IAWA Journal, Vol. 17 (4), 1996: 351-364

PARALLELISM AND REVERSIBILITY IN XYLEM EVOLUTION A REVIEW

by

Pieter Baas 1 & Elisabeth A. Wheeler2

SUMMARY

The irreversibility of the major trends of xylem evolution, such as the origin of vessels in primitive angiosperms with long fusiform initials, and the shifts from scalariform to simple perforations and from tracheids to libriform fibres, has long been accepted by wood anatomists. Parallel development of these and other xylem features is generally accepted, and is suggested by the distribution patterns of the fibre and perforation plate type. Some recent phylogenetic analyses of seed plants suggest that there also have been some reversals in these general trends. The likelihood and extent of parallel origins and reversions of the major trends in xylem specialization are explored here by analysing a number of published hypotheses on the phylogenetic relationships within wood anatomically diverse major clades of angiosperms, and within some individual fami­lies. On the basis of these analyses, it appears that for these major Baileyan transformation series, parallelisms were more than twice as common as reversals. Functional adaptations to increased efficiency and safety of hydraulic architecture can largely explain the high incidence of paral­lelisms in xylem evolution.

Key words: Xylem evolution, parallelism, reversibility.

INTRODUCTION

There seems little doubt about the general validity of the major trends in xylem evolu­tion, outlined over seventy five years ago in Bailey and Tupper's classical paper (1918), and elaborated on by Frost (1930a, b, 1931). A survey of the fossil record (Wheeler & Baas 1991, 1993) supports these general trends because features considered 'primi­tive' in the Baileyan sense are more common in woods from the distant geological past than in Recent woods. Increased understanding of hydraulic adaptations in wood struc­ture to various ecological conditions (Zimmermann & Brown 1971; Zimmermann 1983; Carlquist 1975, 1977, 1988, 1995; Baas 1986) provides rationalefor why xylem evolu­tion has proceeded in the general direction of increased efficiency and increased safety of water transport.

1) Rijksherbarium/Hortus Botanicus, P. O. Box 9514, 2300 RA Leiden, The Netherlands. 2) Department of Wood & Paper Science, North Carolina State University, Raleigh, N.C. 27695-

8005. U.S.A.

352 IAWA Journal, Vol. 17 (4), 1996

In the past, students of plant phylogeny used the Baileyan trends to help unravel patterns of relationships, especially in groups where floral features gave conflicting results (for reviews see Bailey 1944; Metcalfe & Chalk 1950; Stern 1978, Carlquist 1988; Dickison 1975, 1989). The recognition of the 'woody Ranales' (the Magnoliales and related orders) as basal in the dicotyledons gained support from wood anatomy because many primitive wood attributes (e. g., vessellessness, scalariform perforations) are concentrated in these orders. The conviction that the major trends were irreversible made wood anatomical verdicts on the phylogenetic status of a certain plant group highly respected. In these pre-cladistic studies the presence of specialized features, such as simple perforations and libriform fibres (with simple pits), in a taxon excluded the possibility of that taxon being ancestral to a group with scalariform perforations and fibres with distinctly bordered pits (Bailey 1944; Stern 1978).

More recently, the irreversibility of the major trends of xylem evolution has been questioned by phylogenetic systematics (or cladistics). In 1981, Young presented a cladogram, based on a data set of characters from various plant parts, of the so-called primitive angiosperms in which vessellessness turned out not to be the primitive, but rather the derived state. This conclusion was based on the simple reason that it would take more steps (or character changes) in the cladogram, if it were assumed that the earliest angiosperms were vesselless rather than assuming the earliest angiosperms had vessels and vessels were subsequently lost. Later, Donoghue and Doyle (1989) and Loconte and Stevenson (1991) reached the same conclusion for the same reason, i. e. that in Recent angiosperms it is more parsimonious to consider vessellessness a derived feature. Suzuki (1993) discussed the problem of homology and analogy of vessels in angiosperms in the light of these recent suggestions. The shift from vesselless to vessel-bearing woods is but one element of the Baileyan model. There are also the changes from vessel elements with scalariform perforation plates (initially strongly resembling scalariform bordered pits with the pit membranes dissolved) via mixed simple and scalariform plates (with few, widely spaced bars) to simple perforations; and from imperforate tracheary elements with conspicuously bordered pits (tracheids, fibre-tracheids) to fibres with strongly reduced pit borders or even simple pits (libriform fibres).

Cladistics has made many comparative biologists think more explicitly about evo­lutionary character state changes, irrespective of which particular suite of attributes is being used for systematic purposes. Cladistics aims to reconstruct phylogenies on the basis of shared, uniquely derived character states (as opposed to overall similarity), and by applying the principle of parsimony, i.e., that an evolutionary pathway involv­ing a minimum number of character changes is more likely than one involving more steps. The polarisation of characters (i. e., the determination of which state is primitive or plesiomorphic and which one derived or apomorphic) is determined by the condi­tion in an outgroup, preferably the closest of kin to the group (composed of two or more sistergroups) under analysis. When applying these methods to some wood ana­tomical character sets (Baas & Zweypfenning 1979; Baas et al. 1988) it was striking that blindly applying cladistic rules would almost always yield results contrary to the Baileyan model. There are many plant groups in which a small group of genera or

Baas & Wheeler - Parallelism and reversibility in xylem evolution 353

species show primitive features (e.g. scalariform perforations in the Myrtaceae, cf. Schmid & Baas 1984; fibre-tracheids in Combretaceae and Melastomataceae or in Myrtales in general, cf. Van Vliet & Baas 1984), and where the application of an outgroup rule would almost always identify those genera with primitive wood anatomical fea­tures as derived (apomorphic) instead of primitive (plesiomorphic). This begs the ques­tions of a) whether there is something wrong with the Baileyan model; b) whether the parsimony principle applied by the cladistic method is fundamentally erroneous, i. e. incongruent with evolutionary processes in nature; or c) whether parsimony just does not apply to xylem evolution. In other words, the phenomena of parallel or convergent evolution and of reversibility in character changes (jointly called homoplasy in cladistic terminology) could be so common in xylem evolution that the potential for using wood anatomical diversity in phylogenetic reconstruction is seriously reduced. The question addressed in this paper will be how parsimonious has xylem evolution been? Only three character changes will be considered: 1) vessellessness to vessel-bearing; 2) scalari­form to simple perforations; and 3) tracheids to libriform fibres.

The following sources of evidence will be considered: 1) the distribution patterns of certain wood anatomical characters in extant woody dicotyledonous families, 2) some recently published cladograms (hypothetical phylogenies) based on either a large number of morphological characters or on chloroplast DNA sequences, 3) a limited number of cladistic analysis of wood anatomical data sets, 4) ecological and functional wood anatomy, 5) the fossil record. From the results of this review, we will give preliminary conclusions that we hope will serve as a basis for further discussions and research on wood evolution.

Distribution patterns of wood anatomical characters in extant woody dicotyledonous families

Parallelism in xylem evolution - Table 1 lists vascular plant groups with vessel­bearing xylem. With the exception of the Gnetales, vessel elements with scalariform perforations occur within these groups. Although their morphology would thus sug­gest homology, their occurrence in such phylogenetic ally distant clades clearly does not. It is highly unlikely that the presence of vessels in all these groups is due to a single origin of vessels, and the conclusion must be that vessels have arisen more than once.

Table 1. List of plant groups with vessel-bearing xylem.

Ferns (3 times?)

Equisetum Selaginella

Gnetales Monocotyledons

Dicotyledons

354 IAWA Journal, Vol. 17 (4),1996

Table 2. List of dicotyledonous families with both simple and scalariform vessel perfora­tions in different species. Data from Metcalfe & Chalk (1950) and Metcalfe (1987).

Alangiaceae Euphorbiaceae Myricaceae Araliaceae Fagaceae M yristicaceae Caprifoliaceae Flacourtiaceae Myrsinacaeae Casuarinaceae Grossulariaceae Myrtaceae Celastraceae Guttiferae Olacaceae Cornaceae H ydrangeaceae Piperaceae Corylaceae Icacinaceae Ranunculaceae Cunoniaceae Juglandaceae Rhizophoraceae Dichapetalaceae Lauraceae Rosaceae Dilleniaceae Linaceae Sabiaceae Epacridaceae Magnoliaceae Vacciniaceae Ericaceae Marcgraviaceae Violaceae Eucryphiaceae Monimiaceae

Table 2 lists dicotyledonous families in which some representatives have scalari­form perforations, and others have simple perforations. Assuming that at least some of these families represent monophyletic groups, the conclusion that the transition from scalariform to simple perforations must have occurred numerous times is self-evident. Carlquist (1996) has also emphasized that this transition has commonly occurred.

Families in which some members have fibre-tracheids, and others have libriform fibres are listed in Table 3. Interestingly, only slightly more than a third of the families listed in Table 3 are also heterogeneous for type of perforation plate. Again, the con­clusion must be that the transition from imperforate tracheary elements with distinct­ly bordered pits to libriform fibres must have occurred many times in xylem evolu­tion.

In conclusion, we can repeat what Bailey and his contemporaries, and later wood anatomists such as Chalk, were aware of: parallelism has been extremely common in xylem evolution, and in this respect evolution is unparsimonious.

Reversibility - The problem of how common reversions are in xylem evolution is much more difficult to answer. The family lists of Tables 2 and 3 can also be inter­preted as examples where the secondary xylem has reversed from the specialized to the primitive condition (i.e., from simple to scalariform perforations or from libriform fibres to tracheids). This would still mean that there are many instances of parallel development, but in a direction opposite from the Baileyan trends, and also suggesting that parsimony does not apply when considering changes in wood structure. There­fore, merging of wood anatomical data with more inclusive morphological datasets, or mapping of wood character changes on cladograms from other sources, likely is a more appropriate way to determine polarity.

Baas & Wheeler - Parallelism and reversibility in xylem evolution 355

Table 3. List of families with both fibre-tracheids and libriform fibres. Data from Metcalfe & Chalk (1950), and Metcalfe (1987), * = also heterogeneous for perforation plate type.

Annonaceae Guttiferae* Oleaceae Apocynaceae Hydrangeaceae* Opiliaceae Asclepiadaceae Icacinaceae* Passifloraraceae Boraginaceae Lardizabalaceae Phytolaccaceae Calycanthaceae Lauraceae* Proteaceae Caprifoliaceae Lecythidaceae Rhizophoraceae* Caryophy llaceae Linaceae* Rosaceae* Celastraceae* Loganiaceae Rubiaceae Chloranthaceae Loranthaceae Sabiaceae* Combretaceae Malvaceae Santalaceae Cunoniaceae* Melastomataceae s.l. Sapotaceae Dipterocarpaceae Monimiaceae* Scrophulariaceae Ericaceae* Myrtaceae* Simaroubaceae Euphorbiaceae* Ochnaceae Solanaceae Fagaceae* Olacaceae* Violaceae* Flacourtiaceae*

Some recently published cladograms The approach used for analysing the likelihood of reversibility has been to map ves­

sel element and fibre type on a number of recently published cladograms, and then to trace character changes, and to compare the 'cost' or non-parsimony of reversibility and irreversibility. This approach is demonstrated by Figures 1 & 2, which show the method applied to a cladogram by Dahlgren and Bremer (1985, their fig. 2), represent­ing one of 100 equally parsimonious trees, and based on 61 characters, polarized by assuming the primitive angiosperm was a woody plant with strobiloid flowers. Perfo­ration plate type was the only wood character they used for the analysis shown.

In this cladogram of 49 families belonging to the Magnoliiflorae, Nymphaeiflorae and Ranunculiflorae by Dahlgren and Bremer (1985), it appears that vessellessness arises five times independently (including once in the Nymphaeales) (thus showing 5 reversions), and that the change from scalariform to simple perforations has 12 paral­lel developments and no reversions (Fig. 1). The alternative for reversibility of the tracheid-vessel element transition can be calculated by drawing vessellessness back to the root of the cladogram and concluding that vessels have arisen ten times inde­pendently in the core group of angiosperms (Fig. 2). Ten parallel origins instead of five reversals is a difference of five unparsimonious extra steps, provided that the cladogram is a reasonable reflection of the true phylogeny of this group of families, which almost certainly it is not. Each cladistic re-analysis, using slightly different character sets pro­duces rather different cladograms; in other words, none of the cladograms of the higher categories is very robust. The distribution of libriform fibres as mapped onto the same Dahlgren and Bremer cladogram can be interpreted as indicating that this feature has arisen independently ten times, with perhaps one reversion in the Centrospermae.

356

- vesselless

scalariform

simple

1

IAWA Journal, Vol. 17 (4),1996

I {

- Phytol.

- Caryoph.

I - L - Chenop.

I -i L - - - - - - Polygon.

I -I L - - - - - - - - Paeon.

1 L - - - - - - - - - - Sterc. ~

1 I { - Hydnor.

L--------1 - Raffl.

L { - Fumar.

- Papay.

L _______ ~I--- Dillen.

'----- Hamam . .... ---___________ Tetrac.

I - Ranunc.

I - 1 - - Berber.

--------------i

L

L - Menisp.

{ - Lardiz.

- Sargent.

.... -------------- Trochod. 1 - - - - • NYMPHAEALES etc. - -

L----------------------Cmd - Piper.

Saurur.

- Lactor.

- - - - - - Aristol.

I - - - Laur. L ______________________ _

L - - - Monim. L ____________________ ~---- Eupom.

- Annon.

- Calycan.

Gomort. '----- Trimen .

... ----- Ambor. Schizo

IIIic. 1...--- Euptel.

'-------- Austrob. t ----------Himant.

.---------- Winter. - Myrist.

Chlor.

'----- Degen.

- - - - - - Magno!.

Fig. 1. Mapping of vessel features onto the Dahlgren & Bremer (1985) cladogram. Vessel elements with scalariform plates placed at the base, and allowing reversal from vessel-bearing to vessellessness. This scheme shows four parallel origins of vesselless woods, 12 parallel origins of vessel elements with simple perforations, and no reversals in these features.

Baas & Wheeler - Parallelism and reversibility in xylem evolution

- vesselless

scalariform

simple

1

1

10

r

r { - Phyto!.

- Caryoph. r

r - L - Chenop.

r --i L - - - - - - Polygon.

r -I L - - - - - - - - Paeon. L __________ Sterc.

-!

1 r { L---------i

L {

- Hydnor.

- Raffl.

- Fumar.

- Papay.

L-------~I--- Dillen. '----- Hamam .

.. ______________ Tetrac.

r - Ranunc.

r - 1 - - Berber.

L

L - Menisp.

{ - Lardiz.

- Sargent.

.. -------------- Trochod. - - - - - NYMPHAEALES etc. - -

L - - - - - - - - - - - - - - - - - - - - - - Cane!.

- Piper.

Saurur.

- Lactor.

- - - - - - Aristo!'

L _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ ~ - Laur.

L - - - Monim. L-____________________ ~---Eupom.

2

- Annon.

- Calycan.

Gomort. '----- Trimen .

... ----- Ambor. Schizo

Illic. '----- Eupte!.

'-------- Austrob. - - - - - - - - - - Himant.

... -------- Winter. - Myrist.

Chlor. '----- Degen.

- - - - - - Magno!.

357

Fig. 2. Mapping of vessel features onto the Dahlgren & Bremer (1985) cladogram. Vessellessness is basal. This scheme shows 10 parallel origins of vessels, as numbered on the cladogram.

358 IAWA Journal, Vol. 17 (4),1996

Another set of cladograms, based on 104 morphological, anatomical and chemical features, including wood anatomical ones, was published by Loconte and Stevenson (1991). These authors analysed the consistency indices of the characters they used. The consistency index is a measure of the congruence of the character state changes and the topography of the cladogram: the highest value is 1.0 (i.e., no parallelisms), and they found 20 of their 104 characters to have this high value. For the changes from tracheids in vesselless woods, via scalariformly perforated vessel elements to simply perforated ones they found a consistency index as low as 0.21 (which was somewhat lower than most floral characters). Other consistency indices from their analysis: cambial initial length: 0.2; vessel distribution (in roots-sterns-leaves): 0.5; primary xylem pit­ting: 0.5; presence or absence of oil cells: 0.25; nodal anatomy: 0.23; phyllotaxy: 0.20; leaf type (compound-simple): 0.33; pubescence: 0.11; stomatal type: 0.36; exine struc­ture: 0.67. In other words the 'xylem conduction element' character seemed of very limited value only, and the authors concluded that "If this character is coded as irre­versible, the interpretation is 17 steps (!) longer, because Amborellaceae and Winteraceae are nested at least 5 branches within the angiosperms, and the Tetracentraceae and Trochodendraceae are nested approximately ten branches."

The cladogram of Hufford (1992) analysing the Rosidae and their relationships to other nonmagnoliid dicotyledons tells a different story. Hufford used 60 different char­acters, including 10 wood anatomical ones, such as very detailed character states for vessel perforations and fibre tracheid pitting. His strict consensus tree (calculated from 56 equally parsimonious trees with 682 character state changes) has the root of the angiosperms vesselless, and only one vessel origin. Moreover, the vessel-bearing basal clades all have scalariform perforations. However, for the change from scalariform to simple plates several parallel developments and some reversions have to be assumed. If irreversibility is assumed, there are five more parallel developments of simple perfo­rations than if reversibility is allowed. The occurrence of scalariform perforations in the highly derived Caprifoliaceae (Viburnum in particular) is especially hard to imag­ine as a relictual character, because that alone would require four extra parallel devel­opments of simple perforations. The origin of libriform fibres can easily be pictured as a series of about 20 parallel events, with at least one reversal at the base of the Dil­leniaceae/Theaceae and higher up in the cladogram.

A much cited cladogram for seed plants is the one by Chase et al. (1993) which is based on nucleotide sequences from the plastid gene rbcLl of almost 500 species. The authors very clearly state that theirs is only a preliminary proposal for an alternative seed plant taxonomy, rather than the only possible basis for the analysis of character evolution in seed plants. We overlaid the cladogram with wood anatomical features as was done for Figures 1 & 2. According to the distribution of wood characters as mapped onto this cladogram several origins of vessels and reversions to vessellessness, many parallel developments of simply perforated vessel elements and libriform fibres, and a more limited but still appreciable number of reversions from simple to scalariform perforations and from libriform fibres to fibre-tracheids can be hypothesized (again on the premise that the changes in wood anatomical character states and others have fol­lowed the most parsimonious model; cf. discussion of Figures I & 2). On the whole,

Baas & Wheeler - Parallelism and reversibility in xylem evolution 359

Table 4. Incidence of parallelisms and reversals in perforation plate (scalariform - simple) and imperforate element (with distinctly bordered to indistinctly bordered) transformation series. Summarized from mapping character state changes onto the cladograms of Chase etal. (1993), Dahlgren & Bremer (1985), Hufford (1992), and Loconte & Stevenson (1991).

Perforation Plate Parallelisms Reversals

Chase et al. 27 12 Dahlgren & Bremer 12 0 Hufford 7 9

Loconte & Stevenson 12

Sum 58 23

Fibre Type Parallelisms Reversals

Chase et al. 5 2 Dahlgren & Bremer 11 1 Hufford 17 1 Loconte & Stevenson 2 3

Sum 35 7

there is considerable agreement between the relationships suggested by this phylogenetic analysis of nucleotide patterns of a single gene and multicharacter-based traditional classifications of the angiosperms (e.g. Cronquist 1981; Thome 1992). This agree­ment suggests that it is appropriate to use molecular 'phylogenies' as a basis for inves­tigating wood anatomical character transformation.

As a conclusion to this discussion of some large cladistic analyses of higher groups, we can say that the case for irreversibility is certainly not supported. Only the origin of vessels is a unique irreversible event in the (partial) cladistic analysis of Hufford (and likely caused in part because of the inclusion of 10 wood anatomical characters that were pre-polarized in agreement with the Baileyan trends). However, in the cladograms, parallel development is a much more common feature than reversibility, as summa­rized in Table 4. See also Herendeen et al. (in press).

Cladistic analyses of wood anatomical data sets Another sourCe of evidence is the cladistic analysis of exclusively wood anatomical

data sets in the woody families: Oleaceae and Rosaceae. In the Oleaceae (Baas et al. 1988) there is a striking diversity in imperforate tracheary elements, from 'true tracheids' sensu Carlquist (or fibre-tracheids Sensu Baas) to libriform fibres. The character is highly correlated with other features such as vessel grouping and distribution, and also with parenchyma distribution. In various cladistic analyses (depending on whether the wood anatomical character states are run as unordered or polarized according to the Baileyan model), the Oleaceae with fibre-tracheids form either a monophyletic de­rived group (implying a reversal) or a plesiomorphic paraphyletic tail (grade) in the

360 IAWA Journal, Vol. 17 (4), 1996

cladogram (the latter conforms to the Baileyan model). The latter cladogram receives strong support from chromosome numbers: Oleaceae with libriform fibres have an allopolyploid chromosome complement; those with fibre-tracheids have various di­ploid numbers. Because it is unlikely that the latter arose from polyploids, the Baileyan model is vindicated, and the change from fibre tracheids to libriform fibres is con­firmed as a unique specialization event in the evolution of the Oleaceae. The wood anatomical cladogram is independently supported by a recent cladistic analysis of chloro­plast DNA data (Kim & Jansen 1993; Kim, personal communication).

The Rosaceae have recently been studied wood anatomically by Zhang (1992); in his cladistic analysis based on wood characters, the groups with fibre tracheids are basal, and libriform fibres arise only once. Other wood anatomical characters exhibit consid­erable parallelism and reversions. The distribution of fibre pitting in the Rosaceae is as expected according to the Baileyan model, but, as Zhang acknowledged, this is partly the result of a priori polarisation of the wood characters according to the Baileyan model. Nevertheless, fibre type appears to be a useful character for phylogenetic analysis within the family, and in at least one case is supported by karyological evidence (Zhang 1992).

Functional and ecological wood anatomy In the last decades we have become aware of some general ecological patterns in

the incidence (frequency) offeatures such as scalariform perforations and fibre-tracheids. For instance, in Europe, woody floras from cool alpine or arctic regions are character­ized by a very high incidence of scalariform perforations and fibre tracheids (Baas & Schweingruber 1987). There is an increase in the incidence of scalariform perforations in the transition from tropical lowland to tropical alpine or temperate conditions (Baas 1975, 1976). A very plausible explanation has been that scalariform perforations add to the resistance to flow, and that their elimination in all environments with a seasonal or permanent demand for great hydraulic efficiency (i. e., in dry and/ or warm climates) has been accelerated. The high incidence of scalariform plates in cool regions (or for that matter in the ever-humid undergrowth of the tropical rain forest) is then simply a relic of the primitive condition, and no threat to the irreversibility assumption in the Baileyan model. However, Zimmermann (1978) suggested that scalariform perfora­tions might trap gas bubbles arising in thawing xylem sap from cold temperate to arctic trees. This suggestion would apply to over 50% of woody plants growing under cool temperate to arctic or alpine conditions, and the other 50% might trap their embolisms in vessel element tails associated with their very steeply oriented, oblique simple per­foration plates. If this function of scalariform perforations is crucial to the survival and evolutionary success of plants in cool regions, we could, based on intuition, suggest an adaptation driven mechanism for the reversion of simply perforated to scalariformly perforated vessel elements. By analogy one could also cite beneficial properties to fibre­tracheids in these regions, which could secure minimal sap transport in case all vessels had become emboli zed despite their embolism traps in the form of scalariform plates. This is admittedly extremely speculative, but hydraulic functions have been ascribed to fibre-tracheids by Braun (1970) with some experimental evidence, and by Carlquist (1988).

Baas & Wheeler - Parallelism and reversibility in xylem evolution 361

Woody angiosperms have existed for more than 100 million years. During that time there have been many changes in climate and topography, and changes in leaf structure and phenology (cf. Upchurch & Wolfe 1987; Wolfe 1978), which in tum suggest changes in hormone levels and distributions that would affect xylem differentiation (Aloni 1988). Within some families and genera, vessel element length is correlated with environ­ment and assumed to be affected by it. Within genera, species from the tropical low­lands have longer vessel elements than do species from higher latitudes (e.g., Baas 1976). Within a tree, vessel elements and fibres are longer and narrower in the latewood than in the earlywood, and wider towards the base of the tree and in the roots (Pan­shin & DeZeeuw 1980). It is relatively easy to develop scenarios in which tracheary element size could be either increased or decreased over geologic time as affected by changes in the length of growing season, water availability, temperature, and/ or auxin levels.

Whether or not a cell develops a perforation may be affected by its diameter. In some families (e. g., Betulaceae, Ulmaceae, Leguminosae), there are vascular tracheids - narrow cells without perforations which have wall markings identical to the vessel elements and are of about the same length as vessel elements. The occurrence of vas­cular tracheids, sometimes termed degenerate vessel elements, demonstrates that per­forations can be 'lost' and that this loss correlates with a narrowing of the vessel ele­ment. Vascular tracheids, when present, typically occur in the latewood of temperate woods. Changes from earlywood formation to late wood formation are correlated with changes in auxin level, and there is more cell elongation and diameter increase than there is in the earlywood. Sarcandra is reported to have vessels in the roots (Carlquist 1987), where elements typically are wider, and not in the stem.

Bailey did not consider the occurrence of vascular tracheids to provide a sound basis for concluding that the evolution of vessels from tracheids was reversible be­cause "the end products of these trends of specialization differ markedly from typical tracheids." Those who have suggested that vesselless dicotyledonous are secondarily vesselless did not suggest that vesselless woods were derived from woods that repre­sent "end products of these trends of specialization," that is, from woods with simply perforated vessel elements and fibres with simple pits. Whether or not vesselless angio­sperms represent vessel loss that occurred while distinctions between vessels and tracheids were minimal is an unresolved, perhaps unresolvable, issue. As pointed out by Carlquist (1996), loss of perforations at such a stage would barely constitute a character state reversion, and certainly not constitute a reversal of a general trend in wood evolution. There is a need for more data from the fossil record, specifically to determine whether vesselless angiosperm woods are among the oldest angiosperm woods, but also for more data on xylem differentiation to better understand the con­ditions that affect vessel development.

The fossil record The fossil record for dicotyledonous wood features has been reviewed in two ear­

lier papers (Wheeler & Baas 1991, 1993). Despite the strong support of the fossil rec­ord for the Baileyan model the fossil record does not really provide us with any strong

362 IAWA Journal, Vol. 17 (4),1996

evidence for reversibility or irreversibility. If we picture xylem evolution as a dynamic equilibrium with a large arrow going in the direction of the Baileyan trends, and a small one going in reverse, the fossil record is highly unlikely to provide documenta­tion for reversals. Unquestionable vesselless angiosperms are reported from the upper Cretaceous, not earlier (Suzuki 1993), while vessel-bearing angiosperms are reported from the early mid-Cretaceous. However, most of the known Cretaceous angiosperm woods are upper Cretaceous, and there are very few « 1 0) Aptian-Albian woods known. Thus, it would be inappropriate to use the absence of vesselless woods from the early mid-Cretaceous as evidence in support of reversibility from vessel-bearing to vessel­lessness. The fossil record does not shed light on the transition from scalariform to simple perforations, or vice versa, as among the earliest angiosperms is a wood type (Paraphyllanthoxylon) with exclusively simple perforations and fibres with simple pits, and a wood type (Icacinoxylon) with exclusively scalariform perforation plates and fibres with distinctly bordered pits.

CONCLUSION

Two opposing interpretations of the open-ended discussion above are:

1) In view of the well established and functionally plausible common occurrence of parallelism in wood evolution, in phylogenetic analysis one might prefer to accept extra parallelisms in the origins of vessels, simple perforations or libriform fibres, rather than accepting counter-intuitive reversals suggested by cladistic analyses.

2) The dogma of irreversibility should be abandoned because none of the supporting arguments, such as strongly correlated changes in wood anatomical character syn­dromes or the functionality and adaptive advantage of the major Baileyan trends has ever been proven objectively. Even if xylem evolution has been unparsimonious, it is preferable to chose the most parsimonious from two alternative interpretations.

It is likely that the evolutionary truth is somewhere in between these two extremes. The likelihood of reversibility or irreversibility in xylem evolution can be best as­sessed if we understand more of the genetic and morphogenetic background of such features as vessel perforations and fibre pitting. That these features are under strong genetic and morphogenetic control is evident from the distribution pattern of these features over systematic groups, and their variation with plant development or posi­tion within the plant. However, many questions remain as to what sorts of genomic changes are involved in the evolutionary changes of wood anatomical character states. Much future research along these lines of inquiry, and future re-analysis of different, and, hopefully, more complete, datasets, is required to achieve a satisfactory under­standing of the intricacies of xylem evolution.

ACKNOWLEDGMENTS

We thank Christine Kampny for helpful comments and suggestions on a draft of this manuscript.

Baas & Wheeler - Parallelism and reversibility in xylem evolution 363

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