explicit hypotheses about the biogeographic montaneareas)andPrimula(deVosetal.,2014;putativelyassociated
history of the order have been proposed. Biogeographical studies on with the evolution of heterostyly). However, it remains to be seen if
individual families or subfamilies using more complex models than these putative shifts are significant in the context of the order as a
simplecharactermappinghavebeenconductedonDiapensiaceae(Hou whole.
et al., 2016), Ebenaceae (Duangjai et al., 2009), Ericaceae (Kron and Inthis study,wepresentan updated time-calibrated phylogenyof
Luteyn, 2005), Sarraceniaceae (Ellison et al., 2012), Sapotaceae subf. Ericalesusingasupermatrixapproach,incorporatingarichsampleof
Chrysophylloideae (Bartish et al., 2011; Swenson et al., 2014), Styr- both taxa and genes. Using this data set, we attempt to (1) resolve
acaceae(Fritschetal.,2001),andSymplocaceae(Fritschetal.,2015), backbonerelationshipsintheorder,(2)placetheholoparasiticfamily
but the order remains to be treated as a whole. These studies have Mitrastemonaceae, (3) estimate when and where major clades of the
demonstrated a Northern Hemisphere (especially Eurasian) origin of orderoriginated,(4)examinethebiogeographicprocessesresponsible
Diapensiaceae, Ericaceae, and Symplocaceae, African and South for current day distribution patterns, testing hypotheses related to
American or Eurasian and South American origin of Ebenaceae, pantropical distributions (specifically vicariance through polar migra-
Southeast Asian or Australian origin of Sapotaceae subf. Chryso- tions vs. long distance dispersal), and (5) examine the location and
phylloideae,andaSouthAmericanoriginofsarracenioids.Asmostof timing of shifts in diversification rates and provide hypotheses to de-
thesefamiliesarecloselyrelated,nobasalnodesoftheorderhavebeen scribetheirdistributioninphylogeneticspace.
representedinbiogeographicalanalyses.
Based on the present-day distributions of the grade of families 2. Materialsandmethods
leadingtothecorefamiliesofEricales,whichatleastpartiallyoccupy
Indo-Malaysia and/or the Neotropics (balsaminoids, Lecythidaceae, 2.1. Phylogeneticdata
polemonioids),onemighthypothesizetheoriginoftheorderineither
of these regions. However, the largely Afrotropical distribution of Weutilizedasupermatrixapproachofincreasingsamplingoftaxa
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J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
andcharacters,anapproachthatproducesaccuratephylogenies(even (equivalent to 5 million generations) as a burn-in. The posterior dis-
inthepresenceofhighlyincompletedataforsometaxa)suitableforthe tribution of trees was summarized on a maximum clade credibility
analysisofmacroevolutionarypatterns(Roseetal.,2016;Soltisetal., (MCC) tree and on a pruned version of the best ML tree using Sum-
2013;TestoandSundue,2016).Wegatheredsequencedatafrom4,943 Trees. The alignment file and partitions are available via Mendeley
species.TheseincludedmembersofEricales(4,531species),Cornales Data.
(411 species), andAquifoliales(onespecies), with Cornales astheul-
timateoutgroup. 2.2. Fossilcalibrations
Genetic data totaled 25 loci representing the chloroplast (ndhF,
psbA-trnH,rbcL,rpl16,rpoC1,rps16,trnL-trnL-trnF,trnS-trnG,psbB,rps2, As the size of the final data matrix precluded dating in BEAST
rps4, atpB, matK), mitochondrial (atp1, ccmB, cob, cox1, matR, mttB, (Drummond et al., 2012), we utilized penalized likelihood as im-
nad4-nad5,nad5,rps3), and ribosomal (ITS, 18S, 26S) genomes. Most plemented intreePL(Smith andO’Meara, 2012)onourbestMLtree.
sequencedatawerederivedfromGenBankbutwealsoadded470un- Thisprogram has beenshown to estimate divergencedates similarto
published sequences, mostly from the mitochondrial genome. (PCR those of BEAST (Lagomarsino et al., 2016). In total, we used 25 cali-
methods follow Schönenberger, et al. (2005); loci follow Soltis et al., bration points (23 macrofossils and 2 secondary calibrations). We re-
2011).CompleteGenBankvoucherinformationandnewsequencesare strictedfossilcalibrationstomacrofossils(flowers,fruits,seeds,leaves)
listedinSupplementaryTable1ofAppendixAandtaxonomiccoverage of both Ericales and Cornales that could be confidently assigned to
per locus is indicated in Supplementary Table 2 of Appendix A. In- crowngroups,astreePLonlypermitsplacingminimumandmaximum
dividuallociwerealignedinMAFFT(KatohandStandley,2013)using dates around nodes. Several good fossils such as Glandulocalyx upa-
defaultparameters.Sequencedirectionwasadjustedaccordingtothat toiensis(Schönenbergeretal.,2012)areassignabletothesamecrown
of the first sequence to account for potentially reversed sequences in groupsasdifferentbutolderfossilsandwerethereforenotusedinour
GenBank. Alignments for each locus were then concatenated into a dating analysis. For some important fossils assignable to stems, we
singlematrix. placed them on the crown group preceding that stem. In addition to
Geuten et al. (2004), and to a lesser extent Schönenberger, et al. fossils, we restricted the crown ages of asterids, and Ericales+Aqui-
(2005)reportedhigher-leveltopologicalconflictbetweengenomicre- folialesusingsecondarycalibrationpointsfromMagallónetal.(2015)
gionswithintheorder.However,mosttopologicalconflictspresented (Table1,SupplementaryText1ofAppendixA).ForourtreePLanalysis,
inFig.3ofGeutenetal.(2004)arenotwellsupportedexceptforre- we conducted a thorough search using default parameters except we
lationships between balsaminoid families and a Primulaceae+Penta- specified 8 threads, random cross-validation, and a smoothing para-
phylacaceaerelationshipsupportedinaplastid-codingdataset. meter of 100. The treePL configuation file is available via Mendeley
Ourconcatenateddatamatrixwassubjectedtomaximumlikelihood Data.
(ML) analysis in RaxML (Stamatakis, 2014). To account for different
substitution rates among genomes, we used PartitionFinder2 (Lanfear 2.3. Biogeographicalanalyses
etal.,2017)totestforthebestpartitioningschemeamongthreepos-
sible a priori partitions corresponding to the three genomic regions Tobothfacilitateeaseofcodingaswellastoremovepotentialbias
explored in this study (ribosomal, chloroplast, and mitochondrial). incoding,weoptedforanautomaticmeansofcodingtips.Todothis,
Branchlengthsweresettolinked.Welimitedtestingforthebestfitting we first downloaded all databased records of Ericales in the Global
nucleotide substitution model to the GTR models implemented in Biodiversity Information Facility (GBIF; http://www.gbif.org/). We
RAxML with AICc selection between models. The best fitting parti- limitedoursearchtoonlyspecimenrecordsandtospecimenswithno
tioningschemewasfoundusingthe“rcluster”searchscheme(Lanfear knowncoordinateissuesfollowingestablishedprocedures(Maldonado
et al., 2014). PartitionFinder2 suggested all three a priori partitions etal.,2015;Spalinketal.,2016a,b).Usingthissetofcoordinates,we
should be retained and suggested GTR+I+G as the best fitting nu- thendeterminedwhichbiogeographicrealmthesespecimensbelonged
cleotide substitution model for each. Because the RAxML manual re- to by extracting the “realm” raster layer from the “Terrestrial Ecor-
commendsagainstaddinginvariantsitesasafreeparameter,weused egionsoftheWorld”shapefile(Olsonetal.,2001)availablefromthe
the slightly less parameterized GTR+G model in all phylogenetic World Wildlife Fund website (http://www.worldwildlife.org/
analyses.MLanalysiswasconductedinRaxMLundertheGTRGAMMA publications/terrestrial-ecoregions-of-the-world) using the R package
model of sequence evolution. All other parameters were set to their raster(HijmansandvanEtten,2016).Realmswerethencondensedinto
default values. The best tree was found using 10 separate search re- six areas as follows: (1) Afrotropics, (2) Australasia+Oceania (in-
plicates. Branch support was assessed through two runs of 250 rapid cluding Hawaii), (3) Indo-Malaysia, (4) Nearctic, (5) Neotropics, and
bootstrap replicates. ML bootstrap samples were summarized on the (6)Palearctic.Eachtipinourphylogenywaseitherpresentorabsentin
best treeusingSumTreesv. 4.2.0inthePython packageDendroPy v. each area. After initial coding, the range assigned to each tip was
4.2.0(SukumaranandHolder,2010). checked a second time to ensure that realm assignment was accurate
As thebackbone relationships of Ericales havebeencontroversial, (i.e.,thesignoflatitudinalcoordinatesinGBIFwasnotinverted,cul-
wealsowantedtoassesstopologicaluncertaintygiventheassumptions tivatedspecimenswerenotincluded).Additionally,importanttaxanot
inourMLanalysis.WethereforeconductedaBayesiananalysis(BI)on presentintheGBIFdatawerescoredbyhandbasedonspecimendata
asubsetof191species.Thesespecieswereselectedbasedontaxonomic availableonTropicos(http://www.tropicos.org/).
representativeness and genetic completeness (with the fewest missing In general, the distribution of each tip is representative of the
nucleotidesequencesfromthe25targetedloci).Becausethemotivation geographic range of that species. However, for some tips, the tip is
for including a Bayesian analysis in this study was to account for to- representativeofthedistributionofahigher-levelcladeasfollows.(1)
pologicaluncertaintygiventheparametersusedinourMLanalysis,we Mitrastemon yamamotoi was used as a placeholder for
analyzed this reduced matrix using MrBayes version 3.2.6 (Ronquist Mitrastemonaceae, which also occurs in Central America. (2)
etal.,2012)underthesamemodelofsequenceevolutionandthesame Pentameristaneotropicawasusedasaplaceholderforthisgenusandits
threepartitionsmentionedabove.Sixseparateanalysesofthreerunsof sistergenus,Tetramerista,whichoccursinSoutheastAsia.(3)Gordonia
four chains each were run for 10 million generations with sampling singaporeanawasusedasaplaceholderfortheAustralasianG.papaua,
every1,000generations.Allotherparametersweresettotheirdefault as G. papuana has been suggested to have as a close relationship to
values.Weexaminedparameterconvergenceinall18runsusingTracer Indonesian and Philippine taxa (Barker, 1980). (4) Impatiens capensis
v. 1.6.0 (Rambaut et al., 2014). All parameters for this dataset con- was used as a placeholder for Central American I. turrialbana, as its
vergedwithin2milliongenerations.Wediscardedthefirst5,000trees floralmorphologyissimilartoNorthAmericanspecies(Donnell-Smith,
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J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
Table1
Macrofossilcalibrationsusedinthisstudywiththeminimumandmaximumagesandmostrecentcommonancestorsofthenodesconstrained.*indicatessecondarydates**indicates
fossilsbestassignedtostemlineagesinsteadplacedonthenextyoungestcrown.
Fossil(clade) Agerange(My) Crowngroup Reference
Actinocalyxbohrii 84.0–80.6 Diapensia+Styrax** Fritschetal.(2015)
Alangiumsp. 73–66 Alangium+Cornus Xiangetal.(2011)
Androsacesp. 5.2–23.2 Androsace+Douglasia Zhangetal.(2001)
Aquifoliales+Ericales* 107.4–117.1 Aquifoliales+Ericales Magallónetal.(2015)
asterids* 110.4–118.9 root Magallónetal.(2015)
Austrodiospyroscryptostoma 38–47.8 Diospyros+Euclea BasingerandChristophel(1985)
Dichroabornensis 29.4–27.4 Hydrangeamacrophylla+Dichroa SchenkandHufford(2010)
Empetrumsp. 16–11.6 Empetrumeamesii+E.sibiricum Schweryetal.(2015)
Giliseniumhueberi 42–46.2 Ipomopsis+Phlox Lottetal.(1998)
Gordonia/Gordoniopsis/Andrewsiocarpon 38–47.8 Camellia+Polyspora GroteandDilcher(1992)
Hironoiafusiformis 80–90 Nasa+Nyssa SchenkandHufford(2010);Xiangetal.(2011)
Klaprothiopsisdyscrita 45–15 Kissenia+Nasa Poinaretal.(2015)
Lyoniasp. 16–11.6 Lyoniafruticosa+L.ovalifolia Schweryetal.(2015)
Lysimachiaangulata 33.9–28.1 Trientalis+Lysimachia Boucheretal.(2016)
Paleoenkianthussayrevillensis 89.8–93.9 Cyrilla+Pyrola** NixonandCrepet(1993)
Parasaurauiaallonensis 72.1–83.6 Actinidia+Roridula** Kelleretal.(1996)
Pouteriacostata 20.4–28.1 Sarcosperma+Planchonella Bartishetal.(2011)
Primularosiae 16–11.6 Primulamaedia+P.sieboldii Boucheretal.(2016)
Raritanifloraspp. 89.8–93.9 Arctous+Clethra Crepetetal.(2013)
Rehderodendronstonei 56.0–47.8 Rehderodendron+Styrax Fritschetal.(2015)
Rhododendronnewberryaianum 55–56 Rhododendrongroenlandicum+R.redowskianum** CollinsonandCrane(1978)
Richeaphyllumwaimumuensis 28.1–16 Dracophyllum+Sphenotoma Jordanetal.(2010)
Schimananlinensis 11.6–5.3 Schimasinensis+S.wallichii Lietal.(2013a,b)
Symplocospseudogregaria 37.8–33.9 Symplocoszizyphoides+S.povedae Fritschetal.(2015)
Symplocosquadrilocularis 56.0–47.8 Cordyloblaste+Symplocos Fritschetal.(2015)
1897). 2.4. Diversificationanalyses
Oneunresolvedissueincodingwastheabsenceofmoleculardata
forseveralcladesofPentaphylacaceae.TheseincludetheAfricangenus We utilized BAMM version 2.5.0 (Rabosky, 2014; Rabosky et al.,
Balthasaria, African species of Ternstroemia, and the endemic New 2017) on our ML tree to examine the location and timing of shifts in
GuineanArchboldiodendronandAdinandraforbesii(Barker,1980).Inthe Ericales.BecauseofthelargesizeoftheasteridssistertoEricales,we
case of Ternstroemia, only two species are present in Africa and were discardedalloutgrouptaxa.AsourMLtreeonlycontainsaboutathird
hypothesizedbyKobuski(1961)tobecloselyrelatedtothenumerous ofthespecies diversityinthe order,we provided BAMM with a sam-
Asian and South American species in the genus with no further hy- pling fraction file. We assigned tips to groups in the fraction file fol-
pothesesontheirrelationships.TheDNAofBalthasaria(Melchiora)has lowingathoroughsurveyofthetaxonomicliteraturewithaparticular
neverbeensequenced.ThephylogenyofLunaandOchoterena(2004) focus on monographic treatments and paying close attention to syno-
suggestsstrongtopologicalconflictbetweenmolecularandmorpholo- nymy at the generic level and the probable placement of genera for
gicaldataandthusBalthasariacannotbeconfidentlyplacedbasedon whichnogeneticdataexists(Supplementary Table3ofAppendixA).
morphological data. Barker (1980) suggested a close relationship of Groupassignmentinthefractionfilewasasdetailedaspossible(gen-
Adinandra forbesii to Indonesian species with glabrous ovaries. How- erally genus level) and we used the following procedure: (1) We ex-
ever, these species are absent from the phylogeny. Based on mor- amined the topology of our ML tree to determine where genera or
phology, Luna and Ochoterena (2004) found Archboldiodendron to be subgenera were monophyletic, paraphyletic or polyphyletic. (2) We
sistertoAdinandra.However,Adinandraisnotmonophyletic(Wuetal., referencedthetaxonomicliteraturetofindmonographictreatmentsfor
2007).BecauseitisalsopossiblethatArchboldiodendronmaybenested eachgenusorsubgenus.(3)Incaseswherethegenusismonophyletic,
in Adinandra, it is hard to place this genus in the phylogeny without assignmentwasstraightforward.(4)Ifagenuswasparaphyleticornot
molecular data. Therefore, the range of areas represented in Penta- broadly polyphyletic, we assigned a number to that genus, plus any
phylacaceaeisnotcompletelyrepresentative,butitislikelythatthese generaembeddedwithinit.(5)Incasesofbroadpolyphylyofagenus
missingcladesarerecentinorigin. or in cases where a family or subfamily was missing genera, we as-
We performed biogeographical ancestral range (AR) estimation signed a species number to that entire clade. Following our through
(ARE)analysisonourbestMLtreeusingtheRpackageBioGeoBEARS searchofmonographictreatmentsforindividualfamiliesandgenera,a
(Matzke, 2012, 2013). As Ericales is sister to a clade ofcosmopolitan total of 12,520 species of Ericales are recognized, although specific
asterids, we excluded all outgroups for the biogeographical analysis. numbers for some families or genera are estimates due to taxonomic
Weperformedastratifiedanalysisusingthesamedispersalprobability uncertainty (e.g., Sapotaceae, Govaerts et al. (2001); Impatiens, Yu
assumptions andtimeperiodsasin Bergeretal.(2016),allowing an- etal.,2015).
cestorstooccupyuptofourareas.Specifically,weemployedtheDis- PriorsforBAMMweregeneratedusingtheRpackageBAMMtoolsv.
persal,ExtinctionandCladogenesismodel(DEC)(ReeandSmith,2008) 2.1.6(Raboskyetal.,2014).WeranfourMCMCchainsfor100,000,000
with and without jump dispersal (j parameter in the BioGeoBEARS generations with parameters logged ever 2,000 generations using the
supermodel; Matzke, 2012, 2014). The j parameter allows for a generatedBAMMpriorsand1expectedshift.Allotherpriorswereset
daughter lineage to occupy a newarea thatis different from the par- to their default values. Chain convergence was assessed using the R
entallineage.Aswewerealsointerestedinthelocationandprobability packagecodav.0.19-1(Plummeretal.,2006).Afterremoving25%of
ofparticulareventsoneachedgeofthephylogeny,weconducted100 generationsasaburn-in,weutilizedBAMMtoolstocomputethe95%
replicates of biogeographical stochastic mapping in BioGeoBEARS credible speciation rate shift configuration using a Bayes factor (BF)
(Matzke, 2016). All input files for BioGeoBears are available via criterion of 6 with the expected number of shifts set to 1. A large BF
MendeleyData. indicatesstrong evidenceforashifton agiven branch.Weestimated
63
J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
thespeciationrateshiftconfigurationwiththehighestposteriorprob- suggestArbutoideae+Monotropoideaeissistertotheremainderofthe
abilityafterexcludingallnon-coreshifts.Inaddition,weexaminedthe family, excluding Enkianthoideae (BS=98, PP=1.0), with the
diversification metrics of speciation rate, extinction rate, and net di- Pyroloideaeweaklysupportedascomprisingacladewiththeremaining
versification rate for individual families as well as subfamilies in Eri- subfamilies (BS=65, PP=0.62). Vaccinioideae and Styphelioideae
caceaeandPrimulaceaeusingthe“getCladeRates”functioninBAMM- form a clade (BS=87, PP=1.0) sister to Harrimanelloideae. These
tools.AllinputfilesforBAMMareavailableviaMendeleyData. threesubfamiliesareinturnsistertoCassiopoideaeandEricoideae.As
Toexamineiftherehasbeenatree-wideshiftinspeciationand/or mentioned above,withinEricoideaetheplacement of Bryanthus isto-
extinction rate through time, we also used the CoMET model as im- pologically discordant between theMLandBIresults. In theML ana-
plementedintheRpackageTESS(Höhnaetal.,2016;Mayetal.,2016). lysis it is sister to Ledothamnus (BS=72), while in the BI results it is
TheMCMCwasconductedforamaximumof20,000,000iterationsand sister to Daboecia+Calluna + Erica but with no support
aburn-inof5,000,000iterations.Becauseourtreeisnotfullysampled, (PP=0.0035).
wesetthesamplingprobabilityto0.363(4,543/12,520spp.).Allother Our treePL chronogram (Fig. 3, Supplementary data 3) places the
priors were set to their default values. After the analysis finished, ageofthecrownofEricalesat∼110Mya.Rapidcladogenesisalongthe
parameter convergence was assessed using coda. As with the BAMM backbone of the order occurred between 106 and 104Mya. By
analysis,BFthatexceeded6wereinterpretedassupportforatree-wide ∼83Mya stem lineages of all extant families had originated, but fa-
shiftindiversificationrates. milialcrownagesarehighlyvariable,rangingfrom∼95Mya(Penta-
phylacaceae)to∼11Mya(Fouquieriaceae).Rapidcladogenesisisalso
3. Results found within balsaminoids with a crown age of ∼82Mya and diver-
gence date for Tetrameristaceae and Balsaminaceae at ∼81Mya. Le-
3.1. Phylogeneticinferenceanddivergencedates cythidaceae and Mitrastemonaceae diverged ∼104Mya. Crown po-
lemonioidsdatesto∼99Mya,withcrownPolemoniaceaemucholder
The best ML tree from the analysis of our supermatrix of 49,435 than crown Fouquieriaceae (∼54Mya and ∼15Mya, respectively).
alignednucleotides(87.6%missingdata,varyingfrom26.8%to99.5% WithinPolemoniaceae,subf.Acanthogilioideaeisrecoveredassisterto
perlocus;SupplementaryTable2ofAppendixA)withthreegenomic the remainder of the family (BS=84, PP=1.0). Crown primuloids
partitionsresultedinafullyresolvedtreeoftheorder(Fig.2,Supple- datesto∼102MyawithaPrimulaceae/Ebenaceaedivergencedateof
mentarydata1),albeitwithverypoorsupportforsomerelationships. ∼80Mya.CoreEricalesbegantodiverge∼104Myafollowedquickly
Our results largely recapitulate those of Schönenberger et al. (2005). by the divergence of crown theoids at ∼102.2Mya and crown styr-
ThetopologyoftheMCCtreefromourBIresult(Supplementarydata2) acoids+sarracenioids + ericoids at ∼101.6Mya. Crown styracoids
isidenticaltotheMLtreeforallmajornodes,withtheonlytopological date to ∼99Mya with the divergence date of Styracaceae/Diapensia-
differences being found within families, especially where branch ceae at ∼93Mya. Crown sarracenioids date to ∼93Mya with an Ac-
lengths are small. These topological differences are the placement of tinidiaceae/Roridulaceae divergence date of ∼80Mya. Divergence
CyclamenwithinPrimulaceaesubf.Myrsinoideae,relationshipswithin between ericoid families occurred between ∼98 and 91Mya, with
Sapotaceaesubf.Chrysophylloideae,placementofFrankliniarelativeto crownEricaceaedatingto∼91Mya.
Gordonia and Schima in Theaceae, and placement of Bryanthus in Eri-
caceae. Though the topology is identical between the two optimality 3.2. Historicalbiogeography
criteria,lowsupportvaluesforthesebranchesindicatethattopological
uncertaintyaroundseveralnodespersists,butforfewernodesthanin We were able to automatically and confidently score geographic
previousstudies. ranges for 3,875 tips, with an additional 333 tips scored manually.
Werecoverbalsaminoidsastheclade(BS=99,PP=1.0)sisterto Basedon alikelihood ratio test,theBioGeoBEARS DECjmodelofan-
the rest of Ericales (BS=95, PP=0.99). Relationships within balsa- cestral ranges (lnL=−5709.69) was a significantly better fit for the
minoids remain unclear, with either Marcgraviaceae or data compared to DEC (lnL=−5772.72) based on a likelihood ratio
TetrameristaceaesistertoBalsaminaceae.BothourBIandMLanalyses test(D=126.06,P=0.0).Sincejumpdispersalisanimportantfacetof
suggest the placement of Marcgraviaceae as sister to the remaining thehistoricalbiogeography,subsequentdiscussionwillonlyinvolvethe
balsaminoidfamilies(BS=53,PP=0.29).Thenextcladesistertothe model with this parameter (Fig. 4; Supplementary Fig. 1 ofAppendix
remainingEricalesiscomprisedofLecythidaceae+Mitrastemonaceae A). Parameters of the DECj model include anagenetic dispersal rate
(BS=62, PP=0.54), with the monophyly of the rest of the order d=9.77×10−3, extinction rate e=3.64×10−5, and cladogenetic
moderately to weakly supported (BS=58, PP=0.90). Monophyly of dispersal rate j=5.91×10−3. Biogeographical stochastic mapping,
LecythidaceaereceivesfairlyweaksupportintheMLanalysis(BS=77, given the parameters of our DECj model, indicates that of 4,207 cla-
PP=1.0). The next clade we recover is the polemonioids (BS=98, dogenetic events, 84% are sympatry, 10% are subset sympatry, 3.5%
PP=1.0),whichissistertoamonophyleticbutweaklysupportedcore are vicariance, and 2.7% are founder-event dispersals. However, the
Ericales(BS=50,PP=0.69).WithincoreEricales,theprimuloidsare relative contribution of vicariance and dispersal to the biogeographic
recovered as monophyletic but with weak support (BS=59, history of the order is not uniformly distributed through time, with
PP=0.69) and are sister to the remainder of the core Ericales vicarianceplayingamuchmoreimportantroleearlyoninthehistory
(BS=34, PP=0.69). Within this remaining core Ericales, mono- oftheorder,withdispersalonlybecomingimportantinthelast30My.
phyletic Pentaphylacaceae (BS=93, PP=1.0) and Theaceae Withinthelast30My,however,bothprocesseshavecontributedtothe
(BS=99, PP=1.0) form a grade with the remainder of the core historicalbiogeographyofthefamily(Fig.5).
Ericales (BS=75, PP=0.69 and BS=42, PP=0.69, respectively), While probabilities for individual areas of combinations of areas
withTheaceaemorecloselyrelatedtothestyracoids,sarracenioids,and werelowforthebasal-mostnodesofEricales,manyofthesenodeshave
ericoids. relativelyhighprobabilitiesforanAREcontainingtheNeotropicsand/
Styracoids are monophyletic (BS=83, PP=0.98) and sister to or Indo-Malaysia. Crown Ericales originated in a shared Neotropical
sarracenioidsandericoids(BS=93,PP=1.0).Likewise,sarracenioids +Indo-MalaysianAR(P=0.29)withallotherpossiblerangeshavinga
aremonophyletic(BS=78,PP=1.0)andsistertoericoids(BS=75, smallprobability.ThebackbonenodesofEricalesarereconstructedas
PP=1.0). Within ericoids, Clethraceae and Cyrillaceae form a grade remaininginthissharedARorswitchingtosolelytoaNeotropicalAR.
sistertoEricaceae,withCyrillaceaemorecloselyrelatedtoEricaceae. Balsaminoids originated in this shared Neotropical+Indo-Malaysian
However, monophyly of Clethraceae (including Purdiaea) is question- AR, (P=0.55) and shifted to an Indo-Malaysian AR along stem
able(BS=71,PP=0.67).WithinEricaceae,sub-familialrelationships Balsaminaceae. Mitrastemonaceae+Lecythidaceae most likely
64
J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
Clade
balsaminoids
Ebenaceae 1 1 1 RhoR1dhMoodedRenonhzddioeerdnsoodinadr oipemnnil podcesrEaodammnittp udsemcethlrauavmtaicy nuiimgrum
eLreiccyotihdisdaceae 1 1 Ceratiola e1ricoides EricEar isciac ucalarnea Calluna vulgaris
Mitrastemonaceae 1 1 0.98 Kalmiopsis leachiaPnhaylDloadbooceec iaal ecuatnictaaBbrryicaanthus gmelinii
Pentaphylacaceae 1 1 1 Kalmia EapnRigghuaosedtaoif torheliapamennsus chamaecistus
polemonioids 1 Elliottia bracteCaBatasesjaioripae a leysctoupaondsioides
Cassiope fastigiata
Primulaceae 11 11 GEaGuubaltuohltetrhryieasr pirCaarh codaecummummaoiecsbdoaealnapshne calyculata
Sapotaceae 1 1 LeucotZheoneo abxiail lpaurilsverulenta
1 Andromeda polifolia
sarracenioids 1 1 Vaccinium VVmaayccrcctiiinlnliuiuusmm mcoarcyrmocbaorspuomn
styracoids 10.980.98 AgPaierrisista f oprompousliafoliaVaccinium uliginosum
1 Lyonia ligustrina
Theaceae 1 1 OxydenDdrraucmo pahrbyloluremu mpatens Acrothamnus hookeri
Harrimanella hypnoides
1 1 Pyrola picta
1 Pyrola elliptica
1 Chimaphila umbellata Moneses uniflora
1 1 1 ComarostaphAyrlcisto asrtbaupthoyildoess uva−ursi
1 1 Arbutus un1edo0.98 Allotropa virgata MoMnootnrootpraosptaru hmyp houpmitiyles
1 1 EEnnkkiiaanntthhuuss cchaimnepnasniuslatus
Cyrilla racemiflora
1 Clethra barbinervis
Clethra alnifolia
1 1 1 1 11 SaCulerAamSuAcaaticauitnto riyinacdauliiedsaitaii chak Pla roeaauelpr orglrdamouisastiiakeoataca lnaudtaans
1 Roridula gorgonias
1 1 1 RHoerliidamu1lpaS hadorerrnaact ametnaiSniaao rarrlaactaenia purpurea
Darlingtonia californica
1 10.95 HPalteesroias ctyarraoxlCi nhhaisapnigdiuosstyrax dolichocarpa
1 1 11 BruiSnHtsAyumlrnoaiidaxpe hsonytfdyflilrrcuaoimcnnoa bfilodiisaretrsuisnteaitum
0.98 1 1 1 SSymympplolocSoctosSy syrz amibzxo1yp jgplaoohpctooeoinndsis ecpisusasniculata 1 1 ShortiaD uinaipfSleoncrhsaiizaoG lcaaopladpxoo nnu irsccoaelodlaantaelloides
Cordyloblaste pendula
1 Camellia japonica
1 Cam1ePlPliyayr reseninnaaerrinaias m isspicercotcaabriplias
1 Polyspora axillaris
1 1 FrSanchkliimniaa saulaptearmbaaha
G1ordonia lSatseiwanatrhtiuas pteropetiolata
Stewartia pseudocamellia
1 11 EuryEa uermyaa rjgapinoantaicaEuryodendron excelsum
1 1CCleleyyeerraa p jaacphoynpichaylla
1 1 Ternstroemia impressa
1 TernPsetnrotaepmhiyal agxy meunraynotihdeersa
1SSllaaddeenniiaa cinetleagsrtirfiofolilaia
11 1 MyMrsyirnsein see agfuriicnaiina Aegiceras corniculatum
1 1 Lysimachia vuAlrgdaisriisa crenata Anagallis arvensis
Anagallis tenella
Cyclamen purpurascens
1 1 1 1 1 1 PCriomrtuuSlsaoa lm dmaeanaOtdetlihmlaaiop alhilPparliionmgauralam emlaat idoerlavayi
1 1 Samolus valeranSdaimolus repens Douglasia beringensis
1Maesa japonica
1 1 1 1 DiosMpaDyDeriDsooioiassos p ssfpyeapyrrlyorricoersoias fslo ov lktiiauragskiiniana
1 1 EucleaR coryisepnaa lycioides
1 Lissocarpa guianensis
Lissocarpa benthamii
1 ChromPooluucteurmiaa e ruugberinflioifroalia
Pouteria campechiana
1 CChrhyrsyospohpyhlylullmum im oplievrifiaolreme
1 Micropholis venulosa
Amorphospermum antilogum
1 1111 PSaylMnasqMaeudapihnuauimllukc aamfor m ardm izucaolrcposioafpitnchauuymlmla
1 1 Monotheca buSxidifeorloiaxylon salicifolium
SarcosEpbeerrmhaa rldatuiari nauumrata
11 101.98PoPleomle1omnoiunmiu mpa cuaceifrluolreuumLmina1nthPuGhsly odmxic nphoioPlsothtoselmaorixus sdpraurmvumlaoLnedpiitosiphon nuttallii
1 1 1 1 1 11 1 Gilia cAalIlppoioptLamhLtayaoonNlelpguasslvmeoiasli isr gaari ieagglit golmiaarind aeidentgtsutahelteorawtsesaxitia
Aliciella tenuis
1 1 Cobaea scandBenosnplandia geminiflora
1 Acanthogilia gloriosa Cantua buxifolia
1 FoFuoquuqiueireiari ac ofalusmcincaurliasta
Fouquieria splendens
1 Lecythis corrugata
1 1 1 Couroupita guianBeenrsthisolletiaE sLecxehccweylteshiailse rzaa sbaugcoatjioana
1 1 Barringtonia asiatica
NapoleonPalaenac vhoogneiali ivalida
Mitrastemon yamamotoi
Impatiens repens
1 Impatiens auricoma
1 1 ImpatieInmsp caatpieennss insoli−tangere
Hydrocera triflora
1 Pelliciera rhizophorae
1 1 NMoraarnctgeraa vgiuaisatnruenms imsixtum
Marcgravia rectiflora
Fig.2.Bestmaximumlikelihood(ML)phylogramofEricalesprunedtomatchthetaxonomicsamplingoftheBayesiananalysiswithmajorcladescolored.Thickenedbranchesindicate
MLbootstrapvalues>70.Bayesianposteriorprobabilities>0.95areindicatednumericallyabovebranches.NotethattowardthetipsMLbootstrapvaluesmaybelowbecauseof
pruning.(Forinterpretationofthereferencestocolourinthisfigurelegend,thereaderisreferredtothewebversionofthisarticle.)
65
J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
Clade
balsaminoids
EeLMPpPSssTatrheoebariyiitrcnelpcemrreryaotanoaamautcsciatchdpaletooceaieshcadenincmdeyeaaiieaosolceoaaeiiecenddaaassecc98ee.2aaee93.99920.5 84.88832.3.8 79.576.97764.771.7 67666.7796..33.965.366226..431.359.3 5545.6 4466..5344.544 32.4 28.6262.52.3 212.3109.2.11688.1.437.2151.414131.133.392..3.219111111.0..6144.09.177..99 45.3 DLGDGGGVUCVLOHCBKLBDEEEERRCPECCLMRRRRCASSSSPCCCMAAARyaaeeerrrmynaaaaueritaaaaahrhyhlhhhllllrrrochaaaxaeopieeeeliiicabboyccudbruuuuvjrslbrkfrteoccciuuuyoooouronnampmtttolmtiadtcriuuccnicoeesirrrryyoaaadhhhndlllddddloldozdioraenlottttlaaaaiiittmotintiaci aaeiaeiarrriannohhhoooohnosauuuaotnhatatcaeduuuutpaaap dort crrpn ehtiideeeddddeid anlcssp rotea soroiiiiiuuhuia laaomisirhahdbaaaaarrrmradmciueeeeeneo tlsmeaoicpa gypmmm xuiiiiligha u iromacnnnnnnegsaaaeasiha ilnprfppslcaleeuhaunpmca eonueaseslrlu d dddd ld ot ficueeoi uxroaglcaaldwapsymmerzaettaeurns mttuaadrrrrrarreahoirmuqtviltaomrrtnontlmaorrd roooooocg cys aanpi iorrimeab rbomiarpramuinxhetrosmaooaicnnnnnnoan orftni aeusemsaoinrycgmhilreedfoyrpaceypn nesbnois n llgsriiiurbarppeszuidynspuiiocrenhanrcuaupafieeqrenisiiomamioslsocoayasenfvrcnatygsalrrulldiuiolixaiaaeasrelinalsaypioaleilceenabaaimoeellsiinunxna−ltuiaianafnrtineoufwiudriteddaguiclrgcsneaacimomenesoeirduaiesgsunsrssuskncemuruomaiiimisislsasltiiidusnipemuesms
1041.0931.105021.2.699.3 95.19933..42 88 79.758.1 72.1 70 66.7 63.1 596.9057.65653.511.955014.394.834.75.4864.45.34344.522..5540.738.738 3433.336..9930.92288.29.6722.656..8623.822212200.0110...669.141.86.9 1155..5513.711.188..977.9 4.9 TVASEEASABCBCPTTCALTMDPASSPDHHFSSPSSRCGSCSSSSSGSPSSSSSSSHHreeeyioeuiymtrtroltttaayyyyytttcycttdrayrolorineeaoaoauaoycisayaoieyyyyyyyiidddrrrsnemhhrrmmmmxmlrdcmlllrmlinrdmmrrolrrannnndyvwbldiirrrrrerrnnrrayliiiidiinsditloiiaauerdiaaaaaaamssssdlaasdaisssepmzeppppspaepaexauyuanhyoiatjommgllxxxxxxxiii eccnoupmatttanaipallnllllll snalsaaallmgalrosanrrroialoooooueyi aaneeoe clonlappiithi aoeartobgpooo ndctaimaa ie aamaicnscccccrigp onnodab noocs wrta lyhhraajnberlheeedcrca nr oiploooohoeeaalugnmiinrdlaal taodncji eal adioonmmmaeiaaairecaaaba reolamfc absssse staaseknr seearacbo irtcvufaorrsz ah liusdpogomxanau r eue po iiigisrlnirpaanld saenhpnahouoencsniaaaclliantrarweu eorrlrp scnluarcurit eienetciairininbh raaoinin eaasip inphesyabezefnmnanfsinabgwafthibfsebyr luadoeofnnoaahiaoiaoaoointpianiuueoatpaoiinalfirytiisalelrrrailomacllmoiamdgaikllattlntsieatcslpfiuiirialcymdaroiinfascelhufaosasdhreenaniuinsoe blhooaruaanussrthpsariusalarlnreiaisndceruaoiielillptdslmiiieulansidnaaataiashiisuladdaheranlartieentliialocrpanauasaitasltyiaalxusnhmooaisaeisididriaeess
105.61021.030.9 57.1 38 24.1 22001..9541.681.15771..4631.55.1741.3113.42611.239.11100.9.21.8868...99766..9755..846.73.4 SDDDDDDMMDDDDDDDRDDLEPPVMMMMMIPniaaaauiiiiiiiiiiiiiiiioaaaaaaishtooooooooooooooomyllmceyeennnnsaaasssssssssssssssellessuiiiioqqmeolpppppppppppppppnllllanaakkkkscuualyyyyyyyyyyyyyyyabrua aaaaoa iirrrrrrrrrrrrrrrlii puua sanorrrrooooooooooooooomrplaaaaspnymm ndpssssssssssssssssea ecaecis obsc b cyancazofpvarcpcipui lgqeinaoebioirlreaasfrpibaaviaedgedaouuoralrfggnaoint vpayzirniiroe dielmteneccnrsdachdvvraamklsrttnxbearistuilsayoiaaieiealtefsaeiecscftseciaaoeliimtilnlarairraianafoaonannsfligiotrntitoenenrruaniniauailacqarnlrsitseiisavaeaiuuariieitmsasii
30.4 26.62244..43222222.1.513.2228.50001...5944.6 TSSSSPPACEMCMsieyliicuhaiadaddcerccpbrdneeesrbylnurhoircrrasenoaoooruphlogounnixxxchsoprdsadyyyaiionhaea nrlll moooleaf n yiigsuaslnnn ldalgelul a uvctrgclblsi aeoaamrasaoosiaubnnpernir nccle obnehitdtoifrrngosanhlerepoisoeinialrsmihpriroaifsacooyhasuuclliielinimauanermspnease
106.6 58.3 41 28.226.2 2109.2.8 SSPPCoyrihdanuredystreoseorsopxiiapaya hll cuovyamenlmlr u ordpmuxuecy lcmoachsciefiaaiaxcnniuctahmaunmum
45.2 SEIPpoaborlemecrmohosaopprnsdeiitsurima ma atg oc glnaarekuerigrnuianelteunaumsmis
99.4 53.952.1 40.8 20.8 11.2 LFFCCAeoooaccuunabyqqntautuutehhaiiaiee os brrsg uiizcaaiaxla ibcsianfopu odgllcleueliaoannmjrsodinoeasnrasis
110.1 104.8 82.891.781 69.6 64.8 595.995.83.4 54.952.7 49.4464.95.4944.63.5 3355..63 31.832029.93..8258.3 23.22922..55 13.310.5 PPHIIIIIIIIIIIIINBPGCCEMNSMSFPmmmmmmmmmmmmmoeeesaclyaaoaouiaatppppppppppppplntyecrdprrursrrlneciraichtaaaaaaaaaaaaattarortnciroicaooangatttttttttttttnwsdsliihiiiiiiiiiiiiimppevaecttreeeeeeeeeeteeegiieaeoeaaaeoeinrennnnnnnnnnnnnteairaam nvtnornrlasssssssssssssari aea ai tginia gr saoglahsrd dgcvmmafasdnbhureistauy l nltauoahicrtnreoaaoocoimaae omiaaegzi sncmaviasneanlnfry e snlncnoiuvnl oiudinmiepr−aagidostaokdefeaoopteeilltigelemtisufraeelssibinaohrsgahylorisainnaihiglynatnirsraeaanfcoeiticnstlaaaashracitrpmahglorasioahicnneeaasaioernepotanaemealreiuaitnsdecaoisiseiatsiaiss
100 80 60 40 20 0 Ma
Fig.3.ChronogramofEricales.Numbersatnodesindicatenodeagesforeachcladeroundedtothenearesttenthofamillionyears.(Forinterpretationofthereferencestocolourinthis
figurelegend,thereaderisreferredtothewebversionofthisarticle.)
66
J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
Acanthogilia gloriosa
0.51 0.570.53 0.95 0.64 0.56 FFCCIPpooooaouulnbmeqqtamuouueaopiiaee ns brrsiiuiiscuaax am ascinfgpo odcgllleaeuiranenemrsgdunaelatnearusism
0.21 0.52 0.42 00.7.4840.770.47 0.710.44 0.410.403.804.56 0.6 0.0030..799.31960.4300..538810.92 0.613 0.7800.5.7700.4.655 0.550.850.540.506.84 0.4310.900..58084.990.9080.9.0380.79.560600.0..497.271751 0.142 0.9141 SSSDLGDGGGVUCVLOHCBKRRRRCPECCDHHSSRRCASLLBDEEEERMRMAAAyaaeeeaaaaaaynrrrmeritaaaahyeeolhhhhlaocarhhrrraxaaaeopeiliiicabboyccubduuurrurvjrslrllkrtfbeirooooruyuuuoocccnnamiimpolmitrratcriluucciinceoerrrsaariyyndoaaaddddolllllddioddaazioraenlaaaotlatttniittmotinitmmacia aaiieeiannoooonhoohhhccsuuauuoatnahtatcuuuadeutpgp dotr pn crreehtiiddddieddeee llancssp pptroeoa sroiiiiiuuahtuilaaaomisrhihaaaadannbrrrramiueeeeeeono tlsemhhaiocp agypmm mxuiiiiligha u irmiiconnnndnngsnaeaaasiha i looppsrfplcaaaleuhaunpmc aeouneaselur ddddedd l o t ificrroiee uorglcalaapdwsymmarezatetaeurns t mpouaaanadrrrrrrraeahoiumqrltomrrnntotlm arord roooooocg ys uranpi iotrcirmeab rbomirpramuixephhotsreaamooaicnnnnnnon ofrtrai euasemsaorincgmhrilefodyueotprpaceyp nebsino nl llgsiraiurbaszppreudynsptiuicoilprehunanrcuupaieeqrfenisiceioammioslsocayaseonfvrcnahytrgsalrrulldihruoilxiaiaaeasrleeinasaypiroaloeiilceenabaamoeeelllsiinnunxan−ltiuaiaanfadnrtineolufwiudriiteddaguilclrgoccsneaacaimomenesoeirduaaxiesgsunsrssuskncemuaruomaiiimisislsasltiiidusnipemuesms
0.601.57 0.55 0.31 0.68 0.92 0.37 0.730.9 0.61 0.83 0.502.31 00.6.04.454 0.02.8690.350.6141 CSSSSSGSPSSSSSSSHHPCCCtyyyyttttyycttuloalluayeyyyyeeyyhmmmxmmlrrolrtrrrrettrraddiihhhdaaaaaaadzpppsppxiyrrrxxxxxxxaeoailllll laaaaooooou enocnrtobagp cccccraomddcaboctrberlcooohoo agnamreaaldnneaeaosssesstseklnrouoszaxaison r tnirdnpahounsntlvianatel acateiinb aoinaia nieezfnsnatabfn onoynioiaoinepuaoanfiasliimakillsesirlcarfoiudeiouinbuassrsarlsdualltiinaaaaulatetlautalalmoides
0.26 0.52 0.82 0.64 SPCGSotcaoehlmrywdismeaoplrnaloit aiiwraa aj aalm aclplshoiocirnanhyaniiscditahaenulpdshraa
0.67 0.4 0.68 0.5 0.38 0.42 0.37 0.60.52 TTPTVASEFSeeeieiuyldcsarrrnmriannnndnytlsssepeaaahtttanpl norrroe ihooodmaamcyeeer olaoclammmaac ecrudxagiiilaaaaaru rinei pnsmfgwbueootayrrrraoltnaiiaymalfass loopianicliluidaihaerenipnastusnhisaesiria
0.9 0.99 CBCSayolamcnvleaiojlmallui aiesn n pte earbguerrpcaiiafcfontloeldiarauatums
0.210.34 0.30.63 0.43 0.48 00.8.712 0.76 11 0.909.570.7006..97730.970.64 0.48 0.3600.3.9500.5.950000..9.7.34219040.07..62910090...815021217.3320.508.090.9.99880.08.94710.19009..868800..59067.99 1 EASABDPASCALTMDDDDDDMMSPDDDDDDSSSSSPPACEMPPCSLERDDDryiomtrtroiieylruiicyurarinoriiiiiiiiiiiiiihoihyaaisiddaddyoioooooooooooooooiiadddcserccnudmlcbydrmmrrreesnbldeeeesnsssssssssssssssdriiiiiyynlsnlosteurrssmssssooierrcrraepppppppapppppppppeuyuosseonitaengoooolaaiii ncpahallnrsyyyyyyyyyyyyyyyasaalalmsooagusnpiiay xxxxaaia elhsoairrrrrrrrrrrrrrr oeli niacpprapsida ansanyyyygp aoooooooooooooooor si ilonlajnh dcahhasarplyn inlrlllleed clusssssssssssssssn uieaoooodleivaiaierc be yycraifi bcaaia sgssab masltennnnvufac yancazaofpvrpcch ulliom lemu eg sireellpoiu r aereenaca ifrpbiaaclviaeruugwedtrgo oscolbnrulrlrrfgsaeiia ridnanhtveppeaasayainryiimombudiaesnaloxneioscbesnrsdlddviaauuakahlasberitixnbpaceaeriyisniutlirsleiaiei ailtmelfmslcccgaileatscfmocobsnefechaiiacoeitlinmislorsaihoihfrnannrafenonagscosaaninsaliltsroeenflipitroienaneenaaiusroeinineiiaiasaixilrsmaacciahrtrsrsiisinitrsdoainfeainasvaaeaucooycitasrruasiiihumcllaiysiieliiumauaonnrmmuispdmeaes bEeLMPpPSssTatrheaoebraiyiitrclnelpcemrrseryaotanoaaamautcsciCatcmhdpaletoocealieshcaaidenincnmdedyeaaiieooasoelceoaaieiiedcenddasaassecceeaaee
0.29 0.26 MITnsihmeabumosbnoaapn sme plaleacr rhraienentrhiriaquesii Ancestral Range
0.71 0.608.505.4 0.56 0.52 0.06.4060.9.5684 0.940.59 0.660.507.608.771 0.39 00..9978 0.760.071.3341 100..2292001.6.053.07.441 0.9109.911 10.804.59 0.821 GCCELMSECMPPPVMMMMIIIIINSFPBPPPHIIIIIIIINSMmmmmmmmmmmmmmeoaaaeeesabiclaaoaaayouiaaaaaatatcpppppppppppppylltlnyecrrreepprdursdnnnnrraalnecciryeaichtaaaataaaaaaaaatarluorrtnhiiiiqqciroilcaoohotnallllngatttttnttttttttwsdasrlikkkkihuuuhiiiiiiiiiiiiimpspevaaeocattrteeeeregeeeeeeeeiiaaaaeiaceiioeaapaeioeinrre dsnnnnnnnnnnnnnuuteoarrrrimdraaam nvtnoernrla aaaaessssasssssssssmmri apeaz tai trgini aaf grn s aioglahsarsdm obsc uafasbdgcvmmdna huriesitayu dlgq nltbiaunoaoahbicrtin rlaeooaocoimsaaea dmotveiaarguuzi ulsncgmnavionsaeoannlfry e o sz anenlncoiumvtenl cloiudiacenmipvra−anmgidostantaokdenfeoaoprteaeiayloltaigelemtkiasufruaec elssibintraohsgahylajordiistailnnaaiirhiogliyrnatoniarseraaannfcnoeiftgeicintstalaasaohracnirptrmaahgelonrliasioahicnnepnleaasuanioeriinepotanaieumheaalmsreiuaitnsdetmiciaoinassiseiatsieaissnse●●●●●●●●●●●●●●●●●●●●IIANNPAAAAIIIANNNAAAMMMMnTTTTTTaueAAAeTfdr l aos ++++o eo++++++++++rtt at −r rtANNP rIIANPIPiarNNPoMMMMoAcAcAATAATlApATp a ta( ++iiis+Nlccc ai APs AsaNy(A P A s)(T((NAAAiaT)TA ()))IM)
●IM + NT + PA
●AT + IM + NA + NT
●IM + NA + NT + PA
100 80 60 40 20 0 Ma
Fig.4.Mostlikelyancestralrangeformajorinter-familialandintra-familialcladesofEricalesbasedonourDECjBioGeoBEARSmodel.Geographicareasasdefinedinthisstudyare
indicatedonthemap.Circlesatnodesindicatethemostlikelyancestralrangeofthemostrecentcommonancestorofthatclade,withtheprobabilityofoccupyingthisancestralrange
indicatedwithineachcircle.(Forinterpretationofthereferencestocolourinthisfigurelegend,thereaderisreferredtothewebversionofthisarticle.)
originatedintheNeotropics(P=0.71)withdispersaltoIndo-Malaysia also likely. Primuloids originated in a shared Neotropical+Indo-
along stem Mitrastemonaceae. Crown Lecythidaceae originated in a MalaysianAR(P=0.30),althoughaNeotropicaloriginisalsopossible.
shared Afrotropical+Neotropical AR (P=0.58). Polemonioids likely StemSapotaceaeoriginatedinIndo-Malaysia,anARthatthecrownof
originated in the Neotropics (P=0.51), although a Nearctic origin is thefamilyalsooccupied(P=0.64).CrownEbenaceae+Primulaceae
67
J.P.Roseetal. Molecular Phylogenetics and Evolution 122 (2018) 59–79
Fig.5.Histogramofthetemporalcontributionof
founder and vicariance events to the historical
biogeographyofEricalesasindicatedbasedon100
stochasticmapsonourDECjBioGeoBEARSmodel.
60
Eachbincorrespondstoa5Myinterval.Notethat
alljumpdispersaleventshaveoccurredwithinthe
last30Mya.
40
s
nt
e
v
e
of event type
ber fvoicuanrdiaenr c(ej) (v)
m
u
n
20
0
(cid:237)(cid:20)00 (cid:237)(cid:26)5 (cid:237)50 (cid:237)25 0
time before present (My)
occupied the Neotropics (P=0.63). Core Ericales, crown though speciation rate has increased at a more uniform rate through
Pentaphylacaceae,andcrownstyracoidsalloriginatedinIndo-Malaysia time, with a particularly sharp increase in the last ∼10Mya. Unlike
(P=0.61,0.67,and0.55,respectively). speciation rate, extinction rate in the order increased markedly at
Starting with the origin of sarracenioids, styracoids, and ericoids, ∼65Mya with an additional increase ∼20Mya. Extinction rate also
theNearcticbecameamuchmoreimportantgeographicregioninthe increasedsharplyatthistime,butdecreasedbetween∼35and20Mya.
historical biogeography of Ericales. Diapensiaceae+Styracaceae ori- BAMManalysessupportadiversity-dependentspeciationprocesswitha
ginatedintheNearctic(P=0.31).Crownericoids+sarracenioidsand mean speciation rate of 0.25 spp./My and a mean extinction rate of
crown sarracenioids originated in a shared Nearctic/Indo-Malaysian 0.09 spp./My. Within individual clades (families or subfamilies), di-
range(P=0.42and0.44,respectively).Backbonenodesoftheericoids versification rates vary dramatically. The highest net diversification
as well as crown Ericaceae originated in the Nearctic. While crown rates are found in Ericaceae subf. Ericoideae (0.26 spp./My), subf.
EricaceaemostlikelyoriginatedintheNearctic(P=0.47),anoriginin Vaccinioideae(0.25spp./My),andEbenaceae(0.25spp./My)(Table2).
asharedNearctic+Palearcticrangeisalsopossible. ThelowestnetdiversificationratesareinEricaceaesubf.Cassiopoideae
(0.036 spp./My), Diapensiaceae (0.037 spp./My), Tetrameristaceae
(0.037spp./My),andEricaceaesubf.Monotropoideae(0.037spp./My)
3.3. DiversificationwithinEricales (Table2). Of the70 shifts in thebest shift configuration, all are con-
finedtowithinfamilies
OurBAMManalysisdetectedbetween60and105shiftsinspecia-
OurCoMETanalysis(SupplementaryFig.3ofAppendixA)suggests
tionrateinEricales.The95%crediblesetofspeciationrateshiftsin-
there is weak evidence (BF between 2 and 6) for tree-wide shifts in
cluded 477 distinct configurations. The configurations with the nine speciationandextinctionratesinEricales.Thefirstpotentialtree-wide
highest posterior probabilities contain between 69 and 81 shifts. The shiftoccurredat∼90Mya(BFof2.0–2.5foradecreaseinspeciation
bestshiftconfigurationofourBAMManalysis(SupplementaryFig.2of
rateandanincreaseinextinctionrate)andasecondtree-wideshiftat
AppendixA)suggestedthattherehavebeen70shiftsinspeciationrate ∼15Mya(BFof3.1–4.4foranincreaseinspeciationrate andande-
throughout the order (excluding the root shift), only three of which
creaseinextinctionrate).
have been decreases. Of these shifts, 56 have occurred since the
Oligocene,∼33Mya(Fig.6).Onaphylogeny-widescale,twopeaksin
the number of speciation events are evident, one 50–45Mya and an- 4. Discussion
other15–10Mya.Examinationofindividualplotsofnetdiversification,
speciation,andextinctionrates(Fig.7)suggeststhatspeciationratehas 4.1. PhylogeneticrelationshipsinEricales
been increasing exponentially since ∼60Mya. Consistent with this,
speciation rate has also increased markedly since this time period, Thisstudyprovidesanew,morefully-resolvedandcomprehensive
68