Clark (1982), Funk (1981), Humphries (1983), ... They include: R. Jansen, J. Semple, C. Clark, R. Sanders, C. Humphries, H.-E. ...... F. Blake) Clark & Kyhas. -cal.
PHYLOGENETIC
PATTERNS AND HYBRIDIZATION' V. A.
FUNK2
ABSTRACT
Hybridizationis an importantpart of the evolutionaryhistoryof floweringplants. If hybridization has occurredamong the species of a taxon under cladistic analysis the resultsare varied but always data thatobscure the Hybridizationresultsin incongruentintersecting presentadditional difficulties. possible underlyinghierarchy.Guidelines and methodsare examinedfortheirusefulnessin identifying hybridsin a cladistic study. Seven genera are analyzed cladisticallyand the resultingcladograms examined forpossible hybrids.These hypothesesof hybridizationare then compared to otherdata, such as distributionand cytology,to see if the hypothesesof hybridizationare supportedor rejected. it The more hybridsan analysis contains and the more complex the interactions,the more difficult becomes to identifypossible hybridsand theirparents.
ternor hierarchy.The methodof cladistics(phylogenetic systematics)seeks to discover these patternsby groupingtogethertaxa that share apomorphies (evolutionarilynovel, unique, or derived characters).Hybridization,or reticulate evolution, is inconsistentwith a method designed to depict hierarchies.Hybridization is, data intersecting a cause ofincongruent, therefore, that obscure phylogeneticinformation.Cladists have been concernedwiththis problemforseveral years. Most realize that any method that seeks to identifypatternsofrelationshipmustbe able to accommodate hybridizationbecause of its frequency.Workersin the problems of hybridizationand phylogeneticsystematicsinclude Bremer (1983), Bremer and Wanntorp (1977), Clark (1982), Funk (1981), Humphries (1983), Humphries and Funk (1984), Nelson (1983), Nelson and Platnick(1980), Rosen (1979), Wagner (1969, 1983), Wanntorp(1983), and Wiley and Brooks (1982). One favoritemethodofbotanistsin estimating the closeness of relationshipsamong taxa is the percentageof hybridizationin crossingstudies. An importantpoint about such hybridization studieswas made by Rosen (1979: 277): "reproductivecompatibilityis a primitiveattributefor no the membersof a lineage and has, therefore, power to specifyrelationshipswithin a geneaTHE STUDY OF HYBRIDIZATION logical framework."We cannot use the abilityof The basic conceptof phylogeneticsystematics two or more species to hybridizeas an indication (sensu Hennig, 1966) is an ever branchingpat- of close relationshipbecause the abilityis rela-
to overemphasizethe importance It is difficult of hybridizationand polyploidyin evolutionbecause theyare outstandingfeaturesofmanyplant groups. Accordingto some authorities30-80% of the species of angiosperms are polyploids (Goldblatt, 1979; Lewis, 1979; Stebbins, 1974), which allows forthe possibilityof a tremendous amountofhybridization.Of course,thesefigures do not include diploid hybrids.Despite its importance, hybridizationhas been virtuallyignored by those who have dominated the discussion of evolutionarytheory.This is a result,no doubt,ofevolutionarytheorybeinglargelyin the hands of scientistswho workon groupsin which such phenomena as polyploidy and hybridization have a strongrelationshipwithunisexuality and are not consideredimportantin evolution. typesofhybridization.FigThere are different ure 1 summarizes some of the possibilities (a moredetailedexplanationis foundin Funk, 1981) but does not include introgression.For the purpose of this paper it is importantto note that many hybridsare sexuallyreproducingindividdistinctand in some uals and are morphologically manner reproductivelyisolated fromboth parents. Thus, they behave as species no matter whose definitionyou chose to adopt.
I A number of people, who do not necessarilyagree with everything that I have said, have kindlyprovided me withdata and commentson various draftsof the manuscriptand this paper would not have been possible withouttheirassistance.Theyinclude:R. Jansen,J.Semple,C. Clark,R. Sanders,C. Humphries,H.-E. Wanntorp, K. Bremer,G. Nelson, N. Platnick,D. Rosen, and P. Weston. I appreciatethe assistance of B. Kahn in helping preparethe illustrations. Washington,D.C. 2 Departmentof Botany,National Museum of Natural History,SmithsonianInstitution, 20560.
ANN. MISSOURI BOT. GARD. 72: 681-715.
1985.
682
ANNALS OF THE MISSOURI BOTANICAL GARDEN
[VOL. 72
Wagner (1983) has suggesteda method for dealing with hybridsthat he calls reticulistics. This methodworkswithgroupsin whichhybrids are intermediatein characterand progressively [ ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~I II less well with those that are not intermediate. Oftenthehybridsto whichWagnerrefersare F,'s that are being formedcontinuallyand are sexF _A___I ually inviable. Certainlyfor well-definedplant I I groupsin whichthehybridsare intermediateand obvious and are characterizedby beingrareand B eithersterileor polyploids (definition,Wagner, l l 1983: 71), Wagner's method should be considered.These individualsare notunitsofevolution and thusare not species. In thispaper I am conFIGURE 1. Possiblehybrid and polyploidrelation- cernedwithhybridsthat are regardedas evolushipsoftwospecies(A and B) and theirreproductive tionaryunits and that are usually designatedas capabilities (Funk,1981). species, subspecies,or varieties. Theoretically,in cladograms,hybridsshow up tively ancestral, possessed at one time by all by causing characterconflicts;so also do homomembers of the group. In fact,it is the loss of plasies (Fig. 2, character4; Appendix A). One the abilityto hybridizethatis apomorphic. Be- mustbe diligentin tryingto distinguishbetween cause it is never certain that any two taxa are characterconflictscaused by hybridizationand unable to reproduce,whetheror not species hy- thosethatare theresultof parallelor convergent bridize is uninformativein determiningthe pat- evolution. It is advisable to use the cladogram ternof relationship. (developed withthe concept of parsimonyusing Among cladists, three differentapproaches all taxa) to examinetheapomorphiesthatappear have been suggestedfordealingwiththeproblem morethanonce on thecladogram(homoplasies). of hybridization(Humphries & Funk, 1984). Perhaps a closer examination will reveal that Some suggest using the most parsimonious some charactersoriginallythoughtto be apostructures(false cladogram(s)and leavingthehomoplasies (char- morphiesare actually different acters appearing more than once on the clado- homologies) or are combinationsof characters. gram) resultingfromthe presenceof hybridsas For instance,not all black anthersin the Comthetruereflection ofthecharacterpattern.Others positae genusMontanoa Cerv. are homologous. have advocated removingthe hybridsthathave Althoughoriginallytreated as one apomorphy been identifiedby their'intermediacy'at the be- (Funk, 1982) a close examination showed that ginningof the analysis. The thirdgroup advises some black antherswere black only around the leaving all of the taxa in the analysis and then edges of the thecae,some wereblack onlyon the closelyexaminingthecladogramsforpolytomies top of the connective,while otherswere com(nodes with more than two branches)and char- pletelyblack. This additional informationindiacterconflictsthatmayindicatepossiblehybrids. cated that"black anthers"was not a singleapoThere are problems with all three approaches. morphy but three apomorphies. Character The firstdoes not accuratelyreflectthecharacter conflictscan also be the result of a designated pattern;as we shall see, hybridsmay appear on apomorphyactually containingseveral characthe cladogram in a polytomyor with character ters. Characters such as habit, chromosome all can be divided conflictsor even as ancestorswhentheyare none number,and flowerregularity, of these.The patternsdo not reflectthe accurate intoseveralcharacters.New apomorphiescan be sister-grouprelationship(nor are theytrue rep- added to the cladistic studyto reflectthe addiresentationsofphylogeny).The second approach tional informationbecause the "groups of charassumes one can identifythehybridspriorto the acters" should not be viewed as characterconanalysis and this is not possible in many cases. flictsbut ratheras separate apomorphies. Such The thirdpositionreliesto a greatextenton hy- changesshouldbe made onlywhenavailable evibrids causing polytomies. Furtheranalysis has dence indicates that they are not homologous. shownthisusuallydoes nothappen (Humphries, Remaining characterconflictsare the result of 1983). eitherundetectedhomoplasy or hybridization. I ASEXUAL
Autoolygoid727. >2
Diploid
2j
In n
I
SEXUAL
1985]
683
F]UNK-HYBRIDIZATION
assume thatall apomorphiesare dominantover the more plesiomorphiccharactersof a transformation series.The data presentedlaterin this 4 paperindicatethatin theheterozygouscondition of the hybridtheremightwell be a higherpercentageof plesiomorphiccharactersshowingin 5 the phenotype.Therefore,it is possible for the hybridto show only plesiomorphies(primitive, ancestral,or moregeneralcharacters)and appear on the cladogram in an ancestral position. In Figure 2, taxon D could be a hybrid,between 2~~~~~~~~~~ taxon C and any othertaxon, thatinheritedthe plesiomorphiesof both parents.Indeed, it is into speculateon whetheror notone could teresting use such cladistic studies to identifyinteresting geneticproblems. FIGURE2. Cladogram illustrating character conflict Often the hybridsin a cladistic analysis will thatcanbe theresultofeitherhybridization orparallel be groupedwithone or the otherof the parents evolution. dependingon with which parenttheyshare the A lack of apomorphies can also be caused by most apomorphies (Humphries & Funk, 1984). hybridity.The hybriddoes not necessarilyin- When theputativeparentsare sisterspecies (two heritall oftheapomorphiesofbothparents.This species that are more closely related to one observationis important:thereis no reason to anotherthan theyare to any otherspecies), hyA
B
C
A
H
D
B
5
E
C
B
H
A
C
242
1
3
41
H
=4
~~~~~4
5
34
5: 2
2
3
FIGURES
3 1
5
3-6.
6
1
Cladograms illustratingthe patternof species A and B and theirhybrid,H.
ANNALS OF THE MISSOURI BOTANICAL GARDEN
684 A
HBC
7 FIGURE
the patternof 7. Cladogramillustrating
species A and B and theirhybrid,H.
brids are quite often apparent regardless of whetheror not theyformpolytornies.Hybrids that formdichotomous branchingpatternscan be identifiedas such so long as theyhave at least one apomorphyof both parentsor if theylack an autapomorphyof the parentwithwhichthey are grouped. For instance in Figures 3-5 (for characterssee Appendix B), species A and B hybridize to give species H. If therewere an equal numberof apornorphiesin A and B (characters 4 and 5) and if both were found in the hybrid, theresultcould be expressedas two equally parsimonious cladograms(Figs. 3, 4) or as a trichotomy (Fig. 5), althoughthe latterinvolves one more characterchangeand is thereforeone step charactersetis inferred longer.Iftheincongruent thehybridcould to be theresultofhybridization, be placed above the diagram connectingwith both parents (Fig. 6). However, if one parent thantheothtaxonhad one moreautapornorphy er, or if the hybridshowed unequal character inheritance,thena singlecladogramresults.For instance,iftaxon A (Fig. 7; AppendixC) had two autapornorphies(5 and 6), and the hybridinheritedall apornorphiesofbothparents,themost parsimonious cladogram would give the result shownin Figure7. Nonetheless,because theyare sistertaxa, the possibilityof hybridizationis apparent,so long as the hybridhas at least one apomorphyfromeach parent.However,as mentioned earlierit is possible forthe hybridnot to displayall theapornorphies.If the hybridin Figure 7 did not have character4 therewould be no indicationthatit was a hybrid(exceptforthe
[VOL. 72
more indirectevidence of lack of apomorphies in taxa A and H). If one parent has very few autapomorphiesthereis less chance thatthe hybrid will have any indicationof its history. Sometimesthereis morethanone hybridfrom the same two parents(Figs. 8-12; Appendix D). The two hybrids are most parsimoniously grouped with eitherparent (Figs. 8, 9) but the two equally parsimonious cladograms indicate the hybridityof HI and H2. The most parsimonious cladogram has two reticulations(Fig. 12). It is, of course, possible that taxa HI and H2 are the resultof a singlehybridizationevent followedby segregation.One wayto evaluate this possibilityis to examine the distributionof the taxa in question.The possibilityofhybridization followedby segregationlessens as the distance betweenthe hybridtaxa increases. The only time it is "most parsimonious" to have a polytomyis when the hybriddoes not have any of the autapomorphiesof eitherparent (Fig. 13; Appendix E). However,parenttaxa are notalwayssistertaxa. For instance,Wagner (1954) has shown that at leastthreediploids are involved in producingthe hybridsin Asplenium,and Grant (1953, 1964) has shown that species from differentspecies groupsare hybridizingin Gilia (Funk, 1981). In cases such as this the task of identifying hybrids becomes more difficult. For instance,given the cladogram in Figure 14 (Figs. 14-17, 19; AppendixF) themostparsimoniouscladogramthat includes the hybrid,places the hybrid(H, Fig. 15) as thesistertaxon oftheparentthatinvolved the least number of homoplasious events (the number of characterchanges or lengthof this cladogramis L = 11). The lengthwould increase ifthe hybridweregroupedwiththe otherparent (Fig. 16, L = 12) because thereis one more homoplasy. It is much longerto forma polytomy (Fig. 17, L = 14). The only time a polytomy would be formed in the most parsimonious cladogramis if the hybridhad none of the apomorphiesof eitherparent,at least those above the firstnode shared by both parents (Fig. 18; Appendix G). If the hybridis identifiedas such itcan be removedfromthecladogramand placed above it givingan even shortercladogram (Fig. 19, L = 9).
The identificationof possible hybridsis only the beginningof an analysis. Those cladograms indicatinghybrids(e.g., Fig. 19) are merelyhypotheses of hybridizationand should be tested by using other data, such as distribution,chro-
1985]
685
FUNK-HYBRIDIZATION
A
H1
H2
B
C
A
H2
H1
A
5
20
H1
2
C
~~~~~~~~~~~~~~~3
3
8
B
H2
95
B
C
A
tH2
Hi 1
1
2
BC
2
2=
3
13
10
5
H
H
~~~~~~B ~
A
12
5
11
C
5
FIGURES 8-12. Cladograms illustratingsome of the resultswhen the same two parent species (A and B) produce more than one hybrid,HI and H2.
mosome number,karyotyping,and pollen fertilitybeforetheycan be referredto as hybrids. Nelson (1983) has suggesteda methodforanalyzingcladogramsforpossible hybrids.His procedurebeginswiththemostparsimoniousclado-
gram without a reticulationand continues by adding reticulationsone at a time so as to minimize characterconflict.It is based on the idea that when there are two equally parsimonious waysof representing a homologyon a cladogram
686 A
ANNALS OF THE MISSOURI BOTANICAL GARDEN H
B
C
[VOL. 72
but have since speciated(developed autapomorphies), some have numerous hybridsand even hybridizationamong hybrids,and some hybrids do nothave all oftheapomorphiesoftheparents (as in Fig. 2). The workabilityof Nelson's meth2 1 od is dependenton thehybridinheriting theapomorphiccharactersfromtheparenttaxa without too many characterlosses; otherwisethe cladogram with the reticulations(Fig. 28; for characters forFigs. 28, 29 see Appendix K) will be longer than the most parsimonious cladogram 3 withoutreticulations(Fig. 29). Also, thismethod is only feasible when the percentageof hybrids in the data set is low because the possibilities 5 1 3 become endless,especiallywhen the hybridsare hybridizing. that it is more FIGURE 13. Cladogram illustrating There are additional guidelines and methods parsimoniousto have a polytomywhenthehybriddoes that can be used when examiningcladogramsfor not show any of the autapomorphiesof eitherparent. possible hybrids.Use of theseon seven data sets indicates that insightsinto the identificationof one should investigatethepossibilityofinserting possible hybridsand theirparentscan be gained a reticulation.If the reticulationresultsin a de- by studyingthe characterpatternsof the cladocrease of apparent homoplasy and if the taxon gramsas wellas thedistributions and ploidylevels exhibitscharacterconflictof the "intermediate" of the taxa involved. Some of these guidelines type,the reticulationcan be maintained. For a and methodsare elaborationsand evaluationsof certain set of data (Appendix H) thereare two previouslypublished ideas and othersare new. equally parsimoniouscladograms,withthesame branchingpattern.One cladogram (Fig. 20) has GUIDELINES AND METHODS FOR IDENTIFYING a parallelacquisitionof character4 (Figs. 20-22, POSSIBLE HYBRIDS AND THEIR PARENTS Appendix H) and the otherhas one acquisition 1. When thereare two cladogramsof similar of character4 and a subsequent loss (Fig. 21). However,one can introduceone reticulationand lengthand one taxon positionchanges,thetaxon eliminate the need for homoplasy and/or loss thatis movingmay be a hybridand thetwo taxa (Fig. 22). All this diagram indicates is that if betweenwhich it is moving may be the parents. hybridizationis involved it is most likelythat In Figures 3 and 4, taxon H (the hybrid)shifts between taxa A and B in the two most parsitaxon B is of hybridorigin. A more complicated example involves nine monious cladograms.Taxon H may be a hybrid taxa and 12 characters.There are two equally and A and B may be its parents.In Figures 15 parsimoniouscladogramswiththe same branch- and 16 taxon H shiftsbetweentaxa C and D and amountsof homoplasy may be a hybrid. ing patternwithdifferent 2. As an extensionof number 1, it is possible and loss (Figs. 23, 24; forcharactersforFigs. 2325 see Appendix I). By progressivelyadding re- to followa path of characterconflicts.Figure 15 ticulations,all need ofreversaland/orhomoplasy has characters6 and 7 appearingtwice and this can be eliminated.Taxa H and I may be hybrids identifiestaxon D, the parentwithwhichH (the (Fig. 25). Nelson's method of examination of hybrid)is not grouped. Figure 16 has 1, 3, and 5 appearingtwiceand thisidentifiestaxon C, the characterconflictis only a beginning. Microloma illustratesthe use of the Nelson parentwithwhichH is not grouped.You do not method to change the cladogram in Figure 26 have to have all of the characters.For instance, (forcharactersforFigs. 26, 27 see Appendix J) in Figure 16, H mightnot have character3 (Fig. to theone in Figure27 by addingone reticulation 30; forcharactersforFigs. 30, 31 see Appendix L) but as long as it had 1 and 5 taxon C would and therebyshorteningthe cladogram. Some groups have characteristicsthat cause emergeas the otherparent(Fig. 31). 3. Taxa that are definedsolely by character when usingNelson's method.For indifficulties stance, some have theiroriginin hybridization conflictsmay be hybridsor parents. In Figure
687
FUNK-HYBRIDIZATION
1985] A
B
E
D
C
A
C
B
D
H
E
2~~~~~~~~~~~~~~~~~~~~~~~~~~ 4
/6
8
5
7
8
14
~~~~~~~~~25
5 35
14
1
5
6~~~~~~~~~~~~
5
6
2
8
28
14
7
9
16
9
17
H
A
C
B
H
E
DAE A
C
B
~~~~ ~
2
2
1
1
X
x
19
\
T~/ /
/
/
comp.
1(1) 13
10 0
pim
epi
'pf-i
1 3
cana
comp.
4-11 ?
~
\
pfp ne-h
pf-ir / 3
~~~~~~2(I#1
121
14 35(2")
ne-n
aur
can
rup
11(2 11(2)(2
i~ 8
E
2)
2)
'
3~~~~~~~~1 \
2~~~~~~~~~~~~~2
12~~~~~~2123 33
25
46~~~2
21
46 FIGiURE 46.
Cladogramof Agastache with reticulations.
Chihuahua and southernNew Mexico) and parapatricwithA. mearnsii(southernChihuahua and the Chihuahua/Sonoraborder). The A. pallidiflora subspecifictaxa and A. brevifioraare distributedin the southwestUnited States. If A. pringleiis a hybridthe most likelyputativeparents are A. micranthaand A. mearnsii. A thirdpotentialhybrid,A. pallida var. coriacea (pd-c), is sisterto A. pallida var. pallida and has two characterlosses. If A. pallida var. coriacea is a hybridand one parentis A. pallida var. pallida then the other parent is probably somethingthatlacks characters10 and 11; possiblysomethingin the"Pallidifloracomplex" because the putativehybridhas characters16 and 21. Based on geographicaldistribution,themost likelyparentin the "Pallidifloracomplex" is A. mearnsiithathas a parapatricdistributionwith A. pallida var. coriacea. The last two possiblehybrids,A. coccinea(coc)
and A. pallidifloravar. gilensis (pf-i),are more difficultto place because they have less information (fewercharacters).We can estimatethat A. coccinea is a hybridand thatone parentmay be found in the group definedby character32; because of the presence of character21(1') the otherparentwould probablybe A. mearnsii.The distributionof the species does not help in this case because several of the taxa are sympatric. The finaltaxon considered as a hybridis A. pallidifloravar. gilensis.This taxon mightbe the resultofa crossbetweenA. pallidifloravar.greenii and some taxon withoutcharacter24. All taxa in the "Pallidifloracomplex" thathave a distributionthatwould allow forthe formationofthis hybridhave character 24 except A. mearnsii. However,A. pallidifloravar. gilensishas an autapomorphy,and this makes it less likelythat it is ofhybridorigin(butdoes notexcludeit). Based on this analysis the followinghybridsare pos-
1985]
FUNK-HYBRIDIZATION X= 9
flo
gdg
gdv
lan
lat
gs-gd
8,9
BR
X= 9
x=4 pil
mar gs-gg
1~~~~3
2B 2
x=3 sca
T t1
hi
1020
14 \1 7B
697
-7A 12
X=9
gs-c
gs-h 4
21
gs-gt
li-d
lii
1 19 16
14
2B 41
14,19
sub
22
2A 8
17 6 21b\
gs-c
gs-h
sub is1
14
12
21
~~~ 49 ~~~~~~~~~~~~~14
2B 6 gs-gg
gs-c
gs-h 4 16
sub
gs-gt
li-I
li-d
19 1422
21 8
47
| (x=5)
6
48
of Chrysopsis and Bradburia. FIGURES47-49. Cladograms sible:brv= wrtx mm, pm = mic x "Pallidiflora States.Using thecharactersfurnishedby Semple threecladogramswereconstructed(Figs. 47-49). mex-plm,and pf-i= pf-rx some taxon without There is a highlevel of homoplasyin the clado24 (possibly mm). gram because only nine apomorphies lacked Figure46 shows thehypothesizedhybridsand characterconflictsand only fourof these 11 are their possible parents. According to Sanders synapomorphies(10, 20, 11, 2A). Such a high (1981), the hybrids and their parents are as level of characterconflictand characterloss is an indication of possible hybridization.The follows: brv = wrt x mm, pM = mic x mm, chromosome numbers were not used as charpd-c = pd-p x mm, coc = pfrx mm (mex-epl + mm), and pf-i= pf-rx mm (pf-f-pf-r + mm). acters in the analysis and are indicated on the AlthoughSanders' estimatesare in some cases cladogramto facilitatethediscussion.Also, there more specific,thereare no conflicts. is one reportof x = 4 forBradburia thatis not indicatedon the cladogram. Taxa C. lanuginosa (lan), C. gossypinasubsp. EXAMPLE 4. CHRYSOPSIS AND BRADBURIA gossypinaf.gossypina(gs-gg),C. gossypinasubsp. (ASTERACEAE) SEMPLE (1981, AND PERS. COMM.), hyssopifolia(gs-h),and C. linearifoliasubsp. IiSEMPLE AND CHINNAPPA (1984) nearifolia(li-i) are definedonlyby characterconChrysopsis (Nutt.) Elliot (Appendix P; 10 flictsand/orcharacterlosses and may be hybrids species) and Bradburia Semple & Chinnappa themselvesor theparentwithwhichanotherhy(AppendixP; 1 species) are yellow-rayedgolden- brid is not grouped.Two taxa C. godfreyif. viriastersdistributedin the southeastUnited States dis (gd-v)and C. gossypinasubsp.cruiseana(gs-c) (especially Florida) except for one species of are possible parentswith which the hybridsare Chrysopsisthat occurs in the eastern United grouped because theyhave no autapomorphies complex," pd-c = pd-d x mm, coc = mm x
698
[VOL. 72
ANNALS OF THE MISSOURI BOTANICAL GARDEN Ian
gd-v
flo
50
gd-g
lat
gs-gd
BR
sca
pil
mar
sub
gs-5g
gs-gt
li-I
lid
9
FIGURE50. Cladogram ofChryvsopsis and Bradburiawithreticulations.
and have a singletaxonas a sistertaxa. If we hybrids.This supportsthehypothesesofhybridbasedon thesedatawe ob- ization for three of the subspecifictaxa of C. hypotheses construct (gs-gg,gs-c& h), howeverC. gossypina results:lan = gd-gx li-l,gs-c gossypina tainthefollowing and f. decumbens(gs-gt,gs-gd) & h = sub x pil or mar,and gs-gg= sub x some f. trichophylla taxonwithout8. Becauseso manyof thetaxa were not identified,except for notingthat they are lacked autapomorphies.The cladogram clearly thedistributions orparapatric, aresympatric thehypotheses. indicates why C. gossypinaf. decumbenswas inrefining notofmuchassistance The exceptionsare C. gossypinasubspp.cru- overlooked,ithas no synapomorphiesor autapo(gs-c& h) thatcan be morphies.If it is a hybridit is an excellentexiseana and hyssopifolia to a crossbetweenC. subulataand C. ample of a hybridinheritingall plesiomorphies attributed of both parents and appearing in an ancestral mariana(sub x mar). Thereare fourtaxa withno autapomorphies position on the cladogram. Likewise, C. gossywas overlooked because it gs-gd(C. gossypina pina f. trichophylla f.godfreyi), [gd-g(C. godfreyi li-d)1that inheritedmost, but not all, of the plesiomorgs-gt, subsp.gossypinaf.decumbens), are potentialhybridsor parents.Their chro- phies. The chromosome numberof x = 5 does showthatall ofthegstaxaare not support,and in factfalsifies,the hypothesis mosomenumbers x = 9, and based on outgroupcomparisonthe of hybridizationfor C. lanuginosabecause one base numberforthegenerais probablyx = 5 of the hypothesizedparentshas x = 5 and the the other x = 9. (thisagreeswithSemple,1981). Therefore, Figures47-49 show thatthex = 9 taxa do not taxaof C. gossypinaare mostlikely subspecific
1985]
699
FUNK-HYBRIDIZATION frutescens group
californica group van 10(2)
lac
asp
10(1)
cal
can
pal
14()
phe
rad
14(2)
SC
far
act
vir
rav
res
OC
SF
fru 12
12
3 16~~~~~~~~~~~~~~~~~1 7(2)161
7(1)
14(2)
13
12
7(2) 16
1~~~~~~~~~~~~~~~~1 3
511
5
51 FIGURE
51. CladogramofEncelia.
forma monophyleticgroup.Semple (198 1) proposed thatthe x = 9 group is fromone hybridization event between an individual of C. subulataand one of C. marianawith subsequent combinationsof paselectionsto give different rental genes. The cladogram does not support combithat statementbecause of the different nations of charactersin the five differentsubspecifictaxa. However, it also does not reject Semple's suggestion.It simplysuggeststhatone should also consider the possibilityof several eventsinvolvingthe same different hybridization charactersbeing species as parentswithdifferent inheritedeach time (Fig. 50). Using cladisticsalone has not given us a clear answerto the question of hybridizationin Chrysopsis and Bradburia, however when the hypotheses of hybridizationare tested with additional information,such as distribution and ploidy level, we have been able to make five putativehybridsand gain some insightinto possible parents.
EXAMPLE 5. ENCELIA (ASTERACEAE) (CLARK, PERS. COMM.)
Encelia Adanson (Appendix Q) comprises 18 taxa distributedin thewesternUnited States.All taxa are diploids. The data matrixand thetaxon distributionswere furnishedby CurtisClark. There are at least two cladograms that are equally parsimonious(Figs. 51, 52) and one that is one step longer (Fig. 53); all have different branchingpatterns.There are several additional character cladogramsthathave slightlydifferent branching distributionsbut do not have different patterns,and these are not illustrated.On the three cladograms there are several taxa that changepositions.Enceliafarinosa can be placed as thesistertaxa ofE. farinosa var. phenicodonta (Figs. 52, 53) or near the base of the cladogram (Fig. 5 1). In eithercase it is onlydefinedby characterloss and/orhomoplasy.LikewiseE. asperifolia is eitherthe sistertaxon of E. ventorum/E. laciniata (Fig. 51) or it is near the basal node (Figs. 52, 53). In all threepositionsE. asperifolia
ANNALS
700
californica ven
16 10(2)
lac
0) 101
rad
BOTANICAL
[VOL. 72
GARDEN
frutescens
group
phe
far
3~
OF THE MISSOURI
can
pal
asp
cal
SC
act
vir
rav
res
GC
group SF
fru
14(1
12(2 9
7(2) 12!
8 7(1)
3
13 8
5
52 FIGURE
52. CladogramofEncelia.
is identifiedby characterloss and/orhomoplasy. Encelia canescens is eitherthe sistertaxon of E. palmeri (Fig. 51) or it shares the node defined by character7(1) with several other taxa (Figs. 52, 53). Two other taxa have some indication that theymay be hybrids,E. laciniata with intermediatecharacter10(1) and the unidentified taxon fromSanta Carla (SC) that is always definedby characterhomoplasy. There are three taxa that can be indicated as possibilities but cannotbe placed as hybrids,ancestors,or parents because theyhave few apomorphies. Two taxa (E. virginensisand E. actoni) have onlyone apomorphyeach and theyappear on the cladogram at the basal node, and E. californicahas a slight change in position dependingon whethercharacter 3 is treatedas a characterloss or not (Figs. 51-53). Encelia farinosa and E. asperifoliastand out because of characterlosses and homoplasy.The best estimateforE. farinosa is thatit is a hybrid betweenE. farinosa var. phenicodonta(its sister
taxon in Figs. 52, 53) and somethingwithout characters1, 2, and 3. Encelia asperifoliamay be a hybridbetween somethingwithout characters3 and 12 (perhaps somethingin the "Frutescensgroup") and somethingin the "Californica group" with character 8 (perhaps E. californicawithwhich it is closely grouped and whose lack of apomorphies may account forE. asperifolia's similar situation). Encelia canescens mightbe a hybrid,betweenE. palmeri its sistertaxon in Figure 51 and E. farinosa var. phenicodonta,because of the intermediatenatureof character14. Encelia laciniata may be a hybridbetweenE. ventorumand some othertaxon thathas not lefta trace. If so, E. laciniata is an example of a hybridinheritingall of the apomorphiesof one parent.If the taxon fromSanta Clara (SC) is a hybrid,one parent mightbe E. ventorumbecause of characters13 and 16 and theotherparentsomethingfromthe"Californica group" that has character 12. A summation of possible hybridsis as follows:far= phe x some-
701
FUNK-HYBRIDIZATION
19851 californica ven
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lac
10(1)
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rad
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group SF
fru
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2
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group
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3 13
71 12 12 3 8
5
53 FIGURE
53. CladogramofEncelia.
thingwithout1, 2, and 3, asp = cal x something in the "Frutescensgroup" with 8, can = pal x phe, lac = ven x ?, and SC = ven x "Frutescens group" with 12. Listed above are fivehypothesesof hybridization and some possible parents.Examinationof the distributionpatternsand otherdata do not supporttwo of the hypotheses(E. farinosa and SC) and an additional one is added. An F, that has been identifiedas E. virginensishas been found growingwith E. actoni so that E. virginensisshouldbe investigatedas a possible hybrid withE. actoni as one of the parents. Using the distributionswe can narrowdown the choice of possible parentsto the following: asp = cal x SF, can = phe x pal, lac = ven x ?, and vir = act x ?.
The reticulatecladogram is illustratedin Figure 54. The hybridsindicatedwithsolid lines are thosethatweresupportedas hybridsby both the data; those cladisticanalysisand thedistributional withdottedlines were supportedby only one of the two.
EXAMPLE
6.
MONTANOA (ASTERACEAE) (FUNK,
1982)
Montanoa Cerv. (Appendix R) has 20 species in Mexico and Central America and five in northernSouth America. Examiningone of the equally parsimoniouscladograms(Fig. 55), only one taxon (M. hexagona) shows any stronginThis taxonhas theonly dicationofhybridization. two characterlosses on thecladogram.There are however,threeknown high level polyploids in thegenus(Fig. 55). Two ofthese(M. revealiiand M. guatemalensis) show no evidence of being hybrids.The thirdis M. hexagona and, it could be a hybridbetween its sistertaxon, M. hibiscifolia,and somethingoutside of the group definedby character34. None ofthepolyploidsare sympatricwith any other species and they all have at least 95% pollen viability,and during meiosis thereis at least one stage wherea complete bivalent can be observed. So, we are left with these three species being either very old polyploids,twoofwhichhave developed autapo-
ANNALS OF THE MISSOURI BOTANICAL GARDEN
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FIGURE54. Cladogram of Encelia withreticulations.
morphies,or the parentsare extinctso the rela- of SpilanthesJacq. but wereremovedby Jansen tionshipsdo not show up on the diagram. Or, (1981). Thereare 39 taxa (30 species),16 ofwhich less likely,theyare autopolyploidswiththe dip- are diploids (23 polyploids; ploidy level is estiloids no longer extant. The cladogram cannot mated in some species, see Appendix S). The genus is pantropical with one species in the help us in resolvingthis matter. southeastUnited States. Some species formautopolyploidseriesthatwould allow themto cross EXAMPLE 7. ACMELLA (ASTERACEAE) withallopolyploids.Also, some reproduceasex(JANSEN, IN PRESS) ually so odd level polyploids persistin nature. This last example presentsthe most difficult There are at least ten equally parsimonious case: one wherethereare morehybridsthannon- cladogramsofAcmella and a largenumber(over hybridsin a genus, where the hybridsare hy- 100) that are only a few steps longer. Many of structures. bridizing,where thereare fewcharactersin the these cladogramshave verydifferent analysisand some of the hybridshave inherited I have selectedone to discuss as a representative mostlyplesiomorphies,and where the hybrids (Fig. 56), but in no way am I indicatingthatthis are weeds that disperse readilyand tend to hy- particularcladogramis to be preferredover any bridizewherevertheyare. Althoughnot therule, other. In Figure 56 there are only three aposuch situationsare not that unusual in the As- morphies (excluding autapomorphies) that are teraceaefamily.One such genusis Acmella (Ap- not eithersubsequentlylost or found elsewhere pendixS). The species ofAcmella used to be part on the cladogram [7, 1, 2(2)]. The threemajor
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55 ofMontanoa,numbersabove taxa indicate ploidy level of knownpolyploids. FIGURE55. Cladogram groups of Jansen(in press; indicated in Fig. 56 by the largenumbers1, 2, and 3) are obvious on the cladogram and only one, number 2, is nonmonophyletic(thisgroupwas non-monophyletic on all ofthecladogramsthatI constructed).Some taxa may be hybridsbetween the three major groups, some of the more obvious ones are as follows: 1. A. decumbens var. decumbens (23a) may be a hybridbetweensome taxon in group 1 and one in group 2 because it has apomorphies 1 and 2. 2. A. poliolepidica (1) may be a hybridbetweena taxon in group I thathas apomorphy20 and a taxon in group 3 withapomorphy 16. 3. The ancestorof A. darwinii(7) and A. sodiroi(8) may have been a hybridbetweena taxon in group 2 and one in group 3 thathas apomorphies 18(2) and 17(2). 4. A. paniculata (19) may be the hybridof a taxon in group 3 and one outside of it because of its lack of apomorphy 22 (only two taxa in group 3 lack apomorphy22).
Other taxa show some indication of hybridization withinthe groups. However, thereis no strongindication of hybridsand their parents withinthe groupsbecause thereare so many alternativegroupingsand so fewcharacters.Some taxa are obviouslyhybridsor of hybridancestry because of theirploidy level (Fig. 56, Appendix S) but thereis littleindicationof what theirhisparsimonycladotorymightbe. The different possible hybridsand pargramsgive us different ents. With the exception of two or three small groupsofspeciesthatappear repeatedlyon many, if not all, of the cladogramsthereare a fewadditional questions, such as biogeography,character evolution, or ecology that can be investigated usingthese cladograms. To a large extent we are dealing with straightcharacterpatterns. We have apparentlyreached the limitsof cladistics with genera such as Acmella. I say this because cladisticsis merelyan organizedway of lookingat the relevantdata thathave been gathered. If no consistentpatterndevelops usingcladistics then the data are responsible, not the
ANNALS
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56 FIGURE 56. topologies.
One of the many equally parsimonious cladograrns for Acmella, many of which have different
method.So the lack of resolutionin generasuch as Acmella is simplya reflectionof the data. In the futurewe may be able to gain more information fromgenetic level researchto increase resolutionfrom the data base and obtain further cladisticanalyses.
and thata cladogramcan be reconstitutedfrom a classification.In such a classificationonly monophyleticgroupsare recognized.An example usingthe genusAnacyclusfromFigure 39 is listed below:
Classificationof Anacycluswithouthybrids Anacyclus A. pyrethrum CLASSIFICATION OF HYBRIDS A. monanthos A numberof papers have been publishedthat A. maroccanus discuss the possibilities of classifyinghybrids A. radiatus (Wiley, 1979; Wagner, 1980; Humphries, 1983; Clavatus species group Humphries& Funk, 1984; Nelson, 1973) so the A. linearilobus alternativesneed not be discussed in thispaper. A. clavatus As discussed in Humphries and Funk (1984), I A. homogamos preferthe method called phyleticsequencingor A. latealatus the annotatedLinnean Hierarchy.This method A. nigellifolius workson the basic principlethatall information froma cladogramis available in a classification The hybridscan be added in several ways; one
1985]
FUNK-HYBRIDIZATION
705
is to make themthe sistertaxon of eitherone of tions exist in some groupsthatmake a cladistic the parents.Using the firstparentin the phyletic analysis more difficult. Such conditionsinclude sequencewe arriveat thefollowingclassification: the following:1) havingan increasedpercentage of species within a group that are hybrids,2) Classificationof Anacycluswithhybrids havinghybridsthathave mainlyplesiomorphies, Anacyclus 3) havinghybridsthathybridizewithone another, Sect. Pyrethraria 4) having species that can reproduceasexually, A. pyrethrum and/or5) having introgressionoccur. +A. officinarumsedis mutabilis (A. pyrethrumx radiatus) Sect. Anacyclus LITERATURE CITED A. monanthos ADAMS,E. N., III. 1972. Consensus techniquesand A. maroccanus thecomparisonoftaxonomictrees.Syst.Zool. 21: A. radiatus 390-397. BREMER, K. 1983. Angiosperms and phylogenetic Clavatus species group systematics:some problemsand examples. Verh. A. linearilobus Naturwiss.Vereins Hamburg 26: 343-354. A. homogamos & H.-E. WANNTORP. 1977. Phylogeneticsys+A. inconstans sedis mutabilis (A. tematicsin botany.Taxon 27: 317-329. homogamos x clavatus) . 1979. Hierarchyand reticulations & in systematics.Syst.Zool. 28: 624-627. +A. valentinus sedis mutabilis (A. CLARK, C. 1982. Relationshipsbetweenexperimental monogamos x clavatus) and phylogeneticsystematics:an overview. Bot. A. clavatus Soc. Amer. Misc. Publ. 162: 88. A. latealatus FELSENSTEIN, J. 1983. NumericalTaxonomy. Springer-Verlag,Berlin,Heidelberg,New York, Tokyo. A. nigellifolius The special notationsinclude a plus sign(+) for hybrids,the parental species listed are the hybrids in parentheses,and the latin phrase sedis mutabilis("changeable position") thatis used to mean a polytomyin the cladogram. The cladogramis recoveredin the followingmanner.Section Pyrethrariais the sistergroup of sect. Anacyclus, and A. pyrethrumand A. officinarum are sistertaxa withinsect. Pyrethraria(Fig. 39). In succession; A. monanthosis the sistertaxon of the remainingspecies; A. marocannus is the sistertaxon to theremainingspecies;A. radiatus is the sistertaxon to the remainingspecies; the "clavatus group" is thesistergroupto A. latealatus and A. nigellifolius(Fig. 39); withinthe "clavatus group,"A. linearilobusis the sistertaxa of A. clavatus and A. homogamos and their two hybrids;and A. homogamos is the sistertaxon of A. clavatus, but formsa polytomywith the two hybrids. I add to thisthe provisionthatshould the two parentsoccur in different subgenericgroups (or different genera)thenthehybridshould be listed in both groups. CONCLUSION
In general,phylogenetic systematics can be used to help identifypossible hybridsand theirparents forfurtherstudy.However, several condi-
V. A. 1981. Special concerns in estimating plant phylogenies.Pp. 73-86 in V. A. Funk & D. R. Brooks (editors),Advances in Cladistics: Proceedingsof the FirstMeetingof the Willi Hennig Society.New York Botanical Garden, New York. 1982. The systematicsof Montanoa (Asteraceae, Heliantheae). Mem. New York Bot. Gard. 36: 1-133. P. 1979. Polyploidy in angiosperms: GOLDBLATT, monocotyledons.In W. H. Lewis (editor), Polyploidy: Biological Relevance. Plenum Press,New York. GRANT, V. 1953. The role of hybridizationin the evolution of the leafy-stemmedGilias. Evolution 7: 51-64. 1964. Genetic and taxonomicstudiesin Gilia. XII. Fertilityrelationshipsofthepolyploidcobwebby Gilias. Aliso 5: 479-507. HENNIG, W. 1966. PhylogeneticSystematics.Univ. of Illinois Press, Urbana. HUMPHRIES, C. J. 1979. A revision of the genusAnacyclusL. (Compositae: Anthemideae).Bull. Brit. Mus. (Nat. Hist.), Bot. 7: 83-142. . 1981. Cytogeneticand cladistic studies in AnacyclusL. (Compositae: Anthemideae).Nordic J. Bot. 1: 83-96. 1983. Primarydata in hybridanalysis. Pp. 89-103 in N. I. Platnick& V. A. Funk (editors), Advances in Cladistics:ProceedingsoftheSecond Meeting of the Willi Hennig Society. Columbia Univ. Press, New York. & V. A. FUNK. 1984. Cladistic methodology. Pp. 323-361 in V. H. Heywood & D. M. Moore (editors),CurrentTopics in Plant Taxonomy. Academic Press Inc., London. JANSEN, R. K. 1981. SystematicsofSpilanthes(Compositae: Heliantheae). Syst. Bot. 6: 231-257. FUNK,
706
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* In press. SystematicsofAcmella (Asteraceae, * 1980. Originand philosophyof the groundHeliantheae). Syst. Bot. Monographs. plan divergencemethodof cladistics.Syst.Bot. 5: LEWIS, W. H. 1979. Polyploidyin angiosperms:di173-193. * 1983. Reticulistics:therecognitionofhybrids cotyledons.In W. H. Lewis (editor),Polyploidy: Biological Relevance. Plenum Press, New York. and theirrole in cladistics and classification.Pp. MARGUSH, T. & F. R. McMoRRIs. 1981. Consensus 63-79 in N. I. Platnick & V. A. Funk (editors), n-trees.Bull. Math. Biol. 43: 239-244. Advances in Cladistics:ProceedingsoftheSecond Meeting of the Willi Hennig Society. Columbia McMoRRIs, F. R., D. B. MERONK & D. A. NEUMANN. 1983. A view of some consensus methods for Univ. Press, New York. trees.Pp. 122-126 in J. Felsenstein(editor),NuWANNTORP, H.-E. 1983. Reticulatedcladogramsand mericalTaxonomy. Springer-Verlag, Berlin,Heithe identificationof hybridtaxa. Pp. 81-88 in N. I. Platnick & V. A. Funk (editors),Advances in delberg,New York, Tokyo. MICKEVICH,M. R. 1978. Taxonomic congruence.Syst. Cladistics: Proceedingsof the Second Meeting of Zool. 27: 143-158. the Willi Hennig Society. Columbia Univ. Press, NELSON, G. 1973. Classificationas an expressionof New York. phylogeneticrelationships.Syst. Zool. 22: 344WILEY, E. 0. 1979. An annotated Linnaean hier359. archy,with commentson naturaltaxa and com1979. Cladistic analysis and synthesis:prinpetingsystems.Syst.Zool. 28: 308-337. ciples and definitions,with a historicalnote on & D. R. BROOKS. 1982. Victims of historyAdanson's Familles des Plantes (1763-1764). Syst. a nonequilibriumapproachto evolution.Syst.Zool. Zool. 28: 1-2 1. 31: 1-24. 1983. Reticulationin cladograms.Pp. 105111 in N. I. Platnick& V. A. Funk (editors),Advances in Cladistics: Proceedings of the Second Meeting of the Willi Hennig Society. Columbia APPENDICES A-S. Only the apomorphies are indiUniv. Press,New York. & N. PLATNICK. 1980. Multiple branchingin cated in the data matricesbecause in phylogeneticsyscladograms: two interpretations.Syst. Zool. 29: tematicsonlythe apomorphiesare used to grouptaxa. 86-91. NEUMANN, D. A. 1983. Faithfulconsensus methods APPENDIX A. Data matrixforFigure 2. forn-trees.Math. Biosci. 63: 271-287. ROSEN, D. E. 1979. Fishes from the uplands and Apomorphies intermontanebasins of Guatemala: revisionary studiesand comparativebiogeography. Bull.Amer. 7 1 2 4 5 Taxa 3 6 Mus. Nat. Hist. 162: 267-376. 1 1 1 1 1 A SANDERS, R. W. 1981. CladisticanalysisofAgastache 1 1 1 1 1 1 B (Lamiaceae). Pp. 95-114 in V. A. Funk & D. R. Brooks(editors),Advances in Cladistics:Proceed1 1 C 1 ings of the FirstMeetingof the Willi Hennig So1 1 D ciety.New York Botanical Garden, New York. E 1 1980. Analysis of SCHUH, R. T. & J. T. POLHEMUS. taxonomic congruence among morphological, ecological, and biogeographicaldata sets for the Leptopodomorpha(Hemiptera).Syst.Zool. 29: 1APPENDIX B. Data matrixforFigures 3-6. 26. SEAMAN, F. C. & V. A. FUNK. 1983. Cladisticanalysis Apomorphies of complex naturalproducts:developingtransfor2 1 4 Taxa 3 5 mation series from sesquiterpene lactone data. Taxon 32: 1-27. 1 1 1 A SEMPLE, J. C. 1981. A revision of the goldenaster 1 B 1 1 genus Chrysopsis(Nutt.) Ell. nom. cons. (Com1 1 C positae-Astereae). Rhodora 83: 323-384. H 1 1 1 & C. C. CHINNAPPA. 1984. Observations on the cytology,morphologyand ecology of Bradburia hirtella(Compositae-Astereae). Syst. Bot. 9: 95-101. APPENDIX C. Data matrixforFigure 7. SOKAL, R. R. & F. J. ROHLF. 1981. Taxonomic congruence in the Leptopodomorpha re-examined. Apomorphies Syst.Zool. 30: 304-325. STEBBINS, G. L. 1974. FloweringPlants: Evolution 4 5 1 2 6 Taxa 3 Above the Species Level. Belknap-HarvardPress, Cambridge. 1 1 1 A 1 WAGNER, W. H. 1954. Reticulate evolution in the 1 B 1 1 Appalachian Aspleniums. Evolution 8: 103-108. 1 1 C 1969. The role and taxonomic treatmentof 1 1 H 1 1 1 hybrids.BioScience 19: 785-789.
]FUNK-HYBRIDIZATION
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Data matrixforFigures8-12.
D.
APPENDIX
707
I.
APPENDIX
Data matrixforFigures23-25. Apomorphies
Apomorphies Taxa
1
B C Hi H2
1
2
4
3
5
Taxa
1 1 1 1
B C D E F G H I
1
2
1 I 1 11 1 1 I 1
1 1 I
3
5
4
6
7
1 1 1 1 A A~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ A 1
1 1
1 1
Data matrixforFigure 13.
E.
APPENDIX
1
1 1
1 1 1
1 1 1 1 1 1 1
1 1 1 1 1 1
1 1 1 1
8
9
10 11 12 1
1
1
1
1 1
1 1 1
1 1
1 1
1
1
Apomorphies Taxa
1
A B C H
1
2
3
1
1 1
4
1 1 1 1
1
1
Data matrixforFigures 14-17, 19.
F.
APPENDIX
5
Apomorphies Taxa
1
2
A B C D E H
1 1 1
1
1
APPENDIX
3
4
1 1
1
5
6
1 1
1
1 1 1
7
1 1
8
9 1 1 1 1 1 1
1
Data matrixforFigure 18.
G.
Apomorphies Taxa
1
2
A B C D E H
1 1 1
1
3
4
1 1
1
5
6
1
1 1
7
1
8
9 1 1 1 1 1 1
1
APPENDIX J. MicrolomaR. Br. (Asclepidaceae). Abbreviations.-A. M. incanumDecne.-B. M. ionN. E. Brown.Schlechter.-C. M. burchelli gitubum D. M. armatum.-E. M. campanulatum.-F. M. M. spinosum N. E. Brown.-H. M. dolichanthum.-G. N. E. Brown.-I. M. lanatum.Characviridijiorum ters.-Data publishedin Bremerand Wanntorp(1979) and Humphries (1983) but no characterlist was furnishedin eitherpublication.Data matrix.- For Figures 26, 27, 36-38.
Apomorphies Taxa A B C D E F G H I
2
1 1 1
4
3
1 1
1 1 1 1 1
1 1 1
5
6
7
1 1 1 1 1 1 1
1 1 1 1 1 1 1 1
I 1 1 1 1 1 1 1 1
Data matrixforFigures28, 29.
APPENDIX K.
Apomorphies APPENDIX
H.
Data matrixforFigures20-22. Apomorphies
Taxa
1
2
3
A B C D
1 1 1
1 1
1 1
4
5
1 1
1 1 1 1
Taxa
1 2
A B C D E F G H
1 1 1 1 1 1 111 1 1 1 11
3
4
5 6 7 8 9 10 11 12 13
1 1 1 1
1 1 1
1
1
11 1 1
1 1 1 1
1
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L.
APPENDIX
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Data matrixforFigures 32, 33.
M.
APPENDIX
Apomorphies
Apomorphies Taxa A B C D E H
2
1
1
1 1 1
3 1 1
4 1
5
1 1
1
7
6
8
1
1 1 1
9
Taxa
1 1 1 1 1 1
A B C D E H
1
1
1 2
3
4
5
6
1 1 1
1 1 1
1 1 1
1 1 1
1 1
1
1
1
7 1
8
1
9 10 11 12 13
1
1 1
1
1
1 1
1
1 1 1 1 1 1
APPENDIX N. Anacyclus L. (Asteraceae, Anthemideae). Abbreviations.-A. A. pyrethrum(L.) Link var. (L.) Link var. depressus(Ball) Maire.-C. A. monanthos(L.) Thell.-D. A. maroc-B. A. pyrethrum pyrethrum. canus (Ball) Ball.-E. A. radiatusLoisel. -F. A. coronatus(Murb.) Humphries.-G. A. clavatus(Desf.) Pers.H. A. homogamos(Maire) Humphries.-I. A. valentinusL.-J. A. inconstansPomel.-K. A. linearilobusBoiss. & Reuter.-L. A. latealatus Hub.-Mor.-M. A. nigellifoliusBoiss.-N. A. ofllcinarumHayne. Characters.Published in Humphries (1979). Data matrix.-Lower case lettersrepresentgroups of charactersthat display thatpatternso thatthereare fiveapomorphies thathave the distributionpatternsof a, etc. For Figures39-43.
Apomorphies Taxa
a (5)
b (3)
c (1)
AB C D EF G H I J K LM N
1 1 1 1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1 1
d (3)
1 1 1 1 1 1 1 1
e (3)
1 1 1 1 1 1 1
f (1)
1 1 1 1 1 1 1 1
g (3)
h (1)
i (1)
j
(1)
k (1)
1 1 1 1 1 1 1
1 1 1 1 1
1 1 1 1
1 1 1
1 (1)
m (3)
n (5)
o (4)
p (1)
q (1)
1
1
1 1
1 1
1 1 1 1
1
APPENDIX 0. AgastacheClayt. (Lamiaceae). Abbreviations.-aur. A. aurantiaca(A. Gray) Lint & Epling.-b cana (W. J. Hooker) Wooton & Standley.-coc. A. coccinea(Greene) Lint & Epling.-epi. A. eplingianaR. S Wooton & Standley.-ne-h. A.pa ntha (A. Gray) Wooton & Standley. -mm. A. mearnsii Epling.-mic. A. micra (Briquet) Lint & Epling var. havardii(A. Gray) R. Sanders.-ne-n. A. pallidialora(Heller) Rydbergsubsp. ne mexicana. -pd-c. A. pal/ida(Lindley) Cory var. coriaceaR. Sanders.-pd-p. A. pal/ida(Lindley) Cory var. p var. greenei(Briquet) R. Sanders.-pf-i. A. pallidijiora(Heller) Rydbergsubsp. pallidiflorv subsp. pallidijiora var. pallidifiora.-plm. A. pa/meri(B. L. Robinson) Lint & Epling.-pm. (Heller) Rydbergsubsp. pallidifiora (Greenmax)Wooton & Standley.Characters.- As publishedin Sand rupestris (Greene) Standley.- wrt. A. wrightii
7 because it was an autapomorphyfora subspecifictaxon not used in this analysis. Data matrix.-For Figures Apomorphies 2
Taxa1 aur
brv
1
34
56
1
2
1
2 1a
can 1 coc epl111 mex Mic1 mm ne-h ne-n11 pd-c1 pd-p1 pf-i pf-p11 pf-r
1
1
2'
1
1
11
1
1
11 1111Z 11
1 1
1
2526 1
1
1
1
11
11
1111 1111
11
1
1
1
2' 1 2'
11
11
1
1 1 1
1
1 1
1I 1
1
22 2324
17 182021
131416
111
11
p~m nup wrt1
9 10 1112
8
1l11a
2"/
1
2
aVaries betweenthe apomorphyand plesiomorphy.
1
2
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APPENDIX P. Chrysopsis(Nutt.) Ell. and Bradburia Semple & Chinnappa (Asteraceae). Abbreviations.BR. B. hirtellaT. & G.-flo. C. floridana Small.-gd-g. C. godfreyiSemple f. godfreyi.-gd-v. C. godfreyi Semple f. viridisSemple.-gs-c. C. gossypina(Michx.) Elliot subsp. cruiseana (Dress) Semple.-gs-gd. C. gossypina (Michx.) Elliot subsp. gossypinaf. decumbens(Chapm.) Godfrey.-gs-gg. C. gossypina(Michx.) Elliot (Nutt.)Semple.subsp.gossypinaf.gossypina.-gs-gt. C. gossypina(Michx.) Elliotsubsp.gossypinaf.trichophylla gs-h. C. gossypina(Michx.) Elliot subsp. hyssopifolia(Nutt). Semple.-lan. C. lanuginosa Small.-lat. C. latisquamea Pollard.-li-d. C. linearifoliaSemple subsp. dressiiSemple.-li-l. C. linearifoliaSemple subsp. Iinearifolia.-mar. C. mariana (L.) Elliot.-pil. C. pilosa Nutt.-sca. C. scabrella T. & G.-sub. C. subulata Small. Characters-Original charactersfurnishedby Semple and modifiedslightlyby Funk.
2A. 2B. 4. 6. 7A. 7B. 8. 9.
ApomorphicCharacter
PlesiomorphicCharacter
TransformationSeries
10. 11. 12. 13. 14. 15. 16. 17. 18. 19.
Growthform Growthform Pubescence of basal rosettes Achene body Outer pappus Outer pappus Upper cauline leaves Glandulation of upper cauline leaves Upper leaf base Upper leaf size Glandulation of peduncles Upper leaf shape Upper leaf apex Glandulation of phyllaries Pubescence of phyllaries Phyllarysize Phyllaryapex Outer phyllarysize
20. 21. 22. 23.
Head orientationin bud Inflorescencetype Heads/inflorescence branch Disc florets
biennial biennial wooly no translucentribs bristlesnarrow present wooly sparsely
perennial annual pilose translucentribs bristlesbroad absent not wooly densely
sessile, nonclasping not greatlyreduced glandular elliptic obtuse densely glabrate narrow acute-attenuate much shorterthan innerphyllaries erect open cymose few hemaphroditic
clasping greatlyreduced eglandular linear acute eglandular pubescent broad long,subulate similarin size nodding subumbellate many staminate
Data matrix.-For Figures47-50. Apomorphies Taxa BR flo gd-g gd-v gs-c gs-gd gs-gg gs-gt gs-h lan lat li-d li-l mar pil sca sub
2A 2B 4
5
6 7A 7B
1 1
1
10 11 12 13 14 15 16 17 18 19 20 21 22 23 1
1 1
1 1 1 1
1
1 1
9
11
111
1 1
8
1 1
1 1
1 1 1 1
1 1 111
1 1 1 1 1
1
1 1
1 1 1 1 11 1
1 1 1
1
11 1 1
11 1
1 11 1
1 1
1 11
11 1 1
11
1
111
1
1
1
1 1
1
11
1
1985]
711
FUNK-HYBRIDIZATION
APPENDIX Q. Encelia Adanson (Asteraceae). Abbreviations.-act. E. actoni Elmer.-asp. E. asperifolia(S. F. Blake) Clark & Kyhas. -cal. E. californicaNutt.-can. E. canescens Cav. - far. E. farinosa Gray.-fru. E. frutescensGray.- GC. UndescribedtaxonfromGrand Canyon (C. Clark,pers.comm.).- lac. E. laciniata Vasey & Rose. - pal. E. palmeri Vasey & Rose. - phe. E. farinosa Gray var. phenicodontaI. M. Johnston.- rad. E. radians Brandegee.-rav. E. ravendiWiggins.-res. E. resinosa Brandegee.- SC. Undescribed taxon fromPicachos de Santa Clara, Baja (C. Clark, pers. comm.).-SF. Undescribed taxon fromSan Felipe (C. Clark, pers. comm.). -ven. E. ventorumBrandegee.-vir. E. virginensisNelson. Characters.-To be published by Clark (pers. comm.). Data matrix.-For Figures51-54.
Apomorphies Taxa act asp cal can GC far fru lac pal phe rad rav res SC SF ven vir a
1
2
1 1 1
1 1 1
1 1 1 1
1 1 1 1
3
4
1
1 1 1 1
5
6
1 1 1
1
1
2a
1 1 1 1
1
1 2a 2a
1 1 1
1
1 1
7
1
Varies betweenapomorphies 2 and 1.
8
9
1 1 1 1
1
10
11
13
1
1
1 1 1 1
1 2 1
1 1
1 1
1
15
16
2
1
1
1 1
2
1 1
14
1
1
1 1 1
12
1 1
1 1 1
1 1
712
ANNALS OF THE MISSOURI BOTANICAL GARDEN
[VOL. 72
APPENDIX R. Montanoa Cerv. (Asteraceae). Abbreviations.-AN. M. andersondiMcVaugh.-AG. M. angulata Badillo.-AT. M. atriplicifolia(Pers.)Sch. Bip.-B. M. bipinnatifida(Kunth) K. Koch.-E. M. echinacea S. F. Blake.-F. M.fragrans Badillo.-FU. M.frutescensDC.-GA. M. grandiforaDC.-G. M. guatemalensis Robins. & Greenm.-HE. M. hexagona Robins. & Greenm.-H. M. hibiscifoliaBenth.-I. M. imbricata V. A. Funk.-J. M. josei V. A. Funk.-K. M. karwinskiiDC.-L. M. laskowskiiMcVaugh.-LE. M. leucantha (Lag.) S. F. Blake.-LI. M. liebmannii(Sch. Bip.) S. F. Blake.-M. M. mollissimaGroenland.-O. M. ovahfolia DC.-P. M. pteropoda S. F. Blake.-Q. M. quadrangularisSch. Bip.-R. M. reveali H. Robinson.-S. M. speciosa DC.-ST. M. standleyiV. A. Funk.-T. M. tomentosaCerv. Characters.-Published in Funk (1982). Data matrix.-For Figure 55.
Apomorphies 1 AN AG AT B E F FU GA G HE H I J K L LE LI M 0 P Q R S ST T
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
2
3
1
1
1
1
1
1
1
1
1 1
1 1 1
1 1
1 1 1
4
5
6
7
1 1 1
1 1 1
1 1 1
1 1 1
1
1
1
1
1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1
1 1 1 1 1 1 1 1
1 1 1
1 1 1
1 1 1
1 1 1
1
1
1
1
8
9
1
1
1
1
1
1
1
1
1
1
10
11
12
13
14
15
16
17
1
1
19 20
21
22
1
1
1 1
1 1
1
1
1
1
1 1
1 1
1 1
1
1
1
1
1
1 1
1
1
1
1
1
1
1
1
1 1
1
713
FUJNK-HYBRIDIZATION
1985] APPENDIX R.
Continued.
Apomorphies 24 25 26 27 28 29 30 31 32 34 35 36 37 38 39 40 41 42 43 44 45 46 47
23
1
1
1
1
1 1 1
1 1 1
1
1
11
1
1
1
1
1
1
1
1
1
1
1 1
1
1
1
1 1 1 1 1 1 1
1 1 1
1 1
111
1~~~
1
1 1
1 1
1
11
111 1
1
11 1
~1
1
1 11
1
11 1
1 1 1
1
111 1
1
1
11
1
11
1
1 1 1 1
1 1
1
1
1
1
1
1
1
1 1
1 1
[VOL. 72
ANNALS OF THE MISSOURI BOTANICAL GARDEN
714
APPENDIX S. AcmellaRich. ex Pers. (Asteraceae). Abbreviations (* indicates chromosome number is an (A. H. Moore) R. K. Jansen(4x).-2. A.pilosaR. K. Jansen estimatefrompollen diameter).- 1. A.poliolepidica Rich. var. opposiRich. var. repens(Walt.) R. K. Jansen(4x). -3b. A. oppositifolia (2x).-3a. A. oppositifolia tifolia(2x, 3x, 4x, 5x, 6x).-4. A. ciliata(H.B.K.) Cass. (6x).-5. A. caulirhizaDelile (2x).-6. A. calva(DC.) R. K. Jansen(4x*).-7. A. darwinii(D. M. Porter)R. K. Jansen(6x*).-8. A. sodiroi(Hieron) R. K. Jansen (6x).-9. A. ramosa(Hensl.) R. K. Jansen.(2x).- 10. A. pusilla(Hook. & Am.) R. K. Jansen(2x, 4x).- 11. A. lundelliiR. K. Jansen (2x*).- 12a. A. papposa(Hemsl.) R. K. Jansen var. papposa(4x). -12b. A. papposa (Greenm.) R. K. Jansen(4x).- 13. A. iodiscaea(A. H. Moore) R. K. (Hensl.) R. K. Jansenvar. macrophylla Jansen (4x).- 14. A. uliginosa(Sw.) Cass. (4x). -15a. A. filipes(Greenm.) R. K. Jansen var. filipes(2x*).(Greenm.) R. K. Jansen R. K. Jansen(2x*). - 15c. A.filipes (Greenm.) R. K. Jansenvar. cayensis 1Sb. A.filipes (Benth.) R. K. Jansen(2x).- 16a. A. alba (L'Herit.) R. K. Jansenvar. alba (6x*).- 16b. A. alba var. parvifolia (H.B.K.) R. K. Jansen(6x*). R. K. Jansen(6x*). -18. A. leucantha (L'Herit.) R. K. Jansenvar. ecuadorensis 19. A. paniculata(DC.) R. K. Jansen(4x*).-20a. A. radicans(Jacq.) R. K. Jansenvar. radicans(6x).-20b. A. Cass. (6x).-22a. A. radicans(Jacq.) R. K. Jansenvar. devilis(H.B.K.) R. K. Jansen(6x).-2 1. A. brachyglossa (Turcz.) R. K. Jansenvar. brachy(4x*).-22b. A. grandiflora (Turcz.) R. K. Jansenvar. grandiflora grandiflora (Turcz.) R. K. Jansenvar. discoideaR. K. Jansen(6x*).glossa(Benth.)R. K. Jansen(4x). -22c. A. grandiflora (Smith) R. K. Jansenvar. (4x).-23b. A. decumbens (Smith) R. K. Jansenvar. decumbens 23a. A. decumbens (DC.) R. K. Jansen (2x).-25. A. bellidioides (Hook. & Am.) R. K. Jansen (2x).-24. A. leptophylla affinis R. K. Jansen(2x). (Smith) R. K. Jansen(2x). -26. A. grisea(Chodat) R. K. Jansen(2x). -27. A. serratifolia (Hassler) R. K. Jansen(2x*).-30. A. glaberrima (Griseb.) R. K. Jansen(2x).-29. A.psilocarpa 28. A. alpestris series R. K. Jansen(2x). Characters.-Taken fromJansen(in press) withthe followingchanges:transformation series 11 and 12 werecombined 13-15 wereeliminatedbecause I felttheywerethesame as 20-22; transformation series withtwo independentapomorphies. Data matrix.-The apomorphies of transinto one transformation series 2, formationseries 8, 11, and 21 were all treatedas independentof one anotherwhile in transformation 17,and 18,apomorphy1 is ofintermediatenaturebetweentheplesiomorphiccharacterand theotherapomorphy, 2. For Figure 56.
Apomorphies Taxa 1 2 3a 3b 4 5 6 7 8 9 10 11 12a 12b 13 14 15a 15b 15c 16a 16b 18 19 20a 20b 21 22a 22b
1
1 1 1 1 1 1 1 1 1 1 1 1
2
3
1 1 1 1 1 1 1 1 2 2 2 1
1 1 1 1 1 1 1 1 1 1 1 1
4
5 1
6
7
1
8
9
1
1
10
1 1 2 2 2
1
17
18
19
1 1 1 1 1 1 1 1 1
1 2
20
2 2
1
1 1 2 2 2 2
1
16
1
1
1 1
11
1 1
1 1
1 1
1 1
1
1 1
1
2 2 2 2 2 1 1
1
1 2
21
22
1 3
1 1 1 1
3 3 3 3 2 2
2
2 1 2 2 1
3
2 2 2 2 1
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
1
1 1 1
715
FUNK-HYBRIDIZATION
1985] APPENDIX S.
Continued. Apomorphies
Taxa 22c 23a 23b 24 25 26 27 28 29 30
1
2 1
3 1
4 1 1 1 1 1 1 1 1 1
5
6 1 1 1
1
7 1 1 1 1 1 1 1 1 1 1
8
9
10
11 2
1
16
17
18
19
20
21
1
1 1 1
3 3 2
22 1 1 1 1 1 1 1 1 1
