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(American Journal of Botany. 1999;86:1290-1300.)
© 1999 Botanical Society of America, Inc.

Phylogenetic analyses of Andromedeae (Ericaceae subfam. Vaccinioideae)1

Kathleen A. Kron 3 2, Walter S. Judd 4 and Darren M. Crayn 5

3Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27109-7325; 4Department of Botany, University of Florida, Gainesville, Florida 32611-8526; and 5School of Biological Science, University of New South Wales, Sydney 2052, Australia

Received for publication July 6, 1998. Accepted for publication February 23, 1999.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Phylogenetic relationships within the Andromedeae and closely related taxa were investigated by means of cladistic analyses based on phenotypic (morphology, anatomy, chromosome number, and secondary chemistry) and molecular (rbcL and matK nucleotide sequences) characters. An analysis based on combined molecular and phenotypic characters indicates that the tribe is composed of two major clades—the Gaultheria group (incl. Andromeda, Chamaedaphne, Diplycosia, Gaultheria, Leucothoë, Pernettya, Tepuia, and Zenobia) and the Lyonia group (incl. Agarista, Craibiodendron, Lyonia, and Pieris). Andromedeae are shown to be paraphyletic in all analyses because the Vaccinieae link with some or all of the genera of the Gaultheria group. Oxydendrum is sister to the clade containing the Vaccinieae, Gaultheria group, and Lyonia group. The monophyly of Agarista, Lyonia, Pieris, and Gaultheria (incl. Pernettya) is supported, while that of Leucothoë is problematic. The close relationship of Andromeda and Zenobia is novel and was strongly supported in the molecular (but not morphological) analyses. Diplycosia, Tepuia, Gaultheria, and Pernettya form a well-supported clade, which can be diagnosed by the presence of fleshy calyx lobes and methyl salicylate. Recognition of Andromedeae is not reflective of our understanding of geneological relationships and should be abandoned; the Lyonia group is formally recognized at the tribal level.

Key Words: Andromedeae • Ericaceae • Lyonieae • matK • molecular systematics • rbcL.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Andromedeae (13 genera, subfam. Vaccinioideae; see Stevens 1971 , 1995) are a heterogeneous group of doubtful monophyly (Judd and Kron, 1993 ; Kron and Chase, 1993 ; Stevens, 1995 ; Kron, 1996 , 1997, and unpublished data; Kron and Judd, 1997 ; Kron et al., 1998 ). Members of this "group" are characterized by alternate leaves with well-developed blades, usually axillary inflorescences, sympetalous, urceolate flowers with often appendaged anthers, superior ovaries with numerous ovules, and usually loculicidal capsules. The members of this tribe are distinguished from the phenetically similar Vaccinieae by their superior (vs. inferior) ovaries and usually dry, capsular (vs. fleshy, baccate) fruits (Stevens, 1969 , 1971, 1995; Anderberg, 1993 ; Judd and Kron, 1993 ). They are easily distinguished from members of the Arbuteae, which also have urceolate corollas and superior ovaries, by their well-developed, lignified, fiber sheath surrounding the midrib in the leaves (vs. such fibers poorly developed or lacking), anthers that become inverted early in development (vs. inverting only very late), and with numerous (vs. few or only one) ovules per locule, dry fruits (vs. fleshy fruits with a prominent layer of fibers around inside of pericarp), and the lack (vs. presence) of high concentrations of ellagic acid (Matthews and Knox, 1926 ; Stevens, 1969 , 1971; Anderberg, 1993 ; Judd and Kron, 1993 ).

Most genera of Andromedeae have been considered in one of two informal subgroups, i.e., the Lyonia group, comprising Lyonia Nutt. (36 spp.), Craibiodendron W. W. Smith (five spp.), Pieris D. Don (incl. Arcterica Coville) (seven spp.), and Agarista (31 spp., incl. Agauria J. D. Hooker) and the Gaultheria group, including Leucothoë D. Don (eight spp.), Zenobia D. Don (one sp.), Gaultheria L. (115 spp.), Pernettya Gaud. (14 spp., but this genus is often included within Gaultheria; see Middleton and Wilcock, 1990a ; Middleton, 1991b ), Tepuia Camp (seven spp.), and Diplycosia Blume (97 spp., incl. Pernettyopsis King and Gamble; see Stevens, 1995 ) (Stevens, 1970a , 1971, 1995; Judd, 1979 ; Middleton, 1991a , b; Kron and Judd, 1997 ). Andromeda L. (two spp.), Chamaedaphne Moench. (one sp.), and Oxydendrum DC (one sp.). have been considered to be taxonomically isolated (Stevens, 1969 , 1971). The Lyonia and Gaultheria groups are somewhat easier to characterize than the tribe as a whole. The members of the Lyonia group usually have multicellular hairs with biseriate stalks, slender, geniculate filaments, and short and rather broad anthers with white disintegration tissue at the anther–filament junction. Staminal appendages, when present, are spurs borne either on the filaments or dorsally on the anthers; the testa cells are much elongated and have thin walls; the foliar stomata are usually anomocytic; the upper epidermis of the leaf is often lignified; bands of fibers are found in the secondary phloem; and chromosome numbers are all x = 12. In contrast, the members of the Gaultheria group can be characterized by their multicellular hairs with multiseriate stalks; their stouter, straight filaments; often longer anthers with disintegration tissue on the anthers and terminal awns or lacking both awns and disintegration tissue; testa cells variable in shape, but often about as broad as long and distinctly thickened; often paracytic stomata; unlignified cells in the phloem not occurring in bands; and chromosome base numbers of x = 11, 12, 13, and 18.

Monophyly of the Andromedeae has never been rigorously assessed. Therefore, in this paper, we focus on the question of the group's monophyly and its appropriate circumscription. In addition, we investigate here the monophyly of both the Lyonia group and the Gaultheria group. The monophyly of the Gaultheria group has never been investigated, while the monophyly of the Lyonia group has been considered only in a preliminary fashion (Judd, 1979 ; Kron and Judd, 1997 ). Selected members of the Vaccinieae and Epacridoideae are included in these cladistic analyses because of previous analyses that indicated a close relationship to members of the Andromedeae (Anderberg, 1993 ; Kron and Chase, 1993 ; Kron, 1996 , 1997; Kron et al., 1998 ).

Ericaceae show a great deal of morphological variability and have been well studied from the standpoint of morphology, anatomy, embryology, and secondary chemistry (Niedenzu, 1890; Artopoeus, 1903 ; Samuelsson, 1913 ; Matthews and Knox, 1926 ; Cox, 1948 ; Palser, 1951 , 1952, 1954, 1958, 1961a, b; Chou, 1952 ; Copeland, 1954 ; Safijowska, 1960 ; Paterson, 1961 ; Wood, 1961 ; Lems, 1962 , 1964; Watson, 1962 , 1965; Leins, 1964 ; Towers, Tse, and Maas, 1966 ; Harborne, 1969 ; Stevens, 1969 , 1970a, b, 1971; Harborne and Williams, 1973 ; Villamil and Palser, 1981 ; Vander Kloet, 1983 , 1988; Baas, 1985 ; Rao and Chakraborti, 1985 ; Middleton and Wilcock, 1990a , b; Middleton, 1991a ; Odell and Vander Kloet, 1991; Anderberg, 1994 ; Powell et al., 1997 ). In addition, many of the genera considered here have been recently monographed or are part of recent floristic treatments (Sleumer, 1959 , 1966, 1967; Hersey and Vander Kloet, 1976 ; Dorr, 1980 ; Melvin, 1980 ; Judd, 1981 , 1982, 1984, 1986, 1990, 1995a, b, c; Judd and Hermann, 1990 ; Luteyn, 1991 , 1995a, b, c, 1996; Middleton, 1991b ; Luteyn et al., 1996 ), and their general phylogenetic placement within the Ericaceae can be assessed by reference to several higher level phylogenetic analyses that use morphology (Anderberg, 1993 ; Judd and Kron, 1993 ; Kron and Judd, 1997 ) and rbcL, matK, and nr18s sequence data (Kron and Chase, 1993 ; Kron, 1996 , 1997, and unpublished data; Kron and King, 1996 ; Kron and Judd, 1997 ; Kron et al., 1999 ).

Current studies by Kron (Kron, 1997 ; Kron and Judd, 1997 , and work in progress) indicate that matK is an appropriate gene to use for phylogenetic analysis in Ericaceae s.l. (sensu lato). Our knowledge of morphological and molecular variation within the Andromedeae certainly is now sufficient to undertake phylogenetic analyses of this group, and numerous recent studies have demonstrated the effectiveness of combined analyses of phenotypic and molecular data.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Representatives of all 13 genera of Andromedeae were sampled for this study. Twenty-eight taxa were sampled for the phenotypic cladistic analyses, while 29 taxa were included in the molecular analyses (Table 1). This study specifically tested the monophyly of the tribe Andromedeae and thus was not primarily concerned with generic limits. However, most of the genera within the tribe have been monographed and their monophyly is supported by morphological synapomorphies (Judd 1981 , 1982, 1984, 1986, 1995b). As discussed in Kron and Judd (1997; see also Weins, 1998 ) supraspecific taxa (i.e., genera and sections) were represented by particular species.


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  		Table 1.Ericalean species included in cladistic analyses of the Andromedeae. All species were used in both morphological and molecular analyses except Harrimanella hypnoides (see text); GenBank accession numbers are in brackets.a All species were traditionally placed in Andromedeae unless otherwise indicated

 
Character scorings for most of the 60 phenotypic characters (i.e., morphological, anatomical, and embryological—for convenience hereafter merely referred to as morphological characters) (Table 2) are based on the authors' observations of herbarium material and, where possible, living material, supplemented by revisionary and monographic studies (see references cited above). Character scorings relating to chromosome number and chemical features mainly were taken from the literature (see Table 3).


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  		Table 2.Characters used in morphology-based cladistic analysis of Andromedeae. Plesiomorphic characters are listed first, followed by apomorphic ones. (Polarity decisions based on trees rooted with Enkianthus.)

 

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  		Table 3.Character values for species used in morphology-based cladistic analysis. V = condition variable; ? = condition unknown or not applicable

 
Most morphological characters were readily divisible into discrete states, thus avoiding arbitrary decisions relating to state delimitation (Stevens, 1991 ). A few problems are noted in Table 3. Some characters could not be included in the analyses because they showed too much infrataxon variation or could not be delimited into discrete states, e.g., leaf size, inflorescence structure, bracteole position, calyx size, corolla shape and size, fruit shape, and placenta position. All multistate characters were considered to be unordered (Table 2). Species varying in particular characters were scored as "?" (and indicated as "variable" in Table 3).

Total DNA was extracted from fresh or silica-gel dried (Chase and Hills, 1991 ) leaves using the modified CTAB (hexadecyltrimethylammonium bromide) procedure of Doyle and Doyle (1987) . The matK gene of the chloroplast DNA was amplified by the polymerase chain reaction (PCR) via the methods described in Olmstead et al. (1992) using the same parameters as described in Kron et al. (1999) . Primer sequences from Johnson and Soltis (1994, 1995) and Steele and Vilgalys (1994) were used for matK PCR and sequencing. For the rbcL gene, primers and PCR protocols followed those of Olmstead et al. (1992) . Amplified products were cleaned using Microcon 100 filter tubes (Fisher Scientific, Atlanta, Georgia). The nucleotide sequencing was performed at the Wake Forest School of Medicine, DNA Core Laboratory on an ABI 377 Automated DNA Sequencer (Perkin-Elmer, Foster City, California). Raw sequences (for both rbcL and matK) were edited using Sequencher 3.0 (Gene Codes Corp., Ann Arbor, Michigan). The edited sequences were visually aligned.

Voucher information for all taxa sampled in this study can be obtained from KAK. All sequences can be obtained through GenBank (Table 1).

Phylogenetic analyses
Analyses of morphological data included representatives of outgroups identified as appropriate based on previous studies (Judd and Kron, 1993 ; Kron and Chase, 1993 ; Kron, 1996, 1997 ; Kron and Judd, 1997 ). Enkianthus campanulatus, Sprengelia incarnata, and Prionotes cerinthoides were used as outgroups. [Harrimanella (used in the molecular analyses) was not used as an outgroup taxon because its very different morphology makes determining character homology difficult.] Analyses of the morphological data were rooted with Enkianthus, allowing the remaining outgroup taxa to resolve simultaneously with the ingroup taxa. The analyses employed the branch-and-bound algorithm (ie-) with extended branch swapping (bb*) of the Hennig86, version 1.5, computer software developed by Farris (1988) , and the branch-and-bound option of PAUP (Phylogenetic Analysis Using Parsimony) 3.1.1. (Swofford, 1993 ).

As in the morphological study, analysis of molecular data (rbcL and matK nucleotide sequences) included representatives of outgroups identified as appropriate based on previous studies (Judd and Kron, 1993 ; Kron and Chase, 1993 ) and also on the basis of preliminary analysis of larger matK and rbcL data sets (Kron et al., 1999 ). These indicate appropriate potential outgroups as Enkianthus campanulatus, Harrimanella hypnoides, Sprengelia incarnata, and Prionotes cerinthoides; the latter two represent the epacrid clade (see Kron, 1997 ). Analyses of the molecular data were run with Enkianthus designated as the outgroup, allowing the remaining outgroup taxa to resolve simultaneously with the ingroup taxa. The few indels that occurred were treated as missing data. All characters were weighted equally in all analyses. The analyses were run using the heuristic search option (MULPARS, TBR, 1000 random replicates) of PAUP 3.1.1 (Swofford, 1993 ). Three measures of internal support were used to assess clade robustness when appropriate: parsimony jackknife (Farris et al., 1996 ) bootstrap (100 random replicates, both analyses) and decay (Autodecay 3.0; Mishler, Donoghue, and Albert, 1991 ; Eriksson and Wikstrom, 1995 ).

Combined parsimony analyses (1000 random replicates, MULPARS, TBR) based on rbcL + matK nucleotide sequences, and rbcL + matK + morphological data were performed using Enkianthus campanulatus, Prionotes cerinthoides, and Sprengelia incarnata, as outgroup taxa (and analysed by PAUP 3.1.1). Bootstrap (100 replicates) and decay analyses were performed to assess internal support for relationships obtained in the heuristic analyses.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Morphological data
The morphological analyses (Hennig86 and PAUP 3.1.1) resulted in the generation of 36 equally parsimonious trees of 139 steps, a consistency index (CI) of 0.48, and a retention index (RI) of 0.68. The topologies represented in these trees, however, are all quite similar, differing mainly in the placement of Andromeda and a few members of the Gaultheria group. The strict consensus (Fig. 1) and a representative cladogram (Fig. 2) are presented.



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  		Fig. 1. Strict consensus of all most parsimonious trees (36) from analysis of morphological data. Length (L) = 139, Consistency Index (CI) = 0.48, Retention Index (RI) = 0.68. Decay values are below lines. Taxa traditionally placed in the tribe Andromedeae are in boldface

 


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  		Fig. 2. Representative most parsimonious tree (one of 36) from the analysis of morphological data. Phylogenetically informative characters are mapped onto the tree using ACCTRAN optimization (DELTRAN optimizations are discussed in the text). Solid bars—unique; hatched bars—occur more than once in the tree; open bars—reversals. Taxa traditionally placed in the tribe Andromedeae are in boldface

 
Oxydendrum consistently is the sister group to all other ingroup taxa, which are are united on the basis of their inflorescences developing on shoots of the previous season (character no. 22) and the pedicel articulated with the flower (no. 26). Oxydendrum is quite distinctive because of its Calluna-type pith (no. 2-2), deciduous leaves (no. 10-0), and flowers in which all traces to the floral organs leave the elongated floral axis separately (Palser, 1952 ).

The monophyly of Vaccinieae (as represented by Vaccinium macrocarpon, V. meridionale, and Satyria warszewiczii) is supported by their inferior ovary (no. 46) and indehiscent fruit (no. 51-2), and this group is represented in most trees. Fleshy fruits (no. 49) are also synapomorphic for these species under a DELTRAN (see Wiley et al. [1991 ] for discussion of ACCTRAN and DELTRAN) optimization. However, Tepuia sometimes is placed within this clade, while in other trees it links with Diplycosia because they share apical connate bracteoles (no. 25) and methyl salicylate (no. 58). The Diplycosia + Tepuia clade, when present, may be sister to Vaccinieae (Fig. 2), due, in part, to their anther tubules (no. 41), or placed elsewhere in the tree, but these species are always phylogenetically adjacent to members of Vaccinieae. Thus, in the strict consensus tree (Fig. 1) the monophyly of Vaccinieae is not evident.

Several genera, i.e., Pieris, Lyonia, Agarista, and Gaultheria s.l., are consistently indicated as monophyletic. The monophyly of Pieris is supported by the inflorescence exposed during the winter (no. 23) and valvate calyx lobes (no. 27). Paired appendages located at the anther–filament junction (no. 39-1) are also synapomorphic under a DELTRAN optimization. Synapomorphies for the species of Lyonia include the corolla with multicellular hairs (no. 31), disintegration tissue on the staminal appendages (no. 43), ovary with multicellular hairs (no. 47), and capsule with thickened sutures (no. 50). Paired appendages on the filament (no. 39-2) are an additional synapomorphy under DELTRAN optimization. Agarista is supported by the apomorphies of leaves revolute in the bud (no. 4), leaves with a dense vein reticulum (no. 7), and stamens lacking appendages (no. 38). Gaultheria is monophyletic if Pernettya (as represented by P. tasmanica) is included, based on their fleshy calyx lobes (no. 28).

The Lyonia group is monophyletic in some trees, but is paraphyletic in others because Andromeda polifolia is placed within the group (as sister to Agarista). Characters supportive of the monophyly of the Lyonia group include bands of fibers in the phloem (no. 1), S-shaped filaments (no. 33), disintegration tissue on back of anthers (no. 42), and more or less elongated testa cells (no. 57). Members of this group also have leaves with lignified epidermal cells (no. 13) and anomocytic stomata (no. 20-0). Both features also occur in Andromeda and in some trees function as synapomorphies. Generic relationships within the Lyonia group are poorly resolved, but Craibiodendron is always sister to Lyonia (Figs. 1, 2), a relationship consistently supported by their homogeneous pith (no. 2-1) and bifacial leaf midrib bundles (no. 11).

The Gaultheria group is never monophyletic, although some of these genera, i.e., Gaultheria, Pernettya, Zenobia, Leucothoë, and also Chamaedaphne, are linked in a few cladograms by the base chromosome number of 11 (no. 59). Gaultheria, Pernettya, and Zenobia often form a clade based on the presence of forked anther appendages (no. 40). The monophyly of Leucothoë is equivocal, but L. racemosa and L. fontanesiana are sometimes linked by their inflorescences that are exposed during the winter (no. 23), a feature that also evolved in Pieris (Fig. 2).

Finally, although not a major focus in this investigation, we note that Sprengelia incarnata and Prionotes cerinthoides form a clade in all trees that is supported by the lignified leaf epidermis (character no. 13), elongated epidermal cells (no. 14), pedicel with several bracteoles (no. 24-2), and smooth staminal filaments (no. 36-2). These two species represent the epacrid clade (see Crayn et al., 1996 ; Powell et al., 1996 ; Kron, 1997 ; Kron et al., 1998 ).

Molecular data
Analysis of the rbcL data resulted in 42 trees (L = 503, CI = 0.58, RI = 0.50). The strict consensus (Fig. 3) indicates that few clades are well supported including: Vaccinieae (parjack 94), Lyonia (parjack 99), and the Pieris floribunda + P. formosa clade (parjack 90). Most of the structure in this tree collapses in trees one step longer. By contrast, the result of the matK analysis is much better resolved, especially within the Lyonia group (Fig. 4). In the matK analysis (four trees obtained, L = 980, CI = 0.65, RI = 0.62) Vaccinieae and members of the Gaultheria group form a clade strongly supported by the data. Within this clade Vaccinieae are monophyletic and form a polytomy with three other clades. The sister relationship of Andromeda polifolia and Zenobia pulverulenta is strongly supported by the matK data and there is strong support for Chamaedaphne calyculata sister to Leucothoë racemosa. These results are different from the morphological analysis (Fig. 1) where Andromeda is indicated as more closely related to the Lyonia group than the Gaultheria group. Similar to the morphological analysis, Lyonia and Pieris are monophyletic in the matK analysis. The Lyonia group (Lyonia, Craibiodendron, Pieris, Agarista) is monophyletic but not very strongly supported. In both the rbcL and matK analyses the Gaultheria group is placed in the same clade with a monophyletic Vaccinieae. In the matK analysis this large clade is strongly supported. The results of the rbcL analysis indicate only weak support for a Gaultheria group + Vaccinieae clade, with the clade collapsing in trees one step longer than most parsimonious (Fig. 3). The Gaultheria group is not supported as monophyletic by either the rbcL or the matK analyses. Both analyses indicate a core Gaultheria clade that includes Tepuia, Diplycosia, Gaultheria, and Pernettya. In the rbcL analysis Diplycosia is sister to Tepuia, whereas in the matK analysis Diplycosia is included in a polytomy containing Gaultheria and Pernettya. However, none of these relationships is strongly supported in either analysis.



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  		Fig. 3. Strict consensus of 42 trees found in the parsimony analysis of rbcL data. L = 503, CI = 0.58, RI = 0.50. Decay values are below lines, and parsimony jackknife values are above lines. Taxa traditionally placed in the tribe Andromedeae are in boldface

 


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  		Fig. 4. Strict consensus of four trees found in the parsimony analysis of matK data. L = 980, CI = 0.65, RI = 0.62. Decay values are below lines, and parsimony jacknife values are above lines. Taxa traditionally placed in the tribe Andromedeae are in boldface

 
Combined analysis of rbcL and matK data resulted in four most parsimonious trees (L = 1495, CI = 0.92, RI = 0.58). The strict consensus (Fig. 5) is highly resolved with Oxydendrum sister to the remaining ingroup taxa. As in the separate molecular data analyses Agarista, Lyonia, and Pieris are monophyletic, but in the combined analysis they each have higher levels of support than in each individual analysis. In the combined rbcL and matK analysis Vaccinieae are monophyletic and unresolved with respect to the Andromeda + Zenobia clade and the weakly supported clade that includes Leucothoë, Chamaedaphne, Tepuia, Diplycosia, Gaultheria, and Pernettya. In this analysis Gaultheria is paraphyletic with respect to Pernettya, a relationship also found in the rbcL and morphological analyses.



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  		Fig. 5. Strict consensus of four most parsimonious trees obtained from the combined analysis of rbcL and matK data. L = 1495, CI = 0.62, RI = 0.58. Decay values are below lines, and parsimony jacknife values are above lines. Taxa traditionally placed in the tribe Andromedeae in boldface

 
Combined molecular and morphological analysis
This analysis resulted in the generation of a single most parsimonious tree of 1565 steps, a consistency index (CI) of 0.61, and a retention index (RI) of 0.59 (Fig. 6). The position of Oxydendrum as sister to the remaining ingroup taxa is strongly supported.



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  		Fig. 6.  Single most parsimonious tree obtained from the combined analysis of morphology, rbcL, and matK data. L = 1565, CI = 0.61, RI = 0.59. Decay values are below lines, and bootstrap values are above lines. Taxa traditionally placed in the tribe Andromedeae are in boldface

 
The monophyly of the Lyonia group (incl. Agarista, Craibiodendron, Lyonia, and Pieris) is strongly supported (d8, 99% bootstrap). Noteworthy morphological features supportive of the monophyly of this group include bands of fibers in the phloem (no. 1), leaves with lignified epidermal cells (no. 13), S-shaped filaments (no. 33), and more or less elongated testa cells (no. 57). Within this clade, Agarista likely is sister to Pieris, and Craibiodendron is weakly supported as the sister group of Lyonia. Agarista, Pieris, and Lyonia are all strongly supported as monophyletic (Fig. 6); the monophyly of Craibiodendron was not assessed. Cladogram topology within the Lyonia group was identical to that discovered in our previous analysis of this group (Kron and Judd, 1997 ), and that paper should be consulted for a more detailed discussion of these generic and infrageneric relationships.

Vaccinieae form a well-supported clade (d24, 100% bootstrap) with members of the Gaultheria group, Andromeda, and Chamaedaphne. A significant morphological synapomorphy of this clade is paracytic stomata (no. 20). The Vaccinieae are clearly monophlyetic (d19, 100% bootstrap) and are supported by the same morphological characters as in the morphology-based analyses, with the addition of the anther tubules (no. 41). Such tubules evidently have evolved independently in a few other taxa, e.g., Chamaedaphne and the Tepuia + Diplycosia clade.

The remaining taxa, mainly members of the Gaultheria group, form a very weakly supported clade (d1, <50% bootstrap), which possibly is supported by the synapomorphy of a base chromosome number of 11 (although Andromeda has x = 12). In addition, forked appendages (no. 40) occur on the anthers of Zenobia, Gaultheria, and Pernettya and may have been lost from the remaining taxa. Within this group, Andromeda and Zenobia are sister to a potential clade (d1, 63% bootstrap) containing Chamaedaphne, Leucothoë, Tepuia, Diplycosia, Gaultheria, and Pernettya. However, a core element, containing Diplycosia, Tepuia, Gaultheria, and Pernettya is well supported (d11, 100% bootstrap). Members of this clade are united by the presence of methyl salicylate (lost in some species of Gaultheria and Diplycosia). They may also share the apomorphy of sepals that are fleshy and colorful, but the latter feature is absent in Tepuia (and in some species of Pernettya) and may have evolved independently in Diplycosia and Gaultheria. Tepuia and Diplycosia form a moderately well-supported clade (d3, 71% bootstrap) supported by apical connate bracteoles (#25) and anther tubules (no. 41), as do Gaultheria and Pernettya (d4, 84% bootstrap), which may be supported by fleshy, colorful sepals. Gaultheria likely is paraphyletic, justifying the inclusion of Pernettya. The monophyly of Leucothoë is not at all supported.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Results of phylogenetic analyses based on morphology, rbcL, and matK sequences (Figs. 1–4) are generally similar, although analyses based on single character sets are less well resolved than the combined analyses (Figs. 5–6). We note that the cladogram resulting from the analysis based on all three data sets, i.e., morphology and rbcL and matK sequences (Fig. 6), is better resolved and shows stronger statistical support for the various internal clades than any other tree produced in our analyses. This tree strongly supports the monophyly of the Lyonia group (including Lyonia, Craibiodendron, Agarista, and Pieris) and the Vaccinieae (including numerous inferior-ovaried genera), but provides only weak support for the Gaultheria group (circumscribed so as to include Andromeda and Chamaedaphne, as well as Zenobia, Leucothoë, Diplycosia, Tepuia, Gaultheria, and Pernettya). Recognition of the Andromedeae, as traditionally circumscribed (see Stevens, 1969, 1971, 1995 ), cannot be maintained, as genera of the Gaultheria group are more closely related to the Vaccinieae than they are to those of the Lyonia group. The strong support for the Lyonia group in the combined analysis indicates that the group should be given formal recognition, and it is here proposed as the tribe Lyonieae—Lyonieae Kron & Judd, tribus nov. Epidermis foliorum lignea; filamenta floris plerumque S-formis; testa cellulis plerumque elongatis. Type genus: Lyonia Nutt. Other nomenclatural proposals relating to these genera will be presented in connection with a new classification of the Ericaceae (Kron et al., unpublished data).

The monophyly of the Gaultheria group is not supported in most of the analyses and only weakly supported in the molecular + morphology analysis. In the combined rbcL and matK analysis the Gaultheria group is split into two clades that are not resolved with respect to Vaccinieae. Inclusion of the morphological data results in only a weakly supported Gaultheria group. This group needs further study, especially a more comprehensive sampling of Gaultheria, Pernettya, and Diplycosia. In addition, Leucothoë appears as paraphyletic or polyphyletic in most of the trees. Exceptions are in some of the morphological trees and in the rbcL analysis. In both cases the relationship of Leucothoë racemosa to L. fontanesiana is weakly supported.

Andromeda, Chamaedaphne, and Oxydendrum often have been considered taxonomically isolated (Palser, 1951, 1952 ; Stevens, 1969 , 1971), but our results support an isolated position for only Oxydendrum (Fig. 6).

Andromeda has several distinctive features, which probably represent autapomorphies, e.g., seeds with a strongly multilayered testa, campylotropous ovules (Palser, 1952 ), the lack of calyx and corolla stomata, and lack of multicellular hairs. The linking of this genus with Zenobia was not anticipated and is not reinforced by any morphological characters included in our analyses. The base chromosome number of Andromeda, i.e., 12, also is aberrant given its placement with genera of the Gaultheria group, which are mainly x = 11. However, it may be significant that Zenobia nearly lacks multicellular hairs, i.e., they are only associated with the leaf serrations, and if these were lost (as presumably occurred in the ancestors of Andromeda) then this genus, like Andromeda, would lack such hairs.

Chamaedaphne is distinctive in its floral anatomy, embryology, campylotropous ovules (Palser, 1951 , 1952), anthers with tubules, and distinctive lepidote indumentum (composed of peltate scales that are different in form from those of Lyonia sect. Lyonia; see Judd, 1979 ). Both molecular and morphological analyses place Chamaedaphne with members of the Gaultheria group. It is placed sister to Leucothoë racemosa in our combined analysis. Both have stamens with smooth filaments (no. 36-2; see Fig. 4, where feature is homoplasious). Stevens (1969) noted that "in stomata, bracteole, seed and general anatomical characters it shows some similarity to the Gaultheria group." For example, its stomata are positionally paracytic and testa cells isodiametric.

Oxydendrum also is phenetically distinctive, mainly because of its floral anatomy (all traces to the floral organs leave an elongated axis separately; Palser, 1952 ), deeply hooked leaf midrib vascular bundle (Stevens, 1969, 1971 ), anthers with terminal tubules, and terminal inflorescence that fruits in the same year in which the shoot on which it is borne was initiated (Lems, 1962 ). Cox (1948) considered Oxydendrum in its own tribe because its wood has a distinctive medullary ray type and a high percentage of porous vessel perforation plates. Our analyses suggest that these features represent a combination of autapomorphies and retained plesiomorphies.

Our results are in general agreement with those of Stevens (1969, 1971) , Judd (1979) , and Middleton (1991) in supporting the recognition of two major clades within the genera traditionally placed within Andromedeae. Clearly, they also support the hypothesis (see Stevens, 1995 ) that the Andromedeae are not monophyletic, since Vaccinieae are closely related to members of the Gaultheria group. The close relationship of Vaccinieae to some genera traditionally placed within Andromedeae was first noted by Stevens (1969, 1971) , and their phenetic similarity was evident to Watson, Williams, and Lance (1967) .

Higher level phylogenetic analyses of Ericaceae based on both nuclear and chloroplast DNA (see Kron and Chase, 1993 ; Kron, 1996, 1997 ; Kron et al., 1998 ) support the existence of a clade comprising Oxydendrum, the Gaultheria group, the Lyonia group, and the Vaccinieae, i.e., the ingroup taxa of the analyses herein presented. This monophyletic group, which in large part corresponds to the Vaccinioideae of Stevens (1969) , probably should be given subfamilial rank within an expanded Ericaceae (see Anderberg, 1993 ; Judd and Kron, 1993 ; Kron and Chase, 1993 ). The genera comprising this subfamily represent four clades, here listed in presumed order of divergence: (1) Oxydendrum, (2) Lyonia group, (3) Gaultheria group (as here recircumscribed), and (4) Vaccinieae.


   FOOTNOTES
 
1 This study was supported by National Science Foundation grant DEB-9407350 (KAK). Oligonucleotide synthesis was performed in the DNA Synthesis Core Laboratory of the Cancer Center of Wake Forest University supported in part by NIH grant CA-12197. The authors thank the following people and institutions for sending herbarium specimens and providing material for DNA extraction—Roger Hyam, Royal Botanic Garden, Edinburgh, Royal Botanic Garden, Kew, and New York Botanical Garden, Kent Perkins for assistance in processing specimens; and Norris Williams for making available certain computing facilities. Back

2 Author for correspondence. Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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