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American Journal of Botany 86(9): 1290–1300. 1999. 

PHYLOGENETIC ANALYSES OF ANDROMEDEAE 

(ERICACEAE SUBFAM. VACCINIOIDEAE) 1 

KATHLEEN A. KRON, 2,3 WALTER S. JUDD, 4 AND DARREN M. CRAYN 5 

3 Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27109-7325; 

4 Department of Botany, University of Florida, Gainesville, Florida 32611-8526; and 

5 School of Biological Science, University of New South Wales, Sydney 2052, Australia 

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. 

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1993; Stevens, 1995; Kron, 1996, 1997, and unpublished 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, 

1 Manuscript received 6 July 1998; revision accepted 23 February 

1999. 

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. 

2 Author for correspondence. 

1290 

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 tis-

September 1999] KRON ET AL.—PHYLOGENETICS OF ANDROMEDEAE 

1291 

sue; 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 

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 Andro- 

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); Gen- 

Bank accession numbers are in brackets. a All species were traditionally 

placed in Andromedeae unless otherwise indicated. 

Enkianthus campanulatus (Miq.) Nichols—outgroup [matK, GBAN- 

U61344; rbcL, GBAN-L12616] 

Harrimanella hypnoides (L.) Cov.—outgroup [matK, GBAN-U61315: 

rbcL, GBAN-U82766] 

Sprengelia incarnata Smith—as representative the epacrid clade, and 

as outgroup [matK, GBAN-AF015645; rbcL, GBAN-80421] 

Prionotes cerinthoides R. Br.—as representative of the epacrid clade, 

and as outgroup [matK, GBAN-AF015642; rbcL, GBAN-U79743] 

Agarista populifolia (Lam.) Judd [matK, GBAN-U61306; rbcL, 

GBAN-AF124589] 

Agarista salicifolia (Comm. ex Lam.) G. Don [matK, GBAN-U61313; 

rbcL, GBAN-AF124588] 

Andromeda polifolia L. [matK, GBAN-AF124569; rbcL, GBAN- 

AF124572] 

Chamaedaphne calyculata (L.) Moench. [matK, GBAN-AF015630; 

rbcL, GBAN-L12606] 

Craibiodendron yunnanense W. W. Smith [matK, GBAN-U61307; 


Diplycosia acuminata Becc. [matK, GBAN-AF124563; rbcL, GBAN- 

AF124586] 

Gaultheria miqueliana Takeda [matK, GBAN-AF124567; rbcL, 


Gaultheria shallon Pursh [matK, GBAN-AF124565; rbcL, GBAN- 

AF124574] 

Pernettya tasmanica J.D. Hooker [matK, GBAN-AF124568; rbcL, 

GBAN-U82765] 

Leucothoë racemosa (L.) Gray [matK, GBAN-AF124564; rbcL, 

GBAN-U83915] 

Leucothoë fontanesiana (Steudel) Sleumer [matK, GBAN-AF124570; 


Lyonia ligustrina (L.) DC. [matK, GBAN-U61311; rbcL, GBAN- 

AF124578] 

Lyonia ferruginea (Walter) Nutt. [matK, GBAN-U61312; rbcL, 


Lyonia lucida (Lam.) K. Koch [matK, GBAN-U61308; rbcL, GBAN- 

U82764] 

Lyonia ovalifolia (Wallich) Drude ([matK, GBAN-U61305; rbcL, 


Oxydendrum arboreum (L.) DC. [matK, GBAN-AF124562; rbcL, 


Pieris phillyreifolia (W.J. Hooker) DC. [matK, GBAN-U61309; rbcL, 


Pieris floribunda (Pursh) Bentham and Hooker [matK, GBAN- 

U61304; rbcL, GBAN-AF124577] 

Pieris formosa (Wallich) D. Don [matK, GBAN-U61303; rbcL, 


Pieris nana (Maxim.) Makino [matK, GBAN-U61310; rbcL, GBAN- 

AF124582] 

Satyria warszewiczii Klotzsch [matK, GBAN-U61314; rbcL, GBAN- 

AF124579] 

Tepuia cardonae A. C. Smith [matK, GBAN-AF124566; rbcL, 


Vaccinium macrocarpon Aiton [matK, GBAN-U61316; rbcL, GBAN- 

L12625] 

Vaccinium meridionale Sw. [matK, GBAN-U89759; rbcL, GBAN- 

AF124576] 

Zenobia pulverulenta (Bartram ex Willd.) Pollard [matK, GBAN- 

AF124571; rbcL, GBAN-L12626] 

a The prefix GBAN- has been added for linking the online version of 

American Journal of Botany to GenBank but is not part of the actual 

GenBank accession number.

1292 AMERICAN JOURNAL OF BOTANY 

[Vol. 86 

medeae 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. 

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). 

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 

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. 

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


1293 

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.) 

1. Secondary phloem without bands of fibers (0); secondary phloem with bands of fibers (1). 

2. Pith heterogeneous (0); pith homogeneous (1); pith Calluna-type (2). [unordered] 

3. Bud scales numerous to 2, if the latter then minute (0); bud scales 2, enlarged (1). 

4. Leaves convolute in bud (0); leaves revolute in bud (1). 

5. Leaves alternate (0); leaves whorled (1). 

6. Leaf venation pinnate (0); leaf venation parallel (1). 

7. Vein reticulum open, the secondary and tertiary veins not equally prominent (0); vein reticulum dense, the secondary and tertiary veins 

equally prominent (1). 

8. Leaf margin serrate or serrulate (0); leaf margin entire (1). 

9. Leaf margin lacking raised glands (0); leaf margin with raised glands (1). 

10. Leaves deciduous (0); leaves persistent (1). [polarity questionable; see Table 3] 

11. Leaf midrib (as seen in cross section) unifacial (0); leaf midrib bifacial (1). 

12. Fiber strands absent from leaf mesophyll (0); fiber strands present in leaf mesophyll (1). 

13. Leaf epidermis not lignified (0); leaf epidermis at least slightly lignified (1). 

14. Leaf epidermal cells not elongated (as seen in cross section) (0); epidermal cells elongated (1). 

15. Hypodermis lacking (0); hypodermis present (1). 

16. Multicellular hairs on leaves present (0); multicellular hairs lacking (1). 

17. Multicellular hairs with small glandular head (or hairs not glandular) (0); multicellular hairs with expanded and elongated, glandular head (1). 

18. Peltate scales lacking (0); peltate scales present (with margin irregular-erose) (1); peltate scales present (with margin entire) (2). [unordered] 

19. Stalk of multicellular hair multiseriate (0); stalk of multicellular hair biseriate (1). 

20. Stomata anomocytic (0); stomata paracytic (1); stomata tetracytic (2). [unordered] 

21. Inflorescences monotelic, i.e., terminal flowers present (0); inflorescences polytelic, i.e., terminal flowers lacking (1). 

22. Inflorescences developing (and producing flowers and fruits) on shoots of the current season (0); inflorescences developing (and producing 

flowers and fruits) on shoots of the previous season (1). 

23. Inflorescences within bud (0); inflorescences exposed during winter or dormant season (1). 

24. Pedicel lacking bracteoles (0); pedicel with two bracteoles (1); pedicel with several bracteoles (2). [unordered] 

25. Bracteoles distinct, variably positioned (0); bracteoles connate, apical (1). 

26. Pedicel not articulated with flower (0); pedicel articulated with flower (1). 

27. Calyx of imbricate lobes (0); calyx of valvate lobes (1). 

28. Calyx lobes brown, dry at maturity (0); calyx lobes usually colorful, fleshy at maturity (1). 

29. Adaxial calyx stomata lacking (0); adaxial calyx stomata present (1). 

30. Corolla lacking unicellular hairs on inside surface (0); corolla with unicellular hairs on inside surface (1). 

31. Corolla lacking multicellular hairs on outer surface (0); corolla with multicellular hairs on outer surface (1). 

32. Abaxial corolla stomata present (0); abaxial corolla stomata absent (1). 

33. Filaments straight (0); filaments S-shaped (1). 

34. Filaments distinct (0); filaments connate (1). 

35. Filaments free from corolla (0); filaments adnate to corolla (1). 

36. Filaments with unicellular hairs (0); filaments papillose or minutely roughened (1); filaments smooth (2). [unordered] 

37. Anthers inverting late in development (0); anthers inverting early in development (1). 

38. Anthers with projections (awns or spurs) (0); such projections absent (1). 

39. Projections borne on anther, erect to deflexed (0); projections borne at junction of anther and filament (1); projections borne on filament (2). 

[unordered] 

40. Projections single (or lacking) (0); projections divided (1). 

41. Tubules on anthers absent (0); tubules on anthers present (1). 

42. Disintegration tissue on back of anthers absent (0); disintegration tissue present (1). 

43. Disintegration tissue not extending onto the spurs (or spurs lacking) (0); disintegration tissue extending onto the spurs (1). 

44. Anthers open by longitudinal slits (0); anthers open by ‘‘terminal’’ pores (1). 

45. Pollen shed as monads (0); pollen shed as tetrads (or modified tetrads) (1). 

46. Ovary superior (0); ovary inferior (1). 

47. Ovary lacking multicellular gland-headed hairs (0); ovary with multicellular gland-headed hairs (or homologous hair types, e.g., scales) (1). 

48. Locules not divided (0); locules incompletely divided by outgrowth of ovary wall (1). 

49. Fruit dehiscent (0); fruit indehiscent (1). 

50. Fruit lacking thickened sutures (0); fruit with thickened sutures that often separate from the valves in dehiscence (1). 

51. Fruit a capsule (0); fruit a berry (1). 

52. Seed with vascular bundle in the raphe (0); seed lacking vascular bundle in the raphe (1). 

53. Seed lacking fringe formed from differentiated cells (0); seed with fringe due to expanded and/or elongated, bulging cells (1). 

54. Seed lacking tails (0); seed with tails, i.e., expanded portion of testa at hilum and chalazal ends (1). 

55. Seed lacking unilateral wing (0); seed with unilateral wing (resulting from a flattening of chalazal end of seed, with cells of the wing not 

differentiated from those of the body) (1). 

56. Testa one-layered (except sometimes in the raphe) (0); testa with several cell layers (1). 

57. Testa cells isodiametric (in surface view) (0); testa cells much elongated (1). 

58. Methyl salicylate lacking (0); methyl salicylate present (1). 

59. Basic chromosome number 11 (0); 12 (1); 18 (2). [unordered] 

60. Toxic diterpenes of andromedotoxin type absent (0); toxic diterpenes of andromedotoxin type present (1).


[Vol. 86 

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

applicable. 

Species 

Character 

1 2 3 4 5 6 

123456789012345678901234567890123456789012345678901234567890 

Enkianthus campanulatus 000000000000000000000000000000000000000000000000000000000000 

Prionotes cerinthoides 0100000001011100000000020000000?000211?0000010000001000000?0 

Sprengelia incarnata 0100010101001101?0?200020000000?101211?000001000000100001010 

Agarista populifolia 1201001V010010000000V10101000000100011?00101100000010000101? 

Agarista salicifolia 10010011010010100000110101000000100011?0010110000001000010?? 

Pieris floribunda 1000001001000000001011110110100100001010010110000001000010?1 

Pieris formosa 100000000100100000101111011010010000101001011000000100001011 

Pieris phillyreifolia 1000000001001000001011110110100110021010010110000001000000?1 

Pieris nana 11001001010010000010111101100001000110100V0110000001000010?1 

Craibiodendron yunnanense 11000001011110000010010101000000100111?0010110000001001010?? 

Lyonia ferruginea 1100000101101000011011010100001010011V2001111010010101001011 

Lyonia lucida 110000010110100000101101011000101001102001111010010100001011 

Lyonia ligustrina 101000000010V00010101101011000101000102001111010010100001011 

Lyonia ovalifolia 111000010V10V000101011010110001010001020011110V0010100001011 

Vaccinium macrocarpon 01000001010000000001?00101000000000011?010011100102100000010 

Vaccinium meridionale 01000000010000100001110101000000000101010011101102100000010 

Satyria warszewiczii 01000001011000000001110101000000010011?01001110010210000V0?0 

Leucothoë fontanesiana 020000000100000000011111010000000001100001011000000110000001 

Leucothoë racemosa 010000000000000000011111010000000002100001011000000100000001 

Andromeda polifolia 0001000101001001?0?011010100010100001000000011000000100010011 

Zenobia pulverulenta 100000000000000000001101010000000001100101011000000100000001 

Chamaedaphne calyculata 0100001001000000020V11010100000V0002100010011000000100000001 

Diplycosia acuminata 01000000010100100001V10111010000V00211?01001100000010000112? 

Gaultheria miqueliana 000000000100000000011101010100000001100101011000000100000101 

Gaultheria shallon 0000010000100000000011101010101100000100101011000000100000001 

Pernettya tasmanica 00000000010000100001?102010101000000100100011000101100000001 

Tepuia cardonae 01000001110000100001100111000V0?000011?0100110001011000001?? 

Oxydendrum arboreum 0200000V000000000001100100000000000011?001011000000100001011 

Note: 25: Enkianthus scored as ‘‘0’’ because it has free bracts, which are homologous to bracteoles. 28: the coding of this character for members 

of the Vaccinieae, e.g., Vaccinium and Satyria, is problematic; they are coded as ‘‘0’’ based on the assumption that the colorful, fleshy sepals in 

Gaultheria and Diplycosia developed independently from the fleshy fruits of Vaccinieae; developmental studies would be useful. 60: See also 

Hegnauer (1966) and Anderberg (1993). 

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


1295 

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. 

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. 

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. 

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. 

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 inde-


[Vol. 86 

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.


1297 

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. 

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. 

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. 

pendently 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 

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


[Vol. 86 

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 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


1299 

(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. 

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