Maximum likelihood inference implies a high, not a low, ancestral haploid chromosome number in ...

12 Pages·2012·0.41 MB·English

Annalsof Botany109:681–692, 2012
doi:10.1093/aob/mcr302,available onlineatwww.aob.oxfordjournals.org
Maximum likelihood inference implies a high, not a low, ancestral haploid
chromosome number in Araceae, with a critique of the bias introduced by ‘x’
Natalie Cusimano*, Aretuza Sousa and Susanne S. Renner
Department of Biology, University of Munich (LMU), D-80638 Munich, Germany
*For correspondence. E-mail [email protected]
Received:6June2011 Returnedforrevision:26July2011 Accepted:7November2011 Publishedelectronically:30December2011 D
o
w
n
†BackgroundandAimsFor84years,botanistshavereliedoncalculatingthehighestcommonfactorforseriesof loa
haploidchromosomenumberstoarriveataso-calledbasicnumber,x.Thiswasdonewithoutconsistent (repro- de
d
dtruecaitbpleo)lyrpefloeriednyc,echtorosmpeocsioemsreeflautsiioonnshainpdsfianssdiofrneqauseenvceinetssowfidthiffpearertnictunluamrpbreorbsainbialitcileasdne.oLwikaellloihwooredcmonosdtreulscttihoant from
ofancestralchromosomenumbersinanexplicitframework.Wehaveusedamodellingapproachtoreconstruct h
chromosome number change in the large monocot family Araceae and to test earlier hypotheses about basic ttp
s
numbersin the family. ://a
†Methods Using a maximum likelihood approach and chromosome counts for 26% of the 3300 species of c
a
Araceae and representative numbers for each of the other 13 families of Alismatales, polyploidization events de
m
and single chromosome changes were inferred on a genus-level phylogenetic tree for 113 of the 117 genera
ic
ofAraceae. .o
u
†KeyResultsThepreviouslyinferredbasicnumbersx¼14andx¼7arerejected.Instead,maximumlikelihood p
optimization revealed an ancestral haploid chromosome number of n¼16, Bayesian inference of n¼18. .co
m
Chromosomefusion(loss)isthepredominantinferredevent,whereaspolyploidizationeventsoccurredlessfre- /a
quentlyandmainly towardsthe tips ofthe tree. o
b
†ConclusionsThebiastowardslowbasicnumbers(x)introducedbythealgebraicapproachtoinferringchromo- /a
some number changes, prevalent among botanists, may have contributed to an unrealistic picture of ancestral rtic
le
chromosome numbers in many plant clades. The availability of robust quantitative methods for reconstructing -a
ancestral chromosome numbers on molecular phylogenetic trees (with or without branch length information), bs
withconfidencestatistics,makesthecalculationofxanobsoleteapproach,atleastwhenappliedtolargeclades. tra
c
t/1
Keywords: Araceae, Bayesian inference, chromosome evolution, haploid chromosome number, dysploidy, 0
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maximumlikelihoodinference, polyploidy. /4
/6
8
1
/1
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INTRODUCTION chromosome numbers, the ‘Index of Plant Chromosome 8
3
0
numbers’ (http://mobot.mobot.org/W3T/Search/ipcn.html). 7
Chromosome numbers in angiosperms vary from n ¼ 2 Given the incomplete knowledge of angiosperm chromo- by
g
(Tsvelev and Zhukova, 1974; Singh and Harvey, 1975; some numbers, evolutionary changes in chromosome u
e
Sokolovskaya and Probatova, 1977; Erben, 1996) over n ¼ numbers in most clades can only be estimated. Botanists do s
250 (Oginuma et al., 2006) and n¼298 (Johnson et al., this by calculating a so-called basic, or monoploid, chromo- t on
1989) to n¼320 (Uhl, 1978). The range in animals is some number, denoted x, to differentiate it from the haploid 10
A
similar (Crosland and Crozier, 1986; Imai et al., 2002). Such (usually the gametophytic) number n and the diploid (sporo- p
drastic differences in chromosome number, sometimes even phytic or somatic) number 2n. The concept of x goes back ril 2
withinsmallgroups,raisequestionsabouttheevolutionarydir- to Langlet (1927) who explained it using Aconitum as an 01
9
ectionandfrequencyoftheimplieddrasticgenomerearrange- example; if different Aconitum species have n ¼ 8, n ¼ 12,
ments. Cytogenetic studies have shown that chromosome n ¼ 16 and n ¼ approx. 32, their inferred monoploid
numberscanchangeduetofission,fusionorgenomedoubling number x is 4 (Langlet, 1927: 7). Langlet’s idea took off, at
(Guerra,2008),andthereisampleevidencethatsuchchanges least in botany, where thousands of basic chromosome
can contribute to speciation. It has also been inferred that a numbers have been inferred, even for poorly counted groups.
large fraction of all plant species may have polyploid Thus, for flowering plants, Raven (1975, p. 760) suggested x
genomes (Stebbins, 1971; Goldblatt, 1980; Otto and ¼ 7 as ‘characteristic of all major groups of both dicots and
Whitton, 2000; Ramsey and Schemske, 2002; Cui et al., monocots except Caryophyllidae.’ Similarly, base chromo-
2006; Soltis et al., 2009; Wood et al., 2009; Jiao et al., some numbers ofx ¼ 12or x ¼ 5and6havebeen suggested
2011). Chromosome counts, however, exist only for 60 000 forPoaceae(reviewedinHilu,2004)andx ¼ 7orx ¼ 12for
of the 300 000–352 000 species of flowering plants Triticeae (Heslop-Harrison, 1992; Luo et al., 2009). Many
(Bennett, 1998; http://www.theplantlist.org/browse/A/). Most further examples of divergent base numbers having been cal-
published numbers are listed in an electronic database for culated for a clade could be cited (Soltis et al., 2005; Blo¨ch
#The Author2011.Publishedby OxfordUniversity Presson behalfofthe AnnalsofBotanyCompany.Allrights reserved.
For Permissions,please email:[email protected]
682 Cusimano et al. — Maximum likelihood-inferred chromosome number changes
et al., 2009). Part of the reason why different researchers took into account morphological phylogenetic analyses
arrived at different base numbers (x) has to do with the (Grayum, 1990; Mayo et al., 1997).
unclear definition of x, with some treating it in Langlet’s ori- Molecular phylogenetic work over the past few years has
ginal sense as an algebraically discoverable highest common resulted in aroid relationships at the generic level becoming
factor, others as ‘the lowest detectable haploid number relatively clear (French et al., 1995; Cabrera et al., 2008;
within a group of related taxa’ (Stuessy, 2009: 264; italics Cusimanoetal.,2011).Wehereusethemostrecentphylogen-
ours), and yet others as ‘the haploid number present in the etic analysis of Araceae to inferchromosome evolution in the
initial population of a monophyletic clade’ (Guerra, 2008: family, using the model-based approach of Mayrose et al.
340), i.e. an inferred number, since the ‘initial population’ (2010), in both its ML and Bayesian implementations, the
will not usually have its chromosomes counted. How to latter having the advantage that uncertainty in ancestral state
maketheinferenceisuptotheinvestigator.Zoologists,incon- probabilities is readily quantified. To test the power of their
trast, never became enamoured of the concept of an inferred method, Mayrose et al. (2010) first used simulated data and
D
base number x. then four exemplar plant clades (Aristolochia, Carex, ow
Criteria for inferring ancestral (perhaps no longer present) Passiflora and Helianthus) with relatively densely sampled nlo
chromosome numbers from empirical counts could come phylogenetic trees and chromosome counts. Sampling in ad
e
from phylogenetic analyses, the relative frequencies of differ- these clades ranged from 11 to 100% of the species in the d
ent haploid numbers in various species groups, cytogenetic genera. The Araceae data set analysed here represents an fro
m
work on closely related species or, best, a combination of all entire family that is larger and older by at least an order of h
such information. Data from genomics and molecular– magnitude. This poses challenges that we tried to address by ttp
s
cytogeneticmethods,suchasfluorescenceinsituhybridization experimentally modifying character codings to take into ://a
(FISH)-marking chromosomes, are probably the best way to account uncertaintiesinthelarger generaandthe13outgroup ca
d
search for evidence of past chromosome number changes families. e
m
becausetheycanidentifysynteny,fusionsitesorunusualloca- ic
.o
tions of centromeres, in turn providing evidence for duplica- u
tions, fusions or losses (Bowers et al., 2003; Lysak et al., METHODS p.c
o
2006; Peruzzi et al., 2009). Such methods, however, may not m
Familyand order phylogeny /a
be feasible in large clades or those with few species in o
cultivation. ThephylogenetictreeforAraceaeonwhichancestralchromo- b/a
In 2010, an approach was developed that moves the infer- some numbers were inferred in this study is based on the six- rtic
ence of chromosome number evolution to maximum likeli- plastid marker matrix of Cusimano et al. (2011). Clades are le-a
hood (ML) character state reconstruction (Mayrose et al., named as proposed in that study. We used the ML tree from bs
2010). Mayrose et al. (2010) formulated probabilistic models that study or an ultrametric Bayesian tree newly obtained tra
describing the evolution of chromosome number across a using BEAST v. 1.6.1 (Drummond and Rambaut, 2007). In ct/1
phylogenetic tree. Their approach makes use of branch BEAST, we used the GTR+G model with four rate categor- 09
/4
lengths as a proxy for time and of the frequencies of different ies, a mean substitution rate estimated from the data, and a /6
numbers at the tips and in outgroups to infer transition rates pure-birth Yule model as the tree prior. The GTR+G 81
between the different states. Ancestral chromosome numbers model fit the data best, as assessed with Modeltest (Posada /12
8
have previously sometimes been reconstructed using andCrandall,1998).Theanalysiswas runfor37million gen- 30
maximum parsimony (e.g. Soltis et al., 2005: 178, 298– erations,samplingevery1000thstep.Theburn-infraction,i.e. 7 b
302). Parsimony, however, assigns all state transitions the thenumberoftreestobediscardedbeforerunsreachedstatio- y g
same weight and disregards information contained in phylo- narity,wasassessedusingtheTracerv.1.4.1program(partof ue
s
genetic branch length, which tends to result in an underesti- the BEAST package) and AWTY (Nylanderet al., 2008). For t o
n
mate of the number of transition events. one set of analyses (below), we included only Araceae. For 1
InthisstudyweusetheapproachofMayroseetal.(2010)to another, we included one exemplar each of the other families 0 A
rAercaocnesateru,cat laarngceesatnradl olhdapflaomidilycohfrommoonsoomcoetylenduomnbs.erFsorina ooff0A.0li1smexactaelpetsf(oSrtTevoefinesl,d2ia0c0e1aeo(nTwoafiredlsd)i,au),swinhgicbhrawncahstlheengotuhts- pril 20
mainly tropical family, Araceae have a high number of chro- group used by Cusimano et al. (2011) and had an empirical 19
mosomes counts, with 862 (26%) of their approx. 3300 branch length.
species counted, including at least one species for most of
the 117 genera (Petersen, 1989; Bogner and Petersen, 2007;
Chromosome number coding
Appendix; Supplementary Data Table S1 lists all species
with their n and/or 2n counts and the respective references). Totalnumbers of generaandspecies ofAraceaeweretaken
Two basic chromosome numbers have been suggested for fromthewebsiteCreatingaTaxonomiceScience(CATE;http://
Araceae. Larsen (1969) and Marchant (1973) argued for x ¼ www.cate-araceae.org/) and then updated by the Araceae spe-
7, with higher numbers derived through ancient polyploidiza- cialist Josef Bogner (see Acknowledgements). Of the 117 cur-
tion events or ascending dysploid series. In contrast, Petersen rently recognized genera of Araceae, 29 are monospecific
(1993) hypothesized a base number of x ¼ 14 because 2n ¼ (and hence can be coded unambiguously for chromosome
28isespeciallycommoninthefamily.Theformerhypothesis number), 19 have just two species, 31 have 3–10 species, 25
was put forward without the benefit of a phylogenetic frame- have11–50speciesand13have.50species.Araceaechromo-
work, but Petersen (and also Bogner and Petersen, 2007) some counts were compiled from original literature
Cusimano et al. — Maximum likelihood-inferred chromosome number changes 683
(Supplementary Data Table S1, available online), checking the Zosteraceae n¼6, 9, 10 (numbers from Stevens, 2001
generic assignment of each species against the current classifi- onwards). Those of these families with more than one
cationandforsynonymy.Chromosomenumbersforfourmono- number listed by Stevens were coded as polymorphic in all
typicgenerawerecontributedbyJ.BognerandE.Vosyka(see analyses. The above-described three coding schemes were
Acknowledgements)andarenewlyreportedhere:Filarumman- first run on the phylogenetic tree that included only Araceae
serichense Nicolson (M. Sizemore s.n., voucher in the herbar- and then on the tree that included the 13 outgroups, resulting
ium M), Hestia longifolia (Ridl.) S. Y. Wong & P. C. Boyce in six analyses (labelled A1–A6 in Table 1).
(J. Bogner 3003, M), Philonotion americanum (A. M. E.
Jonker & Jonker) S. Y. Wong & P. C. Boyce (J. Bogner
2911, M) and Pichinia disticha S. Y. Wong & P. C. Boyce Inference of chromosome numberchange
(P. C. Boyce s.n., M; Supplementary Data Table S1). One
For ML and Bayesian phylogenetic inferences of ancestral
genus was coded as unknown (X), namely the monotypic
haploid chromosome numbers, we relied on the chromEvol D
ScOocvhuenorttaetladl,r.ieoTlulhare,phtphyreelsoegcnehcnreeotmiocofsaoBnmalecyshsrisoomfinocswlouhmdiceehss 1wh1aa3vseonfontothtceobd1ee1edn7. upbrocg.craam/provg./1c.2hroofmMEvaoylr.ohstemel)t.aTlh.i(s20im10p;lehmttepn:/t/swewigwh.tzomoolodgeyls. ownload
of chromosome number change (Table 2), two more than e
accepted genera of Araceae, with 112 of them coded for d
haploid chromosome number (Appendix). describedintheoriginalpaper.Themodelsincludethefollow- fro
ingsixparameters:polyploidization(chromosomenumberdu- m
Chromosome numbers were coded in three ways to address h
the problem of genera with more than one chromosome plicationwithrater,‘demi-duplication’ortriploidizationwith ttp
number. First, we coded all reported numbers for each lra;tedmes)ceannddindgy,spclhoriodmizaotsioomne(alsocsesndrainteg,dc)hraonmdotswoomelingeaainr rraattee s://a
genus,regardlessoffrequencyindifferentspecies,butexclud- ca
parameters, l and d, for the dysploidization rates land d, d
ing odd numbers (Appendix, column 5; Supplementary Data 1 1 e
allowing them to depend on the current number of chromo- m
Table S1). This resulted in 55 genera coded as polymorphic. ic
somes. Four of the models have a constant rate, whereas the .o
Our second coding scheme (‘reduced polymorphism’ coding) u
other four include the two linear rate parameters. Both p
took into account the frequency of different numbers and .c
modelsetsalsohaveanullmodelthatassumesnopolyploidi- o
treated the most common as the ancestral state (Appendix, m
zation events. We fitted all models to the data, each with 10 /a
column 7; Supplementary Data Table S1). For example, o
000 simulations to compute the expected number of changes b
Lemnoideae have many different chromosome numbers, but /a
n¼20 is especially common (Landolt, 1986; Appendix, omfaxtihmeumfonuurmbtrearnsoitfiocnhrotmypoessomaelsonwgasesaecthtob1ra0n×ch.higThheer rticle
Supplementary DataTableS1). For generawithnumbers sug- then the highest number found in the empirical data, and the -ab
gesting different ploidy levels, we used the lowest haploid s
chromosome number (e.g. Arum). Polymorphisms could thus minimum number was set to 1. The null hypothesis (no poly- tra
be reduced to two states (chromosome numbers) per genus ploidy) wastested with likelihood ratio tests using the Akaike ct/1
information criterion (AIC). 0
or even a single haploid number, leaving 34 instead of 55 9
Wealsoranananalysis,usingtheinformedpolymorphism- /4
genera with polymorphic numbers. In a third coding scheme /6
coding scheme, but excluding Calla because of its unclear 8
(‘informed’ coding), we took into account molecular phylo- 1
relationships in Araceae (Cusimano et al., 2011). For a final /1
genetic analyses for the genera Philodendron (Gauthier 2
et al., 2008), Biarum and Typhonium (Cusimano et al., sensitivity test, we again used the informed coding scheme 830
but the non-ultrametric ML phylogenetic tree from 7
2010), and assigned the state (chromosome number) found in b
Cusimano et al. (2011) instead of the ultrametric tree used y
the early-branching species to the entire genus. The numbers g
in the remaining analyses. u
thus inferred were compared with those inferred by Bogner e
s
and Petersen (2007). This third approach left just ten genera t o
n
coded as polymorphic with maximally two states (Appendix, 1
RESULTS 0
column 8; Supplementary Data Table S1, Supplementary A
p
gDeantausFoifg2s3Ss1pecainedswSi2t)h.aInfewthcishrothmirodsosmcheecmoeu,ntLsaaznadruinms,ufa- TizheedreinsulTtsabolbetai1n.edTihnethtehrseiex-paanraalmyseetser(Ac1o–nAst6an)ta-rreatseummmodaer-l ril 20
1
ficient phylogenetic information (Matthew Barrett, Botanic (Mc2), with the chromosome duplication rate equal to the 9
Gardens&ParksAuthority,WestPerth;personalcommunica- demi-duplicationrate,wasthebestexplanationoftheempiric-
tion, 2011) was coded as ‘unknown’ (X) because no ancestral al data in all analyses. All analyses rejected the null model of
haploidnumbercouldbeinferred.Inallcases,changesamong nopolyploidywithhighsignificance(P,0.999).Theinferred
character states (i.e. chromosome numbers) were assigned rates of change, chromosome numbers at nodes (and their
equal probability. probability) and numbers of events were similar regardless
The remaining families of Alismatales were coded as of which of the three schemes for polymorphism coding was
follows: Alismataceae n¼7, 8; Aponogetonaceae n¼12, applied. We therefore show the results obtained from
16, 19; Butomaceae n¼7, 8, 10, 11, 12; Cymodoceaceae Bayesian and ML analyses with the most conservative
n¼7, 8, 10, 14, 15; Hydrocharitaceae n¼notably variable; coding scheme, namely the one including all polymorphisms
Juncaginaceae n¼6, 8, 15; Maundiaceae only Maundia tri- andalloutgroups(Table1,A1;Figs1and2).Forcomparison,
glochinoides, no chromosome count reported; Posidoniaceae theresultsfromanalysisA6,withoutoutgroupsandthephylo-
n¼10; Ruppiaceae n¼8–12, 15; Potamogetonaceae n¼7, genetically informed coding (Appendix, column 8), can be
12, 14–18; Scheuchzeriaceae n¼11; Tofieldiaceae n¼15; found in Supplementary Data Figs S1 and S2.
684 Cusimano et al. — Maximum likelihood-inferred chromosome number changes
Resultsfromthesixanalyses(A1–A6)carriedouttoinferchromosomenumberchangesinAraceaeunderBayesianandmaximumlikelihoodoptimizationT1.ABLE Chromosomeno.atAraceaeChromosomeno.rangesat.PP.rootnodeAraceaerootnodeCodingschemeRateparametersEventsinferredwith05 Bayes:Bayes:nnTree:AllRed.BestBest;2ndbest;SumSumdlrmPPPPnPPnPPAnalysisoutgroupspoly.poly.Inf.modelLogLikAICLossesGainsDupl.Demi.ML ++............A1Mc2–21954454593969–9818414314318;01816;0161616–18058–1809++..........A2Mc2–23644789564063–112201151318;02617;0131617–1905110–20085++...........A3Mc2–24574973582057–1201011913918;02619;0121717–1905210–2009+............866–866321059318;03817;031717–19086A4–Mc2–196639915041+..........A5–Mc2–21324324536056–8720989418;04217;0231717–1909+..........A6–Mc2–22244507581054–94409710518;03719;0341817–19085 Onlythebest-fittingmodelsareshown.Tree(column2)referstowhetheroutgroupswereincludedornot;codingschemereferstohowgenerawithpolymorphichaploidchromosomenumberswerecoded.Allpoly.,allchromosomenumberpolymorphismcoded(scheme1);Red.poly.,reducedpolymorphismcoding(scheme2);Inf.,phylogeneticallyinformedcoding(scheme3).Bestmodel,Mc2¼¼rmdl(constantratemodelwithduplicationrateanddemi-duplicationrate;compareTable2);Logarithmiclikelihood(LogLik)andAICscores;rateparameters(chromosomelossrate,.¼¼rmPP.duplicationrate,demi-duplicationrate);frequencyofthefourpossibleeventtypeswithaposteriorprobability()05;haploidchromosomenumberinferredatthechromosomegainrate,PPPProotnodeunderBayesianoptimizationwiththerespective,andundermaximumlikelihood(ML).Thelastcolumnshowsthechromosomenumberrangeinferredfortherootnode,eachwithits. wiwwi[r1iBcp1cw(etdctifgn(acoAbbnaPaSflnntwI1(oAaDtMPdltZnnnhonyhheoaAron1nfhhvrnllnn0r0eaunreo2feuaePoaaiiiriaaoau¼¼newscfeeeoacfo.errmidsddeITTttttmd0..al4pn¼8yetsitmgenddalnns55ngoohhhuhtbttnnenphsaac¼te.u)ptrhe,o-ahrisateimisgt1cemmeooso11bvatectraeereofir,rnthd-hsilo¼ine8rss(hhe(rdbeee(huuu56dersaFnenrdannidtgotoiiee0AdoomsedAtdcAaiden–oowrs((intettmt::cegeglcaui)hee(dngs.(liaessAcrohngtfshs6p.a22hlhmi1lr34niipetsteooiPtahPsmseeyonenet(csea(.oooltaa)cohct199re.p380)glTweymmGT)eniy(shnbhgashmt;nPuPoaliuiurhrrrleb)ni4r).)sTSeiicrensthedotryie.-laiti,oamtd,,yrtntairkeetrrffi.ab¼eaeagtos)1hm((a¼gfgn¼aeoihubp4irpaOiebminihfePlarAPnetaBPsenbnerbcsod)etanrrmeedtllnrriygaldinoeno.roAiogPenmonroao1Ptlersuy,nura10c0ucenbia(daoeouwuddeiuouorlRalistocn7idnpyfIAslDfi)h.)1n.psiailtyodnehendttumpeea12ne2npmpsh;(nilsysrfehlihtah–clsdnomicsnoi1fl6ntoaitdresoret.,4a9ssirsiwczllasataegCbchtdeaarh1e,cuotgnite)r,)te,,meylntif))eiila¼peitaw)dahpr.nreFce.yhr,aaareaw9n.o:t,0amafrl-v.trodeSFtltogerirhhpnga¼eteysrdessbisidIdne.iiohanokeFTeidAnuiet(gtcoe8am1r.itlotoriiyiepuaAuIodetih)ahsienugeelhofdmcfariaipse.nhhnns54Mssnd,nltp1a.tt¼nhnrgeecalTtttm.uoo4,o,psodeg,oyssepsop0ldbthaf1d.fbgn1rwp¼pps,hciLhimwete1ametdonrhaAotbnslLTrrnec1oe–hus3(ohSnstohohewtveiysfr)ootoinu3ioleer0maharnosl5etemaareectleu2rg1ovmy02eeepaleamifhlmr.tptyoenhn.eeyoob(sneon2yomne0h8hri.m)es1nisdnrrmbbrAatnpmloivdr7iomnn-rc.lacsooBnubnrt,eehyo8dn4aeeeioeedtoeulubs7oncoceedc¼Fb2sttolelheloariud5(aew≤cr–,onunspmShttuyeaaoy(ro¼dhPiira)AvifsAa11iyipe.aonPFpntontprnerge0rstuodnm9eirSbrme0oos(o,ecub1olftgh12ofe,nedimlratadc..PbaprigPispih.dnsrfngiwde2muoase.bwz(e(csvit4,lmnF5huterce5piirfeoTsPiornc1or.he6taaaamtearg2¼aarpautadriisragilmlheetnolwc.1tdebyt,Aongofanoronteeosntues1alh¼apayCii(irvtaroehreisb4ei.iim.ndcommdeousosoAngpoir)vSesoes31mtTcwleoodA,atlh.eosdlen,nitpuaideopam1tibna3)h41teyolem2tage0etalhclhacefh,oan]sUurlps5rythfoh(lrsw4annsbl1s)ir.olooisaoaer1eePasaetsase.5finSareooa(osot)ctrlt74ii.dtbisdosnhrn,,toclvfAana.ieisPf)dfccoodtuumpdnlroy/rolnnpeAetoeorc(enwc¼argeAdalh1hee(nsyotpaei30oms0fypccagdghahrrodPungicenA¼na1poram8ito1aemaswe1)nr.mc.odro)lyghoenielt1rSoifg5F()da3ueesrreea6.)ndsu(nolmeeDnfsP.olhigmafsd4l2e,du0ti)7t9e9(dsiocr)ttryrr(uehntgs;rccaeal3Ts.sP1ho,t9rpi.aao9A8r8irioPSaa–e(goea3pr5tphsatghahbrnsi(ncee.attd)aPm.phhm.r..vrovino9ieisrTttPnah07l5slir,3rt11reddfdg5snepnmnihloeesoueoaeaPnoou)rh(b.en;eat68e¼aope4AtncAidmmn¼f(eemmpoFdi0irmwtbgni(d((aA.i.itenFagn¼nnemo2nlhhtavtovuin92sAnnhAAe.il1aesibietvnnooadb9ihuui≥s)g1neaeeee1nmzu0cirtffem¼rt))g¼ret6ed41((pssoy9npemminee0.6chal,b.wwea¼AAv.n08oota,y)b))srrrrhtlatlt./tttraaonahiSaobbiin136oorr.18t6mmPtttAeerrh,ewaijie312nn81n1onsnchahheeeeroonoieettti1a4i22osrr..71rassP))))y4ddh55d5nonoon4gnd6ddeeeeeeaeeeeessrrrr--ft;:;;t.,,.,,,, Downloaded from https://academic.oup.com/aob/article-abstract/109/4/681/128307 by guest on 10 April 2019
Cusimano et al. — Maximum likelihood-inferred chromosome number changes 685
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13 Dracontium 13 c
Podolasia clade0·6 14 14 2·40·80·8 1133 DAGSntroyaanlcopaochtnohytpalilooueipstdo se1niss7 1 11433 adem
n =6 14 13 31120··77000···999 1270 AMAANZCanggeaomullplnaalobhtooiropitiadnhccssoeyhuis rmtal2uic s1r4amad 72 si2 a0 201 0274 ic.oup.co
789111111111012345678 Aroideae 1S41p4a11t4·h12i002c·117a902r·18p1e·9a01·3e7 31271117·11271201071077·118217771·2128010717 CCZPPAFHCLSATSGIMCSDGPBnaauahsnpspyheuoorrioeaceyognertcnicaairlgmraanlelctfpcaoecgotuhaattfnrrgaerhheeatatdnouundondoeoiosdianslereanmmoomcdoosrciunetnblaannaithtrimaoldm i issaiatoa aoddgr11y rh21i cnp e2scyu n2rdr m771e17h11oeaaphn0nm 1r7ui717anos aiaeaa11m 3 sd 121 187211m1i 707x808167 e71 720 cZlaandteedeschia m/aob/article-abstract/109/4/68
13 Piptospatha 13 1
1290 11331313 BSBAucarihcdkeooaptartuha 1mar3ile a1lnl3ad 1ra3 13 /1283
22221234 Philonotion clade 14 14 1·6130·2163·2 1313 JHPSCAPahcmsaasheyplloamiauasrr dlpuma1inohmt8aeado t rrp1o1uah1g3mcaloo ln1ltutt3isisu 1m133 13 07 by gu
2267 14 13132·5139 01··77 UFSCiylaleanlaargurdoumiunm mi1u 74m 1 313 est on
2234589026 14 14112138320184·8211·3318111·93 ZZSCXATAAPooycarrmehoipmmanslltobphpaatiirhrhccohrnooouyaanidssssmtrrorpioppponada naeama1 ot 5tl h42lh1ra16aua7a1 1 1m 1 1133 3456 Typhonodorum 10 April 201
5796 Ambrosina clade 14 104·5 27 27 CCPPiraosorltltlieeaatpr o1uhg4myyt no1en4 2277 clade 9
84 14 14 ACroiolopcsaiss i1a4 14
14 Remusatia 14
14 14 Steudnera 14
Alocasia 14
Events inferred with PP > 0·5 Arisaema 14
1414 1·30·6Pinellia 14
CChhrroommoossoommee gloasisness : : 8 9·48·1 14141414111·6 TSTLayhapzeuahrriorooumnpmihau otm8un4m u1m 31 312
Duplications : 14·3 1144 1·1 HEmeliicnoiudmic e1r4os 14 Areae
Demi-duplications : 14·3 1144 BAiraurmum 1 413
14 Dracunculus 14
FIG. 1. Chromosome numberevolutionin Araceae inferred under Bayesian optimization, with outgroups included and all polymorphic chromosomestates
coded (analysis A1 in Table 1). Pie charts at nodes and tips represent the probabilities of the inferred chromosome number(s); numbers inside charts have
the highest probability. Numbers at the tips are chromosome numbers inferred with the highest probability, i.e. the inferred ancestral haploid chromosome
numberforeachgenus.Numbersabovebranchesrepresenttheinferredfrequencyofthoseofthefourpossibleevents(gains,losses,duplicationsanddemi-
duplications)thathadaprobability.0.5.Thecolourcodingofchromosomenumbersandeventtypesisexplainedintheinsets.
686 Cusimano et al. — Maximum likelihood-inferred chromosome number changes
Potamogetonaceae
10 Zosteraceae
10 Cymodoceaceae
10 10 10PosidoniaRceuapepiaceae
10 Maundiaceae
12 Juncaginaceae
12 Aponogetonaceae
8 Scheuchzeriaceae
Alismataceae
8 8 8 HBuydtormocahcaeraiteaceae
Tofieldiaceae
Gymnostachys
16 Orontium
8 15 15 SLyysmicphloitcoanrpus
Spirodela
Lemnoideae 21 21 LLaenmdnoaltia
Araceae16 21 21 WWoollffffiiealla
Anthurium
Pothoideae 14 1212 PPPeoodtthhicooesidlliaurmum D
Spirodela clade 15 15 15 1144 1154 SHARSHlpthoeleoaoltonestdchorcoohishpsplpeahpsemmyairsltmolyhunsaametion ownload
Rhaphidophora clade 15 330300 MSARcnhoiaanndpsdehtaenipdrdasorupushmora ed fro
30 Amydrium m
True Araceae 15 Lasioideae 11313113331330 UPCPALELaaoynpryosscrdaiptsiinopomarpolhesaaospymstrplehpilnaaurahumtmahmaa https://aca
13 Dracontium d
13 Anaphyllopsis e
14 13 Dracontioides m
Podolasia clade 14 17 ZGSatoymnloaioctohcupaluecstaosn ic.o
Callopsis u
13 AMnounbtriiacshardia p.c
14 20 AAggllaaoodnoermuam om
13 20 20 20 20 PANnseecphuhodthmoyhatyinsdersosme /aob
Aroideae 14 20 20 2120 20 CCPFHuhueorilrmlctcoaaeaddssleooitanimasderonna /article
Sp1a4thica19rpeae 1177117117771117771717 ZATSSGIMCSDGBnaasppyorioeaceonctnaagraanefacgtattfnrrgerhheatouunoeiodianernmmcdsrunenblaaitrldmisiatoaagrhicpscumehaphmuiaaiaamdix Zclaandteedeschia -abstract/109/4/68
Philonotion 1
13 18 CLarygpetnoacnodryrane /12
13 Piptospatha 8
13 Bucephalandra 3
113313 SBArcaihdkooatartuamriella 07 b
Philonotion clade 14 1313 PShchymismataatrougmlottis y g
Calla u
14 13 13 JHAPamsasepoauarrdlpuinohmedorpahcaolnlutsium est on
14 13 13 SCyanlagdoiunmium 1
13 9 UFilleaarurumm 0 A
14 1133 113313 ZZSCXoocahammnloptiirhcchooaaisssrrppppoaaeamttlhlhaaaa pril 201
14 AArmisbarrousmina 9
14 Peltandra
28 Typhonodorum Typhonodorum
28 Arophyton
Ambrosina clade 14 14 27 27 CCPPiraosorltltlieeaatprouhgmyytnoen clade
Ariopsis
1414 14 1144 SRCteoemluodcuanssaeitraiaa
Alocasia
1414 PAirnisealleiama
14 14 TLahzeariroupmhonum
14 Typhonium
14 Sauromatum
14 Eminium Areae
14 Helicodiceros
1144 BAiraurmum
14 Dracunculus
FIG.2. ChromosomenumberevolutioninAraceaeinferredundermaximumlikelihoodoptimization,withoutgroupsincludedandallpolymorphicchromosome
statescoded(analysisA1inTable1).
Cusimano et al. — Maximum likelihood-inferred chromosome number changes 687
TABLE 2. The eight models of chromosome number evolution rearrangements haveoccurred aftergenome doubling,perhaps
implemented in the software of Mayrose et al. (2010), indicating especiallyfollowinghybridization(Hayasakietal.,2000;Lim
the considered parameter estimates (d, l, r, m, d, l), the et al., 2008; Peruzzi et al., 2009; Tu et al., 2009).
1 1
number of parameters included, and, in the case of m, with In general, basic chromosome numbers inferred according
whichcondition to Langlet’s (1927) approach, as the lowest detectable or
somehow calculated haploid number within a group of
Model d l r m d1 l1 No.ofparameters related taxa, will be low, simply because of the way they are
arrived at (see Introduction for Langlet’s original example).
Mc1 + + + – – – 3 For Araceae, the hypothesized ancestral numbers were x¼
Mc2 + + + r¼m – – 3
Mc3 + + + r=m – – 4 14 or x¼7 (Larsen, 1969; Marchant, 1973; Petersen, 1993).
Mc0 + + r¼0 m¼0 – – 2 The present study instead inferred an ancestral haploid
Ml1 + + + – + + 5 numberofn¼16(underML)orn¼18(withBayesianinfer- D
Ml2 + + + r¼m + + 5 ence) and, moreover, an evolutionary trend from higher to ow
MMll30 ++ ++ r+¼0 rm=¼0m ++ ++ 46 ltoowkeerenpuminbemrsi,ndraththeartthnaonnetheofotthheer ewaaryliearrosutunddi.eOsn(eLanreseedns, nload
e
1969; Marchant, 1973; Petersen, 1993) included Lemnoideae d
ratMepcairnadmiceateterss(mdo1,dlel1s).wZiethrocionndsitcaanttesratthees,raenspdeMctilvmeonduelllsmthoadteiln.cludelinear in Araceae, a taxonomic difference that greatly affects the from
range of chromosome numbers found in early-diverging h
clades (Figs 1 and 2). It is also likely that the high frequency ttp
s
of 2n¼28 in the well-counted unisexual Aroideae unduly ://a
duplication event on the branch leading to the Typhondorum influenced the hypotheses about x being 7 or 14. Finally, the ca
d
clade (from n ¼ 14 to n ¼ 28). earlierhypotheses weredevelopedwithouttherelativelycom- e
m
Results of the two additional analyses (inclusion/exclusion plete and solid phylogenetic information that is available ic
of Calla; ultrametric or non-ultrametric trees) did not yield today. .ou
p
results substantially different from those obtained in analysis Nevertheless,anyinferencesaboutcharacterevolutionfrom .c
o
A6 and shown in Supplementary Data Fig. S1. Model Mc2 a taxon sampling of just 112 representatives, however well m
remained the best-fitting model, and chromosome number coded their states may be, must be regarded with caution. /ao
b
reconstructions at nodes and change rates were similar. Every genus with more than one species must have its own, /a
perhapscomplex,historyofcytogeneticchange.Itisalsocon- rtic
le
DISCUSSION ceivablethatdysploidyratesmightchangeindifferentpartsof -ab
thetree(e.g.incladesoftaxalivingindifferentenvironments) s
Theresultspresentedhereprovideanexampleofthepowerof and that relatively derived and rapidly radiating clades, tra
c
ML-based or Bayesian inference of chromosome number perhaps with frequent hybridization, might have different t/1
0
changes. The new approach, which distinguishes (and separ- rates of polyploidization than older, genetically isolated 9/4
ately infers) chromosome gains, losses, polyploidization and groups. The phylogenetically informed coding scheme (our /6
8
demi-ploidization, not only reconstructs numbers at particular scheme three) may be the best way of coding ancestral 1
/1
phylogeneticnodes,butalsoinfersratesofchangethroughout haploid chromosome numbers in larger clades (here genera), 2
8
3
thephylogenetictree.Equallyimportantly,BayesianPPsyield an idea that could be tested by cytological work in small 0
7
a statistically well-understood measure of confidence in the genera with solid phylogenetic hypotheses, such as Arum b
y
results.Mostpreviousancestralchromosomenumbers,incon- (e.g. Esp´ındola et al., 2010). g
u
trast, have been inferred without confidence assessment Giventheinferredhighancestralhaploidnumbers,chromo- e
s
(examples and critical discussion in Soltis et al., 2005). The some fusions (neutrally termed ‘losses’ in the models of t o
n
experiments we carried out with the different coding Mayrose et al., 2010) must have been common during evolu- 1
0
schemes for genera polymorphic for chromosome number tion of Araceae. This hypothesis now needs to be tested. A
p
rneovdeeasl,edaltshuorupgrihsinasgerxopbeucsttendestsheofinthcelusstiaotnesorinefxecrrleudsioatnionfteoriuotr- Ltroarmgeerecsh,rommaoysobmeethseinreAsuraltceoafe,fuwsiiothndbiesttwalelyenposmsitailolneerdmceetna-- ril 20
1
groups (in our case 13 families) affected the number inferred centric chromosomes (Petersen, 1993). If so, one expects to 9
for the basal-most node, albeit only slightly (Table 1). The find interstitial telomeric sites. With probes, using primer
results of the present study further confirm that model-based pairs homologous to the basic plant telomeric repeats, one
chromosome inferenceworks well even with large data matri- can visualize these regions (Ijdo et al., 1991;
ces;thelargestofthefourmatricesanalysedbyMayroseetal. Weiss-Schneeweiss et al., 2004). Such chromosome prepara-
(2010) had 107 terminals, and the present tree had 126. tions are now being carried out in our laboratory on
Chromosome fusion (loss) appears to be the predominant Typhonium species with suspected chromosome fusion (pre-
pattern in the evolution of chromosome number in Araceae; dicted from high or low chromosome numbers in species of
polyploidization events are much less frequent and apparently known phylogenetic relationships).
occurredmainlytowardsthetipsofthetree.However,ancient The results of the present study suggest that quantitative
polyploidization events may be harder to detect than recent methods for inferring ancestral haploid numbers should
ones, because of the genomic restructuring that follows poly- replaceinferencesthatrelyonalgebraicallyfindingthegreatest
ploidization.Onlydetailedstudies,perhapsinvolvingchromo- common factor for a series of numbers or on interpreting the
some painting techniques, will reveal how rapid intergenomic lowest available haploid count as the ancestral condition.
688 Cusimano et al. — Maximum likelihood-inferred chromosome number changes
The new approaches also yield a measure of statistical confi- unravelling its evolutionary history. Botanical Journal of the Linnean
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690 Cusimano et al. — Maximum likelihood-inferred chromosome number changes
APPENDIX
The117generaofAraceaewithnumberofspecies,numberandpercentageofspecieswithchromosomecounts,diploidchromo-
somenumbersandcodedancestralhaploidchromosomenumbersinthethreecodingschemesusedinthisstudy(seeMethods).
X ¼ unknown.
Counteddiploid Reduced
Spp. Spp. chromosome Allpolymorphic polymorphic Informed
Genera number counted % numbers2n¼ n¼ n¼ n¼
1 Aglaodorum 1 1 100 40 20 20 20
2 Aglaonema 23 6 26 14,40,100 7,20,50 7,20,50 20
3 Alloschemone 2 1 50 84 42 42 42
4 Alocasia 107 17 16 24,26.28,40,42,56,68,70, 12,13,14,20,21,28, 12,13,14,20,21,28, 14 D
o
84 34,35,42 34,35,42 w
5 Ambrosina 1 1 100 22 11 11 11 nlo
6 Amorphophallus 196 47 24 26,28,39 13,14 13,14 13 a
d
7 Amydrium 5 2 40 60 30 30 30 e
d
8 Anadendrum 11 3 27 60 30 30 30 fro
9 Anaphyllopsis 3 1 33 26 13 13 13 m
10 Anaphyllum 2 2 100 26 13 13 13 h
11 Anchomanes 6 3 50 40 20 20 20 ttp
s
12 Anthurium 903 171 19 1340,+20B,s2,43,42,63,62,84,02,94,8,49, 7,13,15,17,18,30 7,13,15,17,18,30 15 ://ac
56,60,84,approx.90,approx. ad
124 em
13 Anubias 8 8 100 48 24 24 24 ic
14 Apoballis 12 6 50 26,39,56 13,28 13 13 .o
u
15 Aridarum 10 4 40 24,26 12,13 12,13 12,13 p.c
16 Ariopsis 2 1 50 28,84,86 14,42,43 14 14 o
m
17 Arisaema 150 97 65 20,24,26,28,32,42,48,52, 10,12,13,14,16,21, 10,12,13,14,16,21, 14 /a
56,64,70,72,84,112,140, 24,26,28,32,42,56, 24,26,28,32,42,56, o
b
168 70,84 70,84 /a
18 Arisarum 4 2 50 14,28,42,52,56 7,14,21,26,28 7,14,21,26,28 14 rtic
19 Arophyton 7 6 86 38,40,54,approx.76 19,20,27 19,20,27 19 le
20 Arum 29 26 90 28,29,30,42,56,63,70,84 14,15,21,28,35,42 14 14 -a
b
2221 BAastkeoraostigma 28 22 10205 2364 1137 1137 1137 stra
c
23 Biarum 21 12 57 16,18,22,24,26,32,36,40, 8,9,11,12,13,16,18, 8,9,11,12,13,16,18, 13 t/1
74,approx.96,98,108 20,37,49,54 20,37,49,54 09
24 Bognera 1 1 100 34 17 17 17 /4
25 Bucephalandra 3 3 100 26 13 13 13 /68
26 Caladium 12 6 50 19,22,26,28,30 11,13,14,15 11,13,14,15 13,14 1/1
27 Calla 1 1 100 36,54,60,72 18,27,30,36 18 18 2
8
28 Callopsis 1 1 100 36 17 17 17 3
0
29 Carlephyton 3 3 100 54,108 27,54 27 27 7
30 Cercestis 10 6 60 approx.36,42 21 21 21 by
31 Chlorospatha 28 2 7 26 13 13 13 g
u
32 Colletogyne 1 1 100 44,46,54 22,23,27 27 27 e
s
33 Colocasia 16 5 31 26,28,30,36,38,42,44,46, 13,14,15,18,19,21, 13,14,15,18,19,21, 14 t o
48,52,58,84,116 22,23,24,26,42,58 22,23,24,26,42,58 n 1
34 Croatiella 1 1 100 34 17 17 17 0
35 Cryptocoryne 60 64 107 20,22,28,30,33,34,36,42, 10,11,14,15,17,18, 10,11,14,15,17,18, 17,18 A
p
5940,,5160,2,661,126,8a,p7p0r,o7x2.,18352,88, 2316,,2474,,2485,,3531,,3546,35, 2316,,2474,,2485,,3531,,3546,35, ril 20
36 Culcasia 24 9 38 approx.40,42 21 21 21 19
37 Cyrtosperma 12 4 33 24,26 12,13 12,13 13
38 Dieffenbachia 57 14 25 34,36,40,44,68 17,18,20,22,34 17 17
39 Dracontioides 2 1 50 26 13 13 13
40 Dracontium 24 5 21 26 13 13 13
41 Dracunculus 2 2 100 28,32 14,16 14 14
42 Eminium 9 3 33 28 14 14 14
43 Epipremnum 15 3 20 60,70,84 30,35,42 30,35,42 30
44 Filarum 1 1 100 28 14 14 14
45 Furtadoa 2 1 50 40 20 20 20
46 Gearum 1 1 100 34,68 17,34 17 17
47 Gonatopus 5 4 80 34,approx.68 17 17 17
48 Gorgonidium 8 3 38 34 17 17 17
49 Gymnostachys 1 1 100 48 24 24 24
50 Hapaline 8 2 25 26,28 13,14 13,14 13,14
Continued