evolutionary analysis of five bryophyte families using ... · textbook examples of the former are...

Evolutionary analysis of five bryophyte families using virtual fossils

by

Richard H. Zander

Missouri Botanical Garden, P.O. Box 299, St. Louis, MO 63166-0299 U.S.A. [email protected]

Anales del Jardín Botánico de MadridVol. 66(2): 263-277

julio-diciembre 2009ISSN: 0211-1322

doi: 10.3989/ajbm.2224

IntroductionIt has long been recognized that phylogenetic

analysis does not model evolution of sequences ofnamed ancestral and descendant taxa, i.e. genealo-gies, but demonstrates the evolution of characteristicsas branching lines of trait changes (e.g., Bowler, 1989:345-346; Farjon, 2007; Hörandl, 2006, 2007) for ex-emplars of named terminal taxa. Of three particulartaxa, two are more likely to share an ancestor but thatancestor is generally not identified as a taxon differentfrom its descendants; it is simply represented in phy-logenetics by an unnamed node, or “common ances-tor” of descendant lineages. When fossils are at hand,however, they are potentially more informative of evo-

lution as descent with modification (Hall, 2003) oftaxa because bioroles may be inferred from expressedtrait combinations. In phylogenetic analysis, ancestralmapped morphological or molecular traits, thoughpresented as sequential, remain atomized. Attemptsto infer soft tissues in geologic fossils also deal with in-dividual traits. For instance, in extant phylogeneticbracketing (Witmer, 1995, 1998), a fossil lineagebracketed by two lineages each sharing one particulartrait in their extant taxa would be expected to alsohave that trait, but features not present in both brack-eting lineages would be expected to be absent in thefossil. This method does not rely on and explain, how-ever, para- or polyphyly.

Resumen

Zander, R.H. 2009. Análisis evolutivo de cinco familias de briofi-tas empleando fósiles virtuales. Anales Jard. Bot. Madrid 66(2):263-277 (en inglés).

Los táxones parafiléticos o polifiléticos tradicionales en un árbolmolecular filogenético pueden interpretarse como poblacionesde ancestros supervivientes que están evolutivamente estáticosen los caracteres expresados a través de lábiles en los caracteresADN que se emplean para seguir la continuidad genética. Enesos casos en los cuales la re-evolución (convergencia) de talestáxones se considere improbable, la heterofilia puede usarsepara inferir series evolutivas de fósiles virtuales que reflejan lamacroevolución. El descenso con modificación de táxones se de-muestra con la interpretación publicada de los cladogramas deestudios moleculares de Dicranaceae, Pottiaceae, Grimmiaceae,Hypopterygiaceae y Mniaceae como árboles taxonómicos. Envista de este argumento, resulta que los ancestros inferidos su-perimpuestos apoyan la teoría del equilibrio puntuado.

Palabras clave: fósil virtual, heterofilia, equilibrio puntuado, ár-bol taxonómico, evolución, autofilético, Grimmiaceae, Hypop-terygiaceae, Mniaceae, Pottiaceae.

Abstract

Zander, R.H. 2009. Evolutionary analysis of five bryophyte fami-lies using virtual fossils. Anales Jard. Bot. Madrid 66(2): 263-277.

Traditional taxa paraphyletic or polyphyletic on a molecularphylogenetic tree may be interpreted as populations of surviv-ing ancestors that are evolutionarily static in expressed traitsthough labile in DNA traits used to track genetic continuity. Inthose cases in which re-evolution (convergence) of such taxa isdeemed improbable, such heterophyly may be used to inferevolutionary series of virtual fossils reflecting macroevolution.Descent with modification of taxa is here demonstrated by rein-terpreting published cladograms of molecular studies of Di-cranaceae, Pottiaceae, Grimmiaceae, Hypopterygiaceae, andMniaceae as taxon trees. Given this argument, superimposedinferred ancestors are support for the theory of punctuatedequilibrium.

Keywords: virtual fossil, heterophyly, punctuated equilibrium,taxon tree, evolution, autophyletic, Grimmiaceae, Hypoptery-giaceae, Mniaceae, Pottiaceae.

R.H. Zander

Of particular importance for the present analysis isthe idea that a split in a molecular lineage is not nec-essarily a speciation event. It could signal any isola-tion event, sometimes followed by phenotypic stasisof the isolated population, resulting in a surviving an-cestor. Identification of a surviving ancestor as a kindof living fossil may be done by (1) identification of ageologic fossil with an extant taxon; (2) biosystemat-ic and cytogenetic studies, particularly in the case of“quantum” or local evolution (Lewis, 1962; Grant,1971; Levin, 2001), the budding of a descendantspecies from a peripheral ancestral population,which are identifiable, for instance, as in the event ofapparent daughter species being all more similar toan apparent parent than to each other; (3) the recentmethod of Theriot (1992) inferring a surviving ances-tor in a group of diatoms by evaluating a morpholog-ically based cladogram and biogeographical informa-tion; (4) the somewhat more simplistic and problem-atic selection of a surviving ancestor as one lackingautapomorphies on a polytomous morphologicalclade (Wiley & Mayden, 2000: 157; discussion byZander, 1998); or (5) the method of virtual fossilsused here.

When exemplars of different taxa are clustered to-gether on a molecular tree, it is impossible to satisfac-torily infer the phenotype of the shared ancestor orancestors. It could be the phenotype of any one of theexemplars or even of a taxon of entirely different phe-notype. When exemplars of the same taxon are clus-tered together on a molecular tree, it is straight-for-ward to infer that the phenotype of the immediateshared ancestor is that of the exemplars, rather thanall exemplars resulting from multiple convergencesfrom an ancestor of a different phenotype. If the ex-emplars are all one species, the ancestor is thatspecies. If they are of different species of one genus,the ancestor may be inferred to be that genus; or ifgenera, then their family, and so on. If two such clus-ters are sister groups, one may infer a particular an-cestor for each of both clusters, but the phenotype ofthe immediate shared ancestor of the two clusters isimpossible to infer. It could be one or the other or adifferent extinct or unstudied taxon of perhaps inter-mediate phenotype.

A solution may be found if exemplars of the sametaxon are separated by a lineage of a different pheno-taxon. And in spite of such separation (phylogeneticdisjunction) on a cladogram the exemplars of the for-mer paraphyletic taxon, when examined for possiblemistaken taxonomy, remain assuredly that taxon. Giv-en that the circumscription of traditional phenotaxa,at least those of modern studies, commonly involve

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Anales del Jardín Botánico de Madrid 66(2): 263-277, julio-diciembre. ISSN: 0211-1322. doi: 10.3989/ajbm.2224

conservative, gapped phenotypic traits, and that totalconvergence or crypsis is improbable or less probable(Jardine & Sibson, 1971: 144) than other explana-tions, simply enforcing monophyly by taxonomicallyrecognizing cryptic species, genera or families may beless productive scientifically than examining other ex-planations. The point of traditional taxonomy is tomake complete evolutionary convergence improbable,and this applies at any taxonomic level. Classificationis here presented as a major source of informationabout evolution needing only reliable information ongenetic continuity to reveal taxic steps. Even morpho-logical phenocopy involving two or more taxa thatlose traits when highly reduced (e.g. in high elevationhabitats) commonly allows retention of one or moreconservative traits that allow accurate identification(Zander, 1977: 261), or when unidentifiable, it is be-cause the reduced plants are intermediate or general-ist in form. Thus, Dollo’s Rule (Hall, 2003) is at leastmethodologically applicable at the organismal level ofa unified combination of traits, while many individualmorphological characters may be quite homoplastic(Endress, 1996: 313).

The null hypothesis is a fully nested set of pheno-taxa, without indication of descent with modificationof such taxa (Fig. 1). The null hypothesis for the evolution of expressed traits in a genus is that anyphenospecies may be derived from any other in spiteof any inferred phylogenetic trees, which give no def-inite information on the phenotype of any ancestor.Falsification of that null is demonstration of one ormore phenoancestors diagramed (e.g., Fig. 5) by mov-ing these (along with all descendants) out of the groupas a linked sequence, and leaving a “residuum” of un-ordered taxa. By extension, with less resolution, onephenogenus of a family may be derived from any oth-er, unless an ancestor is demonstrable.

When exemplars of the same taxon (particularly ofthe same species) are distant from each other on amolecular tree, being separated by other taxa at leastas sister lineages, the homoplasy is commonly eitherexplained as (1) evidence of that taxon or somethingquite like it being basal or ancestral to a portion of thecladogram, or (2) cryptic or sibling taxa that need dif-ferent taxonomic names. Textbook examples of theformer are given by Futuyma (1998: 456, 470), citingMoritz & al. (1992) where coastal and Sierran Cali-fornian subspecies of the salmander Ensatina es-chscholtzii “appear to have been derived from” subsp.oregonensis, and citing Hey & Kliman (1993) and Kli-man and Hey (1993) for the Drosophila melanogasterspecies group where the paraphyletic D. simulans“gene copies are traced back to a ‘deeper’ common

ancestor than in any other species.” Rieseberg andBrouillet (1994) discuss mechanisms for evolution of monophyletic daughter taxa from paraphyleticparental taxa through geographically local models ofspeciation. All this assumes that the molecular analy-sis has accounted for any homoplasy introduced intothe analysis by inappropriate technique, e.g. wrongmodel (Alfaro & Huelsenbeck, 2006) or inappropri-ate data, e.g., incomplete concerted evolution (Doyle,1996).

Nelson & al. (2003) refuted Brummitt’s (2002) as-sertion that paraphyly implies an ancestor. They as-severate that “In practice, extinct ancestral taxa areseldom of concern, because organisms credibly repre-senting them are seldom if ever in hand.” Here Istrongly suggest that exemplars of the same taxon thatare distant on a molecular phylogenetic tree are cred-ible representatives of ancestors of themselves and alllineages intermediate on the cladogram. An extensivediscussion of paraphyly and the possible inference ofancestry is given by Wiley & Mayden (2000), whowrote: “Only the paraphyletic taxa of evolutionarytaxonomy can be ancestors”. It is clear, however, thatif evolution is descent with modification, particularlyof taxa rather than traits, then sister-group analysis(cladistics) is only an indirect guide to evolution,while ancestor-descendant relationships are direct in-ferences of evolution.

Although imputing an ancestral status to para-phyletic taxa is not particularly new, a formal methodfor using heterophyly (i.e., either paraphyly or poly-phyly) as it implies an ancestor surviving in two ormore isolated populations that may be used as a virtu-al fossil embedded in a molecular phylogenetic tree,ancestral to all dependent (more terminal on the tree)lineages on the cladogram, to create evolutionary ortaxon trees. The alternative hypothesis is illustrated

Evolutionary Analysis

by Fig. 2; for traditional taxa A and X, phenotaxon A*is ancestor of exemplars A1, X, and A2. Exemplar X isinserted to indicate that heterophyly is methodologi-cally allowable though X is not strictly necessary forinference of the virtual fossil A*, but heterophylydemonstrates any descendents of the virtual fossil be-yond the exemplars of the same taxon. The same kindof inference may be made for phenotaxon B, and thenancestors A* and B* are sequentially ordered on amolecular cladogram as diagramed in Fig. 2 to infermacroevolution on the molecular tree. Convergenceor parallelism occurring to develop what is essentiallythe same taxon two or more times from a differenttaxon or taxa, short of orthogenesis (an internal evo-lutionary goal), is here taken to have a much lowerprobability than existence of populations of survivingancestors. Although evolution of trait combinations isdoubtless ergodic (all possible combinations ex-plored, including duplication), evolutionary stasis ofeach of two isolated populations I believe is more ac-ceptable an explanation of heterophyly given thatmany traits, particularly those at higher taxonomiclevels are chosen as important in taxonomy for theirconservative nature, perhaps because their DNA ismore vigorously repaired than that of other traits.Trait combinations, judging from evaluations of fossilgroups over time in the literature, apparently divergefrom a “root” combination in a kind of drunkard’s

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Anales del Jardín Botánico de Madrid 66(2): 263-277, julio-diciembre 2009. ISSN: 0211-1322. doi: 10.3989/ajbm.2224

Fig. 1. A diagram of the null hypothesis of all taxa nested be-cause no evolutionary ordering of phenoancestors is inferable.Molecular lineages can provide continuity between ancestorsbut the phenotype (resolvable at some taxonomic level) of an-cestors is unknown beyond the general feeling that ancestorsshould be somewhat similar to nearby exemplars.

Fig. 2. Demonstration cladogram of sequential evolution of taxaas inferred from heterophyly on a molecular cladogram. Exem-plars A1 and A2 , and B1 and B2 allow inferences of virtual fossilsA* and B*, exhibiting sequential evolution of taxa A* from B*(when cladogram is rooted below B*). Exemplars X and Y are in-terspersed to signal heterophyly in this contrived example. Alter-natively, again as a demonstration, A* and appended lineagescould replace Y, as a different but expected form of evolutionarynesting, with the molecular cladogram indicating the correct se-quence.

walk (divergence distance a function of the squareroot of elapsed time), restricted only by phylogeneticconstraint (limitation on evolution of one complex or-ganism into another of much different complexity)and selection on some of the traits or their combina-tions. Conservative traits, phylogenetic constraint,and a general slow divergence of trait combinations(except for static populations) act against fully crypticconvergence in spite of clear convergence of sometraits in response to adaptation to similar environ-ments.

The idea that sister lineages must have differenttaxonomic names if there is a split in a molecular treeis purely definitional, because isolation does not en-sure speciation unless speciation is simply defined asisolation, and anagenesis is conceived in molecularphylogenetics as any changes in DNA, including non-coding. In the present paper a molecular tree demon-strates genetic continuity of lineages (to the extent it isreliable), but not necessarily series of speciationevents. Macroevolution is best described by descentwith modification of taxa, not morphological traits at-omized on molecular tree.

An example of heterophyletic information on evo-lution is the increasingly common discovery of whatare generally viewed as phylogenetically isolated cryp-tic species, e.g. the 14 cryptic or nearly cryptic speciesof bryophytes recently found in mosses by Shaw(2001), also the cryptic species of Hedenäs (2008) and

R.H. Zander

Hedenäs and Eldenäs (2007), but which are moreprobably surviving phylogenetically and geographi-cally disjunctive populations of shared ancestors. Theisolated populations accumulate different DNA mu-tations over time but may be morphologically staticthrough time through some process like stabilizingevolution (Foote & Miller, 2006). Persistence of someor even a great proportion of evolutionarily staticpopulations or species (Guillaumet & al., 2008;Leschen & al., 2008; Shen & al., 2008) is implied bythe increasingly supported punctuated equilibriumtheory of Eldredge and Gould (1972), Gould &Lewontin (1979), and Gould & Eldredge (1977,1993), which may be valid for many or most taxa,though gradual (Futuyma, 1998: 114) or stepwisetransitions have been demonstrated (e.g., Deméré &al., 2008; Benton & Pearson, 2001).

The present paper emphasizes virtual fossils at thegenus level and above. Do supraspecific taxa evolve?Discussions of selection at the genus level and aboveare given by Rensch (1960) and Stebbins (1974),while Stanley (1975) has promoted the idea of speciesselection, with differential speciation rates for differ-ent species favoring those with high speciation rates,a kind of natural selection operating on species insupraspecific taxa rather than individuals in a po-pulation. In the present paper, readers may view vir-tual fossils as either simply representing populationsor species evolving in the past, or as higher taxaevolving by selective extinction of species, with re-sults similar to balancing, directional and disruptiveselection.

An autophyletic taxon is one that causes anothertaxon to be paraphyletic because of its recognition ata particular rank, a taxonomic level that indicates evo-lutionary importance due to particular unique au-tapomorphic traits. In a new classification of mossesby Goffinet & al. (2008), although the family nameEphemeraceae is used in their introduction in discus-sion of the evolutionary importance of its autapomor-phies, that name is entirely suppressed in the actualclassification apparently because those autapomor-phies are of no value in determining sister-group rela-tionships (i.e., are not phylogenetically informative).Two other families, Cinclidotaceae and Splachnobry-aceae are entirely absent (the classification lacks syn-onymy) apparently because their exemplars areimbedded in the Pottiaceae in other studies, thusmaking them autophyletic and the Pottiaceae para-phyletic. The loss of evolutionary information on ancestor-descendant relationships (Dayrat, 2005)flagged by these names apparently solely due to en-forcement of strict monophyly is particularly trou-

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Fig. 3. Demonstration cladogram of a “double ancestor” oroverlapping virtual fossils that may be explained by, in this in-stance, a very short and unresolved branch connecting B* andC*, due perhaps to punctuated equilibrium rather than doubleconvergence. Exemplars C1 and C2, which are paraphyletic be-cause of autophyletic exemplar Z, which is sister to C1, infer an-cestor C*, which itself is embedded in or overlapping of ancestorB*, inferred from phylogenetically disjunct exemplars B1 and B2.

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bling as taxonomic classifications inform other fields,such as biodiversity studies, evolution, biogeography,and ecology.

Methods

The present method uses heterophyly of phenotaxato infer a surviving ancestor (Zander, 2008b) with in-between (bracketed) lineages seen as descendants. Es-sentially, if one can map morphological traits proba-bilistically on a molecular tree, then mapping naturaltaxa on a molecular tree as composites of many ex-pressed traits is only prevented by intransigent insis-tence on phylogenetic monophyly, an artificial classifi-cation system. Thus, two exemplars of one speciesthat are separated on a molecular tree by an exemplarof a different phenospecies imply a shared ancestor ofall three that is identical or nearly identical to the twoisophenes. A surviving ancestor at the genus level isimplied by two phylogenetically disjunctive (distanton a cladogram, heterophyletic) species of the samegenus. Minimally, a phylogenetic disjunction involves

two exemplars of one taxon with an exemplar of a dif-ferent taxon as sister group to one of them. The nullhypothesis (or state of nature) is that there is no phe-notypic descent with modification inferable, and allphenotaxa are completely nested (Fig. 1). This is falsi-fied by demonstration that one of the extant pheno -species represented by a pair of surviving ancestorsdistant on a molecular tree, implying a virtual fossil is“buried” in the cladogram, and any other taxa be-tween the two exemplars on the molecular tree are de-scendants. Molecular phylogenies provide the conti-nuity that allows creation of a taxon tree, which is a se-quentially organized, sometimes branching, ancestor-descendant diagram of named, diagnosable taxa. It isa phylogeny but not a cladogram in the sense that evo-lutionary relationships of taxa represented by exem-plars are sequential, not based on relative distancefrom shared unnamed ancestors.

Given the assumption that surviving taxa are moreprobable than convergence of taxa, rejection of thevirtual fossil requires demonstration that the phyloge-netically disjunctive isophenotype exemplars are dif-

Fig. 4. Cladogram showing position of Dicranaceae virtual fossil(starred), and best resolvable taxon tree for Dicranaceae and de-scendant moss families. See text for details of trait changes in-volved in macroevolution of these taxa.

Fig. 5. A taxon tree (stylized Besseyan cactus) of the Pottiaceae,showing heterophyletic ancestral taxa (starred) some of whichare ancestral consensus taxa (“residua”) of assorted species (andsometimes genera) that cannot be further internally evolutionar-ily ordered from available data. Many exemplar species (notshown) are also attached variously about the taxon tree, andmay be inferred from the cladogram of Zander (2007a) or Wern-er & al. (2005).

ferent at the species level (minimally following a dif-ferent evolutionary track involving the phenotype, orsome other species definition that is not merely de-fined by a split in a morphological or molecular tree),or come from different ancestors. Sometimes disjunc-tion of exemplars of what are only apparently thesame taxa (species, genera, etc.) on a cladogram mayrepresent taxa that should, after judicious considera-tion, be taxonomically separated into two. One mustbe aware, however, that any small number of, for in-stance, species might be split randomly into twogroups and “generic descriptions” written that osten-sibly describe such groups (in the main, and withsome contrary traits explained as “reversals”), butsuch morphology may not comprise a robust pheno-typic genus with conservative characteristic traitsmore or less well gapped from related genera, com-monly with a distinct evolutionary biorole. Althoughthe importance of gaps between taxa in taxonomy issometimes deprecated as simply relying on ignorance,particularly when geologic fossils are part of an evolu-tionary analysis (Gauthier, 2001: 33), an evolutionarybased taxonomy should reflect the present day resultsof selection, not simply inferred genetic continuity.Extinct taxa based on geologic fossils, though per-haps well gapped from similar taxa in their day, havetrait combinations that reflect evolutionary advan-tages of past bioroles in long gone habitats and com-petitive situations, and need to be fit as best possibleinto present classifications as somewhat evolutionari-ly incongruent. An evolutionary taxonomy should beexpected to change with geologic time.

Apparent homoplasy of traditional groups, some-times ingenuously characterized as “massive,” in anymolecular cladogram signals a possible survivingspecies, genus, family or other taxon (Zander 2007 b,

R.H. Zander

c). Inferential demonstration of two ancestral pheno -species is made by the presence on a molecular tree oftwo pairs of such individually phylogenetically isolatedisophenes, implying two different ancestors, these,ideally, ordered to show sequential evolution of onefrom the other. With enough data, this can be extend-ed to identification of many ancestral species in thegenus. Such ancestral phenotypes lead to a tree of vir-tual fossils, or a taxon tree, for instance exemplified asa “Besseyan cactus” (Bessey, 1915; Zander, 2008b),perhaps, with enough data, along the lines of the im-pressive geologic fossil-based horse genealogy present-ed by Futuyma (1998: 141) based on McFadden(1992). The analysis may be extended to higher taxo-nomic categories demonstrating multiple ancestors re-solvable only at the phenotypes of the higher taxo-nomic categories, where the virtual fossil is identifiableonly to genus or higher. Clearly, to use the method, onemust view heterophyly and homoplasy involving iso-lated populations leading to apparent molecular paral-lelism or convergence as a common and expected re-sult of evolution (or sometimes non-evolution) of taxa.With study of increasing numbers of exemplars of par-ticular taxa in any one molecular analysis, particularlyof geographically isolated populations or morphologi-cally distant species, a complex tree of sequential evo-lution of taxa may be demonstrated.

Two kinds of ancestral taxa can be inferred for thetaxon tree. (1) A poorly resolved consensus taxon,which is basically the diagnosis of the next higher tax-onomic category of a mixed group of phenotaxa forwhich the evolutionary sequence is unknown. A con-sensus ancestral taxon is simply the null hypothesis of no evolutionary order based on expressed traits, a nesting of all taxa, as in Fig. 1 and identified as a“residuum” in other figures given here. (2) Survivingancestors from which may be inferred an identical ornearly identical paraphyletic or even phylogeneticallypolyphyletic ancestor of the same rank. This wouldbe, for example, one or more ancestral species in agenus, or ancestral genera in a subfamily or family. Allsuch phenotype ancestors may be arranged in pro-gressive evolutionary diagrams with the help of reli-able molecular trees (Zander, 2007a). Cronquist(1975) contended that parallelism among closely re-lated taxa is of no import or consequence in taxono-my, and can be ignored. This agrees with the presentpaper in that parallelism implies no important ex-pressed evolutionary feature that must be reflected intaxonomy. Cronquist (1987) also supported recogni-tion of paraphyletic groups. A critique of his paper byDongoghue and Cantino (1988) asserted among oth-er things that paraphyletic groups “do not serve as an-

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Fig. 6. Grimmiaceae taxon tree based on Hernández-Maqueda& al. (2008). Heterophyletic inferred ancestors are starred.

cestors, and are unacceptable in the phylogenetic sys-tem.” The present paper rejects the former with aclear alternative, and suggests that the phylogeneticsystem cannot adequately portray evolution. Whenmorphological and molecular data agree, they maysimply be subject to the same bias (neutral evolution,adaptive selection, and even convergence), but whenthey disagree (and are not simply due to error) thennew information may sometimes be deduced.

Molecularly heterophyletic taxa can provide evolu-tionary data just as parsimoniously informative traitsprovide phylogenetic data. Phylogenetically poly-phyletic taxa are not of necessity evolutionarily poly-phyletic – if the phylogenetically disjunct exemplarsare determined to be surely the same taxon in pheno-type, then the inferred phenotypically identical ances-tor of these surviving populations completes the lin-eage as evolutionarily monophyletic in the sense of be-ing coherently ordered. When one or two lineages ofa phylogenetically split taxon are renamed to enforcemonophyly, however, as is now common practice,evolutionary data is unfortunately hidden. There is noempiric evidence supporting phylogenetic monophy-ly as a thing in nature. On the other hand, reinterpret-ing cladograms with somewhat older nomenclaturethat reflects morphology (or phenology, to includebiorole) alone will best preserve evidence of hetero-phyly and its evolutionary information.

The reliability of any pair of heterophyletic lineages(or exemplars) implying a surviving ancestor dependson the joint probability of the two lineages being in-deed phylogenetically monophyletic and disjunctfrom each other by at least one internode (which sup-ports a different taxon as a descendant). For example,in the cladogram ((A1, B) A2) C, for two exemplars ofspecies A, namely A1 and A2, to be patristically distantby one internode such that they imply a shared ances-tor A with B, depends on the probability of A1 and Bbeing sister groups on a molecular tree, while A1 andA2 must also be involved in calculation of joint proba-bility if these are lineages of multiple species and thereis uncertainty that these are not phylogeneticallymonophyletic. In the preliminary survey here, reliabil-ity is commonly quite good for most virtual fossil in-ferences but, because the method is new, statisticalpower in distinguishing possible evolutionary featuresis emphasized over reliability of the taxon tree (seediscussion of statistical power by Zander, 2007a).

For this study, several published cladograms wereexamined to search for inferable sequential evolution-ary relationships from evidence of surviving ances-tors.


Results

The evolutionary diagrams or taxon trees (Figs. 4-6) combine consensus ancestral taxa (labeled as“residua”) with those inferred from heterophyly,which differ in being evolutionarily resolved throughinference of descent with modification of taxa. Theancestral taxa are linked using the genetic continuityprovided by phylogenetic information from molecu-lar analyses. Examination of published moleculartrees and exemplars named as traditional taxa com-monly demonstrates cladistic splitting of what areprobably ancestral taxa at various ranks surviving tothe present. With increasing numbers of exemplars of particular taxa in recent molecular analyses, thisshould become more evident. In the figures givenhere, all linkages are well-supported in the molecularanalyses of the literature on which they are based, andthe here-inferred virtual fossils are denoted with astar.

Zander (2008a) found that the Dicranaceae was theparaphyletic ancestor of two phylogenetically disjunc-tive and well-supported reciprocally monophyleticclades, the Dicranaceae s.str. and a lineage of general-ly small-sized taxa commonly referred to in phyloge-netic literature as the “Rhabdoweisiaceae” but withno agreed upon morphological diagnosis to distin-guish it from the Dicranaceae. Dicranaceae is here de-scribed as a virtual fossil (conceivable as one or morepopulations resolved only with the morphology of thisfamily), and ancestor of the genera Amphidium andFissidens, and the families Calymperaceae, Grim -miaceae (as Grimmiales), Leucobryaceae, and the Er-podiaceae and Pottiaceae together sharing a lineage(Fig. 4). Of course, the few exemplars provide poorsampling of the whole family, but may be consideredsufficient statistics for the phenotypic center of thefamily. Thus, the more advanced members of the Di-cranaceae, characterized by a morphological mainline of evolution (Crum & Anderson 1980) of narrow,tapered leaves with a strong, single costa and often in-flated alar cells, and flat, forking peristome teeth thatare vertically pitted-striolate, gave rise to the (1) Leu-cobryaceae, with glaucous leaves, leaf hydroid strandabsent, costa very broad, laminal cells strongly differ-entiated into chlorophyllose and hyaline cells; and (2)Calymperaceae, with stem central strand absent, lam-inal cells sometimes papillose, hyaline cancellinae jux-tacostally, peristome of 16 segments that are variouslyornamented; and (3) Erpodiaceae, being cladocarpic,lacking a costa, laminal cells commonly papillose; and(4) Pottiaceae, with twisted peristome, and leaveswith enlarged basal cells and papillose distal cells. Theless advanced members of the Dicranaceae that gave

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rise to Amphidium, Fissidens, and Grimmiaceae arepresently much reduced in morphology and it may bepresumptuous to detail trait changes. A main evolu-tionary theme, therefore, among families evolvingfrom Dicranaceae involves differentiation and elabo-ration of laminal cells (and often the costa) by infla-tion or ornamentation.

Phylogenetically disjunct taxa in molecular studiesof Werner & al. (2004) and Werner & al. (2005) of thePottiaceae were translated into virtual fossils andthese figured as a “Besseyan cactus” by Zander(2008b) but here presented more simply (Fig. 5). Thebasal “Pottiaceae residuum” is an unordered groupout of which many Pottiaceae taxa have been isolatedas virtual fossils (starred). It is established by thestrong disjunction on the phylogenetic tree of Tim-mielloideae and the remainder of the Pottiaceae (Zan-der, 2007a). The Timmielloideae are derived from themost basal elements of Pottiaceae through elabora-tion of the laminal cells and reversal of peristometwist; together with the at least tentative identificationof Pseudocrossidium as having the apparently primi-tive traits of broad leaves, commonly ovate to ellipticleaves, rather small distal laminal cells, small size orabsence of the adaxial costal stereid band, crescentshape of the abaxial stereid band, and lamina yellowor orange (with occasional red spots) in KOH; and di-rectly giving rise to Trichostomoideae (narrow, planeor marginally incurved leaves with two stereid bands),Pottioideae (broad leaves with recurved margins).The Ephemeraceae (highly reduced morphologicallyand adapted to evanescent moist habitats) is derivedfrom elements of the Trichostomoideae.

Three species of Barbula are heterophyletic in thesame manner as Pseudocrossidium species, with B. bol-leana (Müll. Hal.) Broth. (B. sect. Hydrogonium) andB. indica (Hook.) Spreng. (B. sect. Convolutae) placedwith the Trichostomoideae, and B. unguiculata Hedw.(B. sect. Barbula) with the Pottioideae. The hetero-phyly plus the fact that the laminal margins are flat insections Hydrogonium and Convolutae like those ofTrichostomoideae, but recurved in sect. Barbula asper Pottioideae, indicated that the two sections of Bar-bula may represent to different genera. A study, how-ever, rejects this in that all species are correctly placedin Barbula, or at least the Pottioideae, by the stem sec-tion with strong sclerodermis, large cells of outer cen-tral cylinder grading into smaller cells within and astrong central strand, leaves deeply grooved along theadaxial surface of the costa, differentiated basal lami-nal cells extending farthest distally midway betweencosta and leaf margin, and hydroids evident in thecostal section. This is opposed to the Trichosto-

R.H. Zander

moideae’s stem section showing poor sclerodermisdevelopment, nearly homogeneous central cylindercells and a small or absent central strand, leaves shal-lowly channeled adaxially, differentiated basal laminalcells commonly extending to a greater or lesser extentup the margins, and hydroids usually lacking in thecosta. Thus, both Barbula and Pseudocrossidium rep-resent deeply buried ancestral taxa, resolvable only asBarbuleae, which would then be the ancestral groupof the remainder of the tree (an unordered group dis-tinguishable only as Pottioideae but with Pottieae ap-parently derived from Barbuleae), including the Cin-clidotaceae.

In the Trichostomoideae, Pseudosymblepharis is de-rived from Trichostomum tenuirostre through Chio -noloma by narrowing of the leaves (narrowest in Pseu-dosymblepharis), thickening of the cells of the stemcentral cylinder, thickening of the ventral costalstereid band, elaboration of basal laminal cells, andapparently convergent (with Tortella) elaboration ofthe marginal band of hyaline cells. Arising from theTrichostomoideae residuum by monoicy, sharply in-curved distal laminal margins, and adaxially bulginglaminal cells, Weissia controversa Hedw. is apparentlythe ancestor of a number of species of Weissia (notshown). From the Tortella residuum, T. tortuosa(Hedw.) Limpr. and T. fragilis (Drumm.) Limpr. joint-ly (as a poorly resolved ancestor) give rise to T. incli-nata; note that T. fragilis may be easily mistaken for T.tortuosa when young (Eckel, 1998) and thus the poorresolution here may be in identification of the exem-plars. Pleurochaete is clearly derived from Tortella,though not directly from T. tortuosa, through pleuro-carpy and elaboration of the hyaline band of marginallaminal cells that does not meld with the basal cells.

Descendents of the Pottioideae include: (1) thefamily Cinclidotaceae, adapted to aquatic or other-wise hygric habitats; (2) the Barbuleae, with narrow,marginally recurved leaves having two stereid bandsleading to Leptodontieae, which have squarroseleaves, commonly lack a stem central strand and ven-tral costal epidermis, and have reduced peristomes;and (3) the Pottieae, with broad leaves and one costalstereid band, from which are derived Tortula, withstem sclerodermis and hyalodermis both absent, cos-ta transverse section and dorsal stereid band bothrounded, hydroid strand usually present, distal por-tion of leaves KOH yellow, peristome and capsule in areduction series, which is itself the ancestor of Chenia,characterized by leaves with sharply pointed marginalteeth ending in a papilla but laminal cells mostlysmooth, leaf ending in a more or less distinct spinosecell with thickened walls, upper portion of leaf KOH

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red. The overall taxon tree seems to fit in broad out-lines the morphological cladogram of the family byZander (1993), but of course the latter does not iden-tify ancestors.

Certain families in Fig. 5 (as “Dicranaceae and oth-ers”) appear to arise from the Pottiaceae residuum, in-cluding the Dicranaceae, Fissidentaceae, Grimmi-aceae, Ptychomitriaceae, Seligeriaceae, and War-diaceae. These apparently contradict Fig. 4, which de-rives Pottiaceae from the Dicranaceae. This is becausethe Timmielloideae are more basal than these familiesby one reliable internode in the analysis of publishedmolecular cladograms by Zander (2007a), on whichFig. 5 is based, while Fig. 4 does not include thestrongly basal Timmielloideae in its molecular dataset. If Timmielloideae were included in Fig. 4, itwould doubtless be basal to the Dicranaceae, possiblyresulting in a “double ancestor” (diagramed in Fig. 3and see discussion) of internodes of Dicranaceae mor-phology inserted as a unit within the lineage of Potti-aceae morphology. Such double or superimposed an-cestors may be best explained by rapid bursts of evo-lution and associated unresolved short branches cou-pled with long stasis of isolated populations, confusedin analysis by long-branch attraction. In fact, such ful-ly collapsed nested ancestry would be an expectedoutcome of punctuated equilibrium combined withmultiple isolated static populations, and may be takenas additional evidence in support of that theory. Muchnesting due to collapse because of many short branch-es may be a measure of the relative amount of punctu-ated equilibrium versus gradual change. Additionalexplanations that might be explored are ancestral bal-ancing selection, long-term or latter-day low levels ofhybridization between isolated populations, or aproblem with analysis of genetic continuity such aslack of data resulting in an unresolved phylogeneticbranch connecting the Pottiaceae and Dicranaceaevirtual fossils, or data-destroying extinctions, or bymore exotic possibilities such as lateral gene transfer,or epigenetic reversion by reactivation of silencedgenes (Caporale, 1993, 2003; Zander, 2007d). Thepossibility of explanations alternative to convergence,or in this case double convergence, must be counte-nanced, even though convergence as parallelism froma shared ancestor (B* or C*in Fig. 3) is quite possiblethrough two or more identical events of allopoly-ploidy over time, or when the same niche is twice in-volved in speciation from the same ancestor. Certain-ly additional data should be pursued to help resolvethis problem. The particular scientific interest in thisdiscrepancy lies in examination of various mecha-nisms that explain such contradiction. The use of het-


erophyletic exemplars as evolutionary information isstill in early days.

Examination of a study (Hernández-Maqueda &al., 2008) of genera of the moss family Grimmiaceaeand related families allowed inference of a rather un-ambiguous or well-nested evolutionary taxon tree(Fig. 6) of heterophyletic taxa. The Grimmiaceaeresiduum brackets on the molecular tree and is the an-cestor of (i.e., is heterophyletic and includes as de-scendant lineages), Campylosteliaceae and Ptychomi-triaceae (bracketed by Jaffueliobryum and Indusiella)while Grimmia brackets Schistidium and Coscinodon.The latter brackets Hydrogrimmia.

In a study of the moss family Hypopterygiaceae,Shaw & al. (2008) analyzed six nuclear, plastid andmitochondrial nucleotide sequences of 32 exemplarsand found that of four species of Cyathophorum, twowere paired near the base of the strongly supportedcladogram and two were buried deeply among 10 ex-emplars of the genus Hypopterygium. Although Shaw& al. chose to simply transfer the two species bracket-ed in Hypopterigium to that genus to preserve mono-phyly, it is clear that the cladogram is also evidence ofCyathophorum being a heterophyletic genus ancestralto several genera bracketed by it in the cladogram (Ar-busculohypopterygium, Canalohypopterygium, Catha -rom nion, Dendrohypotperygium, Hypopterygium, Lo-pidium) while itself has one of these (Hypopterygium)as ancestor of two of its species. This scenario may bedescribed as another “double ancestor” (see Fig. 3)similar to that discussed above with Dicranaceae andPottiaceae. In any case, there are two reasons not toaccept the transfer of the two species of Cyathopho-rum to Hypopterygium: (1) preserving phylogeneticmonophyly is insufficient reason not to recognize dif-ferences at the genus level (particularly when the samelevel of difference is recognized elsewhere in thecladogram), and (2) inference of a shared isopheno-typic ancestor is an explanation far more plausiblethan total re-evolution of a combination of several ma-jor morphological traits (including anisophylly anddifferentiated laminal border) to converge at thegenus level, when such a combination of traits isknown to be so conservative as to be valuable ta-xonomically. Although a two or three unique traitsmay be assigned to the two autapomorphic Cya tho -phorum species, the possibility that these are simplyrandomly selected from among all species of thegenus as a multiple tests problem in statistics (Zander,2007a) has never been evaluated. Because the twospecies of Cyathophorum are embedded deeply in Hy-popterygium, abrupt re-evolution through reactiva-tion of an evolutionarily advantageous suppressed

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trait complex (Zander, 2007d). Although this appearsto be true evolutionary po lyphyly, it may also be a caseof true saltative evolution (Zander, in prep.). See Vrba(1984) for discussion of linked suites of characterswith heterochronic variation.

A molecular evaluation (Harris, 2008) of the mossfamily Mniaceae demonstrated that Plagiomniummaximoviczii is paraphyletic. If the phylogeneticallydisjunct exemplars are interpreted as surviving popu-lations of the same ancestor, then P. maximoviczii(Lindb.) T.J. Kop. has given rise to several species in-cluding P. cordatum T.J. Kop. & D.H. Norris, P. inte-grum (Bosch & Sande Lac.) T.J. Kop., P. novae-zealan-diae (Colenso) T.J. Kop., P. rhynchophorum (Harv.)T.J. Kop., P. rostratum (Schrad.) T.J. Kop., and P. vesi-catum (Besch.) T.J. Kop. Plagiomnium integrum, how-ever, also survives in two ancestral populations phylo-genetically distant on the cladogram, which imply avirtual fossil overlapping that of P. maximoviczii.Again, there is apparent double convergence (be-tween three lineages with the morphology of P. maxi-moviczii and two with the morphology of P. integrum,which is almost certainly less probable an explanationthan, for instance, punctuated equilibrium amongmultiple surviving ancestors, ancestral balancing se-lection or hybridization, or the polyploidy discussedfor other taxa in the Harris (2008) paper. Althougheach of the last two species is attributed morphologi-cal and ecological differences between at least somegeographically disjunct populations, this phenome-non warrants additional attention. Given that P. max-imoviczii is thrice heterophyletic and P. integrumtwice in the Harris (2008) molecular cladogram, therelationship may be an important evolutionary labora-tory for further research.

Even papers with no or little indication of reliabili-ty of molecular phylogenies can offer hypotheses or atleast instruction, though emphasis on statistical pow-er (Zander, 2007a), that can be pursued with moredata and deeper taxonomic coverage. For instance, acombined molecular and morphological study of Po -gonatum by Koshinen & Hyvönen (2004) found ex-emplars of P. pennsylvanicum (W. Bartram ex Hedw.)P. Beauv. polyphyletic. Closer analysis found that theheterophyly was due to the lack of data on one se-quence for one (of three) exemplar of that species. Amolecular-morphological phylogeny of the Poly-trichales by Hyvönen & al. (2004) demonstrated het-erophyly that was discussed by the authors as possiblydue to long-branch attraction. The alternative expla-nation of multiple surviving ancestors postulated inthe present paper suggests that a deep virtual fossil(resolvable at the genus level of) Oligotrichum give

R.H. Zander

rise to complex molecular lineages involving the gen-era Atrichum, Italiella, Meiotrichum, Notoligotrichum,Psilopiloum, and Steereobryon, and also to anothervirtual fossil resolvable as the genus Pogonatum,which itself gave rise to Eopolytrichum and Poly-trichastrum.

This has been an introduction of the use of appar-ent surviving ancestors to infer at least short evolu-tionary series of macroevolution in mosses and posingsome interesting questions that are amenable to fur-ther research given the existence of living representa-tives of inferred ancestors. Other publications existthat include large numbers of exemplars that could al-low evolutionary inferences at the species or genuslevel, but the nomenclature may be already be muchmodified to fit phylogenetic strictures of monophyly(e.g. Huttunen & al., 2004) or the support values maynot be quite high enough for adequate resolution (e.g.Gardiner & al., 2005), requiring additional analysis(e.g. following Zander, 2007a) more appropriate for adifferent paper.

Discussion

That mosses may exhibit evidence of punctuatedevolution (bursts of speciation followed by long sta-sis) is supported by geologic fossil evidence. Althoughmosses have changed little in the past 300 millionyears, the oldest from the Upper Devonian and prin-cipal groups distinguishable before the end of the Pa-leozoic (Lacey, 2008), of 40 Miocene and 79 Plioceneknown European species of mosses (Dickson, 1973),all but four are modern taxa (Frahm, 1994). Recentlyan Andean moss species “indistinguishable from theextant Drepanocladus longifolius” was found in mid-Miocene deposits of continental Antarctica (Lewis &al., 2008). The Madeiran endemic Brachythecium per-currens Hedenäs, on the basis of fossil calibration andabsolute rates of nucleotide exchange, is apparently arelictual Eocene species with static morphology overthe past 40 million years, well before the present habi-tat emerged from the sea (Vanderpoorten & al., 2009).According to Konopka & al. (1998), extant moss fam-ilies, and in some cases extant genera of mosses diver-sified by the Late Cretaceous. It is well known thatcontinental disjunctions of moss species and generaapparently parallel at those taxonomic levels those ofvascular plant genera and families (Herzog, 1926).This “slow evolution” of mosses may be due to strongstabilizing evolution associated with narrow nichesand microhabitats.

Assumed in such standard phylogenetic terminolo-gy as “sister groups” and “shared ancestry” is the ideathat products of evolution signaled by phylogenetic

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splitting must be new taxa, and there are no or veryfew surviving ancestors. Phylogenetically disjunctiveexemplars of the same taxon showing “massive homo-plasy” of phenotypic traits on published molecularcladograms, on the other hand, apparently contra-vene Dollo’s Law (Hall, 2003) that complex traits can-not be expected to re-evolve (short of invoking ortho-genesis). These may be taken, in fact, as probabilisticevidence of deeply buried shared ancestral taxa, al-though such heterophyly is commonly interpreted inphylogenetics as calling for massive rearrangements inclassification. At the genus and species level, phyloge-netic nesting on the basis of molecular trait changesmay be accurate, but any one ancestral species may bephylogenetically complex, e.g., the domestic catspecies (Driscoll & al., 2007), any split in a molecularlineage may involve one or more populations of a sur-viving ancestor, and “evolution” as changes in mostlynon-coding DNA base changes is scarcely as impor-tant to systematics as descent of taxa with modifica-tion of expressed traits. Molecular lineages, however,do provide a window on genetic continuity, except, ofcourse, in the case of hybridization or lateral genetransfer, in which case other data must be used to re-solve incongruities.

A virtual fossil is an inferred taxonomically diag-nosable direct ancestor. It comprises two or morenodes on a molecular tree, and has the same or higherrank than that represented by the two or more extantexemplars. Virtual fossil analysis is independent ofspecies concept, except phylogenetic species con-cepts intolerant of the concept of a single taxon beingpresent in two or more molecular lineages at once.This includes incomplete reciprocal monophylywhere the populations of differentiating species maybe initially paraphyletic but assumes, sometimeswrongly, that eventual extinction of assorted geneticlines must lead to monophyly. It is possible that virtu-al fossils, like geologic fossils, may be dated. Certainlya minimum date would be an estimate of the length oftime that molecularly different populations of isophe-notypic exemplars were isolated, e.g. that of continen-tal drift. Given a molecular clock, even if appro-ximate, other methods could be used to date sharedancestors of heterophyletic exemplars of the sametaxon.

Promoters of the use of molecular phylogenies insystematics commonly invoke the idea of “crypticspecies” for what is here interpreted as shared phenotaxon ancestry involving surviving ancestors(species, genera, etc.). In many cases cryptic speciesdiscovered with molecular analysis such as barcoding(Hebert & Gregory, 2005; Kress & al., 2005; New-


master & al., 2006) may indeed be associated laterwith diagnosable morphological or life history traits(Hebert & al., 2004; Hillis & al., 1996: 519). Onemust be wary, however, of multiple-test problems, inthat there may be two alternative morphological setsof traits associated with phylogenetic recognition ofnearly any two different almost fully cryptic groupsbut molecular support is not support for one of themsimply because morphology and DNA by chanceagree (Zander, 2007a, c). In many cases, on the otherhand, the species remain fully cryptic, that is, phy -logenetically disjunctive isophenes (e.g. Elmer & al., 2007).

Presently, the emphasis in phylogenetics is on usingparsimony or coalescent theory Bayesian analysis ondata sets of randomly mutating DNA sequence traitsthat theoretically track lineages of phenotypic or atleast biological speciation. Although such molecularlineages apparently are statistically demonstrable,when conflicts occur with the results of morphologi-cal analyses or when resolution is needed in morpho-logical analyses, the relationship between a molecularsplit and a speciation event is commonly based solelyon the biological species concept requiring speciationafter an event of isolation (e.g., as criticized by Riese-berg & Burke, 2001). This does not apply to many ifnot most groups of organisms. Systematics is gradual-ly becoming based primarily on this molecular foun-dation, isolating itself from fields, such as populationbiology, ecology, evolution, and biogeography, that in-vestigate or use theories of evolution based largely onexpressed traits. Theories in science, particularly qua-si-experimental (Cook & Campbell, 1979) or histori-cal fields whose assumptions and results are not di-rectly verifiable, are often easily generated and if in-ternally consistent may be sustained by pure reason inthe absence of empiric data (Hey, 2001). This is par-ticularly true in systematics where the theoretic scaf-folding for progression of evolutionary change inspecies is poorly resolved or understood because of alack of facts, beyond that of evolution itself, and thusfact-based theory. Pieces of the puzzle are easily filledin by appeal to simplicity, a fancied similarity to thePrinciple of Least Action in physics. The latter, how-ever, is quite solidly based in observation, while parsi-mony of tree length, or probabilities of branch coales-cence, are at a remove from corroborative observa-tions of details of descent with modification of taxa asto their expressed or unexpressed traits.

According to Arendt & Resnick (2007), becausegenomic analysis has demonstrated that the samegenes may be involved in the same phenotypic adap-tation in phylogenetically distant groups of animals,

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while different genes are apparently the source of thesame phenotypic adaptation in related groups, theusual distinction between parallelism and conver-gence (parallelism expected to be based on the samegenomic pathways, and convergence on different)breaks down. The authors recommend that “conver-gence” should be the general term. As this applies tothe present paper, evolution of the phenotype may bequite disconnected from evolution of the genotypethough remaining based on it. Although homologousfeatures are derived from common ancestors, non-homologous features may also, and, if these are part ofthe same lineage, they are not convergent (or parallel)but simply are substitutions of one gene system for an-other in support of the same evolutionary feature asno more than a kind of anagenesis along one line ofevolution, this tracked by the molecular data. Conver-gence is indeed the general term but the phenomenonis informative, not confounding.

Watson (1913) presented a long list of morpholog-ical features of mosses that he inferred to be adapta-tions to periodic drying of habitats. Patterson (1964),however, in a review of experimental studies, con-cluded that physiological responses were far moreimportant than morphological traits in determiningresistance to desiccation, suggesting that Watson’slist of traits lacked any basis in fact. Anderson (1974),on the other hand, in a review of experimental physi-ology, suggested that the morphology of mosses isprobably of some importance in determining theirability to live in dry habitats. Certainly many Pot -tiaceae with apparent elaborate adaptations to harsh environments (leaves with hair points, papillae,and inflated basal cells, reduced capsules with lar-ge spores) grow side-by-side with Bryaceae and Di -trichaceae, these with little apparent morphologi-cal adaptation. With the present technique detail-ing macroevolution, however, correlations of traitchanges and habitat may prove illustrative of selec-tion on the basis of morphology rather than phy-siology.

Tests of the virtual fossil method need to be devel-oped. Of course the most obvious tests are whetherthe method (a) fits the facts, which it does as dis-cussed above, and (b) whether it melds well with evo-lutionary theory. Although evolution is a fact, theoryon the mechanisms of evolution is still in vigorousflux (Gould, 1983), and it is here hoped that the in-ferred relationships of virtual fossils on moleculartrees might illuminate aspects of such theory giventhat surviving ancestors are available for study. A sec-ond test might involve co-evolution of organisms andtheir parasites, pollinators, or predators; the latter

R.H. Zander

might be expected to similarly diverge in moleculartraits but retain phenological characteristics.

It is here hoped that the difficult task of retrodict-ing phenotypic evolution of taxa diagnosed by ex-pressed traits is not abandoned in adhering to the pastparadigm change of substituting molecular phyloge-nies for taxon trees in systematics. Declaring a diffi-cult problem solved by simply changing the matterunder scientific investigation because a differentproblem is more tractable is not helpful and is evendoubtfully a paradigm change since different subjectsare addressed.

It is only an importunate homage on the part ofphylogeneticists to their sister-group analytic methodthat requires enforcement of strict phylogeneticmonophyly (holophyly) in modern classifications,splitting, excising, or reducing in rank taxa thatshould have unique evolutionary traits flagged at anappropriate level in classification. Because ancestor-descendant relationships and lineages probably af-fected by punctuated equilibria are not recognized inphylogenetic classification, a major source of evolu-tionary information is gradually being deleted fromthe classifications that inform biodiversity and evolu-tionary study. This isolates systematics, whichpresently cannot or will not provide a general-pur-pose classification.

Hull (1979) has pointed out that genealogy and di-vergence cannot both be represented in a classifica-tion and be separately retrievable. Although this istrue, the existence of ancillary cladograms and taxontrees allows distinction of which taxa are flagged byhigher taxonomic level because they are sister groupsto major lineages or because they are significantlyunique autophyletic descendants. A classification including both types are information would be ofgreater value to ecologists, morphologists, evolution-ists, students of evol-devo, teachers, government, andso on, certainly of greater pragmatic value than a spe-cial-purpose classification of interest largely only tophylogeneticists.

Acknowledgements

I thank R.K. Brummitt, R. Mesibov, and others for commentson various drafts of this paper. The abiding encouragement of P.M. Eckel is much appreciated. Thanks are due the MissouriBotanical Garden for on-going support of this research.

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Associate Editor: J. GuerraReceived: 25-II-2009Accepted: 28-V-2009

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