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Systematics and Phytogeography |
Department of Biology and Microbiology, University of Wisconsin Oshkosh, Oshkosh, Wisconsin 54901 USA
Received for publication July 18, 2000. Accepted for publication December 14, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Brighamia • Campanulaceae • Cyanea • Delissea • Lobelioideae • scanning electron microscopy • seed coat morphology
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1200 species assigned to 29 currently recognized genera (T. G. Lammers, unpublished data). In recent years, much taxonomic attention has been focused on the subfamily, due to the growing realization that its existing classification (Wimmer, 1943, 1953, 1968
) is suboptimal in many respects (Rosatti, 1986
; Ayers, 1990
; Lammers, 1993, 1998a, 1999a
; Pepper, Gustafsson, and Albert, 1997
; Serra, Crespo, and Lammers, 1999
). Phylogenetic analyses of DNA restriction site mutations and gene sequences hold great promise for an improved understanding of systematic relationships among Lobelioideae (Knox, Downie, and Palmer, 1993
; Givnish et al., 1995
; Dotti and Ayers, 1997
; Pepper, Gustafsson, and Albert, 1997
; Schultheis and Baldwin, 1997
; Knox and Palmer, 1998
). However, for practical purposes, any clades revealed by sophisticated molecular analyses also must be distinguishable on the basis of more readily observed features (cf. Grant, 1998
).
Among the various types of nonmolecular data germane to Lobelioideae, seed coat morphology appears to be of great value. Compared to many vegetative and floral structures, seed coat morphology shows very little plasticity; variation among individuals and taxa almost certainly reflects genetic and phylogenetic differences (Barthlott, 1984
). McVaugh (1936, 1940a, b, 1943)
relied heavily on seed coat characters in distinguishing genera and infrageneric groupings of North American lobelioids. More recently, Murata (1992, 1995)
has examined a diversity of lobelioid seeds via scanning electron microscopy (SEM). The testal characters he emphasized correlated well with certain vegetative and floral features (e.g., habit, anther trichomes), as well as with additional data not available to Wimmer (1943, 1953, 1968)
, i.e., chromosome numbers (Lammers, 1993
) and chloroplast genome rearrangements (Knox, Downie, and Palmer, 1993
). Synthesis of these data led to a revision of the supraspecific classification of the largest genus in the subfamily, Lobelia L. (Murata, 1995
).
The objective of the present study was to extend Murata's surveys to lobelioid genera in which he examined few or no species. Particular emphasis was placed on genera endemic to the Hawaiian Islands (Lammers, 1988, 1989, 1990, 1991, 1995
), especially Cyanea Gaudich. (including Rollandia Gaudich.; cf. Lammers, Givnish, and Sytsma, 1993
), as these plants recently have been the focus of detailed molecular phylogenetic studies (Givnish et al., 1994, 1995, 1996a, b
). As noted by Givnish et al. (1995)
, the clades revealed by these analyses correlate very poorly with previous sectional classifications (Hillebrand, 1888
; Rock, 1919
; Wimmer, 1943
); the vegetative and floral characters used by earlier authors to characterize taxonomic sections do not distinguish the molecularly based clades. It thus was anticipated that seed morphology could offer a nonmolecular basis for their recognition. Seeds of additional non-Hawaiian lobelioids were likewise examined with an eye towards answering various other taxonomic questions that have arisen over the years.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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did not examine (Brighamia A. Gray, Delissea Gaudich., Hippobroma G. Don, Legenere McVaugh) or to large ones in which he examined only one species (Cyanea, Centropogon C. Presl, Siphocampylus Pohl). For Cyanea (72 species endemic to Hawaii; Lammers, 1990, 1996, 1998b
), 26 species were examined. This sample included a minimum of three species from each of the three (Hillebrand, 1888
; Wimmer, 1943
) or five (Rock, 1919
) sections recognized in previous classifications, as well as a minimum of two species from each of the six clades identified in the recently published molecular phylogeny of the genus (Givnish et al., 1994, 1995
). For Delissea (11 species endemic to Hawaii; Lammers, 1990, 1998b, 1999b
), two species were studied, one from each of the two sections recognized (Hillebrand, 1888
; Wimmer, 1943
; Rock, 1919
). For Centropogon and Siphocampylus (each with 216 species in the neotropics; Lammers, 1998a
), four species of the former and five of the latter were examined. Our coverage of species was complete for Brighamia (two species endemic to Hawaii; Lammers, 1989
), Hippobroma (one species originally endemic to Jamaica but now widespread in the tropics; McVaugh, 1940a
), and Legenere (a single species distributed amphitropically in California and temperate South America; Ruiz de Ciolfi, 1976
).
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8 nm of gold/palladium and examined in a Hitachi 2460N SEM at 25 kV, 20 mm working distance, and a consistent spot size. The resulting images were recorded on Polaroid type 55 film. Magnification was verified by photographing a calibration standard (Ladd Research Industries, Burlington, Vermont, USA) at the same instrument settings used for viewing seed samples. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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for the Lobelioideae (Table 1). Type B seeds, characterized by a weakly or distinctly reticulate surface, sometimes verruculate on the reticulum, were found in all examined species of Centropogon C. Presl and Siphocampylus Pohl (Figs. 3–6, 37–41). Type C seeds, characterized by a striate or striate-verruculate testa, were found in 21 of the 26 species of Cyanea examined, including those formerly segregated as Rollandia (Figs. 7, 9–10, 13–15, 17–27, 29–32). Type D seeds, characterized by a wavy-striped or beaded testa, were found in Legenere McVaugh (Fig. 36), while Type E seeds, which resemble Type B but lack a cuticle, were found in Hippobroma G. Don (Fig. 35).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Five of the genera (Brighamia, Clermontia Gaudich., Cyanea, Delissea, and Trematolobelia Zahlbr. ex Rock) are endemic, while cosmopolitan Lobelia is represented by two endemic sections of subg. Tupa (G. Don) E. Wimm.: sect. Galeatella E. Wimm. and sect. Revolutella E. Wimm.
Until recently, it was believed that the Hawaiian Lobelioideae were polyphyletic, i.e., that they were the evolutionary result of multiple introductions to the archipelago from continental source areas via long-distance dispersal (Rock, 1919
; Brown, 1921
; Skottsberg, 1928
; Stone, 1967
; Carlquist, 1974
; Lammers and Freeman, 1986
; Lammers, 1988, 1990
). This hypothesis was based on differences in the morphology of inflorescences, flowers, and fruits. A single introduction was hypothesized for Clermontia, Cyanea, and Delissea, the three genera with axillary inflorescences, curved bilabiate or unilabiate corollas, and fleshy indehiscent fruits. A second extra-Hawaiian ancestor was hypothesized for Brighamia, which also has axillary inflorescences, but straight salverform corollas and dry dehiscent fruits (albeit fleshy-walled at first). Finally, one to three additional origins were proposed for the taxa with terminal inflorescences, curved bilabiate or unilabiate corollas, and dry dehiscent fruits: the two sections of Lobelia plus Trematolobelia.
In contrast to these morphological data, phylogenetic analyses of molecular data (Givnish et al., 1995, 1996a
; E. Knox, Rutgers University, personal communication) strongly support the monophyly of the Hawaiian lobelioids. These data indicate that all six genera evolved from a single colonization of the archipelago. Within this lineage, Delissea is not allied to Clermontia-Cyanea, as suggested by morphology, but rather is sister to Brighamia. The Brighamia-Delissea clade is then the sister-group of Clermontia-Cyanea. Because Trematolobelia and the two sections of Lobelia form the basal branches of the Hawaiian clade, it has been hypothesized (Knox, Downie, and Palmer, 1993
; Givnish et al., 1995, 1996a
) that the extra-Hawaiian progenitor of the Hawaiian Lobelioideae was most likely an Asian species referable to Lobelia subg. Tupa, with terminal inflorescences, curved bilabiate or unilabiate corollas, and dry dehiscent fruits. Our seed data offer support for various aspects of these molecular findings.
Origin of the Hawaiian Lobelioideae
All Hawaiian Lobelioideae examined have either Type C seeds or unique testal patterns that appear to be modified from a Type C pattern (i.e., Type F and Type G). This uniformity of testal pattern supports the monophyly of the Hawaiian Lobelioideae. If the Hawaiian lobelioids in fact stemmed from three to five independent introductions, one might expect at least some of the genera to show other testal patterns.
Outside the Hawaiian Islands, Type C seeds have been reported only from certain members of Lobelia subg. Tupa, specifically Asian species of sect. Colensoa (Hook. f.) Murata and African species of sect. Rhynchopetalum (Fresen.) Benth. (Murata, 1992, 1995
). In the molecular analysis of Knox, Downie, and Palmer (1993)
, all Type C species fell into a single clade that was sister to the remainder of the subfamily; no other seed coat type was found within this clade (Murata, 1995
). Thus, on the basis of seed morphology alone, one might hypothesize that the ancestor of the Hawaiian lobelioids would be referable to these members of Lobelia subg. Tupa. In fact, Asian species of sect. Colensoa (e.g., L. nicotianifolia Roth ex Schult.) are very similar to sect. Revolutella in overall morphology (Rock, 1919
; Skottsberg, 1928
; Stone, 1967
; Carlquist, 1974
; Lammers, 1990
) and have been particularly implicated as ancestors of the Hawaiian lobelioids on the basis of recent molecular data (Knox, Downie, and Palmer, 1993
; Givnish et al., 1995, 1996a
). Earlier suggestions that the fleshy-fruited genera in Hawaii (Clermontia, Cyanea, Delissea) are derived from South American species of Centropogon (Hemsley, 1885
; Drake del Castillo, 1890
; Guppy, 1906
; Rock, 1919
; Brown, 1921
; Wimmer, 1943
; Stone, 1967
; Carlquist, 1974
) are not supported by our data. As noted below, all species of Centropogon that have been examined have Type B seed coats.
Relationship of Brighamia to Delissea
The unique Type G testal pattern found in Brighamia and Delissea supports the close relationship between these two genera revealed by the molecular analyses. It argues against a close relationship between Delissea on the one hand and Clermontia and Cyanea on the other (Rock, 1919
; Stone, 1967
; Carlquist, 1974
; Lammers, 1988, 1990
) and against the proposed merger of Cyanea and Delissea (St. John, 1987
; St. John and Takeuchi, 1987
). In addition to testal pattern, seeds of Brighamia and Delissea differ from all other Hawaiian Lobelioideae in their white color and large size (Hillebrand, 1888
; Rock, 1919
; Wimmer, 1943
; Lammers, 1990
; Givnish et al., 1995
); seeds of the other genera are dark brown or black and only one-half to one-third as large. These three traits collectively, then, offer morphological synapomorphies for the convenient recognition of a clade detected by molecular means.
Previous workers (Rock, 1919
; Degener, 1937
; Stone, 1967
; St. John, 1969a
) have suggested that Brighamia was derived from Isotoma (R. Br.) Lindl. (11 species endemic to Australia; Lammers, 1999a
) or Hippobroma (see below), based on their common possession of an unusual salverform corolla. Seed morphology will support neither of these hypotheses: Murata (1995)
reported Type B seeds in the one species of Isotoma he examined, while Type E is reported here for Hippobroma (see below).
Sectional relationships within Cyanea
Cyanea was the only genus examined in which two distinct testal patterns were observed. Twenty-one of the 26 accessions showed Type C morphology, as reported by Murata (1995)
for C. kunthiana. The species with this seed type belonged to four of the five sections recognized by Rock (1919)
: sect. Cyanea (C. grimesiana subsp. grimesiana, C. horrida, C. longissima, C. platyphylla, C. shipmanii), sect. Hirtellae Rock (C. hirtella, C. kuhihewa, C. membranacea), sect. Palmiformes (Hillebr.) Rock (C. hamatiflora subsp. hamatiflora, C. leptostegia, C. macrostegia, C. solenocalyx, C. truncata), and sect. Pilosae Rock (C. acuminata, C. copelandii subsp. copelandii, C. floribunda, C. kunthiana, C. stictophylla). The species formerly segregated (Hillebrand, 1888
; Rock, 1919
; Wimmer, 1943
; Stone, 1967
; Lammers, 1990
) as Rollandia (C. calycina, C. humboldtiana, C. longiflora) also had this type seed, data that further support their merger (Lammers, Givnish, and Sytsma, 1993
). Type C seeds were also found in species belonging to five of the six molecularly based clades recognized by Givnish et al. (1995)
: the four sublineages making up the Orange-fruited Clade, plus the Leptostegia Clade within the Purple-fruited Clade.
The remaining five accessions showed the Type F testal pattern, characterized by rounded, knob-like protuberances on the radial walls at the opposite ends of the cells. All five are referable to sect. Delisseoideae (Hillebr.) Rock, and three (C. angustifolia, C. coriacea, and C. hardyi) have been included in molecular-based phylogenetic analyses (Givnish et al., 1994, 1995
). Together with C. spathulata (Hillebr.) A. Heller (for which we were unable to obtain mature seed), they formed the Hardyi Clade, the other sublineage within the Purple-fruited Clade. The other two species with this seed type, C. fauriei and C. "pseudofauriei," were not included in the molecular analyses, but would appear referable to the Hardyi Clade based on their resemblance to C. coriacea and C. hardyi in various characters. This unique seed coat pattern thus offers a morphological marker for the recognition of the Hardyi Clade. In a formal classification, the name sect. Delisseoideae would be available for this clade, as C. angustifolia is its lectotype (St. John, 1969b
).
Distinctness of Centropogon and Siphocampylus
These two large neotropical genera are very similar overall and frequently confused by collectors. The only character by which they can be distinguished is fruit type: fleshy indehiscent berries in the former, dry apically dehiscent capsules in the latter (Wimmer, 1943, 1953
; Lammers, 1998a
). Preliminary molecular studies (Pepper, Gustafsson, and Albert, 1997
) indicate that this is not a sound basis for recognition, as species of the two genera are interdigitated throughout the resulting cladograms. It appears that Centropogon is polyphyletic, having arisen at several points within Siphocampylus through an apparently simple shift from capsular to baccate fruit.
The four species of Centropogon and five species of Siphocampylus examined confirm Murata's (1995)
previous findings of Type B seeds in one species of each genus. Despite having what would seem to be very different types of fruit, the seeds of the two genera are of the same type. Given the large size of these genera (216 species each), our data are far from comprehensive. However, they do offer some support for the hypothesis that Centropogon and Siphocampylus are closely related if not congeneric.
Affinities of Legenere
Legenere comprises a single annual species amphitropically distributed in ephemeral wetland habitats in California, Chile, and Argentina (Ruiz de Ciolfi, 1976
). Although Wimmer (1953)
considered it taxonomically isolated within the family, relegating it to the monotypic subtribe Legenerinae E. Wimm., recent molecular studies (Schultheis and Baldwin, 1997
) have shown that it forms a clade with three other western North American genera of annual plants growing in similar habitats: Downingia Torr. (also found in Chile and Argentina), Howellia A. Gray, and Porterella Torr. Our finding of Type D seeds in Legenere offers some support of this hypothesis. Murata (1995)
reported this type of seed in one species of Downingia, and earlier line drawings of Downingia seeds executed via light microscopy (McVaugh, 1941
, figs. 14–16) also appear to represent the Type D testal pattern.
Affinities of Hippobroma
Hippobroma comprises a single species originally endemic to Jamaica but now found throughout much of the tropics (McVaugh, 1940a
). As noted above, the genus has been thought to be allied to Brighamia or Isotoma, primarily due to its unusual salverform corolla (Wimmer, 1953
; Stone, 1967
; St. John, 1969a
). Our finding of Type E seeds in Hippobroma does not support that hypothesis. Brighamia has the new Type G testal type (Figs. 1–2), while the one species of Isotoma examined by Murata (1995)
had Type B seeds.
The only lobelioid reported by Murata (1995)
that had Type E seeds was Lobelia grandifolia Britt. of Jamaica. Although Murata (1995)
assigned that species to sect. Pratia (Gaudich.) Murata, it is better accommodated in sect. Tylomium (C. Presl) Benth. (Adams, 1972
; Wilbur, 1991
; Lammers and Proctor, 1994
), a group characterized by bilabiate or unilabiate curved corollas. Because these are the only two species known with Type E seeds, it is reasonable to hypothesize that they are closely related. Just as in Hawaii, salverform Brighamia appears to be most closely related to bilabiate/unilabiate Delissea, so too do our data suggest that in the West Indies, salverform Hippobroma appears to be most closely related to bilabiate/unilabiate Lobelia sect. Tylomium.
Summary
Seed coat morphology continues to prove useful in understanding systematic relationships within the Lobelioideae. In particular, testal patterns may offer hallmarks for the convenient recognition and description of clades revealed by phylogenetic analysis of DNA sequences and other molecular characters. Though the surveys of Murata (1992, 1995)
were extensive, they were not exhaustive; two new testal patterns were discovered within the Hawaiian clade of the subfamily and additional patterns may remain to be uncovered.
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FOOTNOTES |
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2 Author for reprint requests (lammers{at}uwosh.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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