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Systematics and Phytogeography |
2Department of Botany, University of Oklahoma, Norman, Oklahoma 73019-0245 USA; 3Falklands Conservation, P.O. Box 26, Stanley, Falkland Islands
Received for publication June 11, 2002. Accepted for publication October 10, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: ITS • Littorella • molecular systematics • Plantaginaceae • Plantago
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Rahn, 1996
). It has a worldwide distribution and it is well represented throughout most geographic regions with the exception of the Antarctic continent, much of the Arctic, and the lowland tropics (Pilger, 1937
). Some Plantago species such as P. lanceolata L. and P. major L. are almost ubiquitous weeds and, in some cases, agricultural pests, while others such as P. tasmanica Hook.f. and P. moorei Rahn are highly specialized endemics. Historically, all but four species within the family have been placed in the large cosmopolitan genus Plantago L. The remaining two genera are Bougueria Decne., a monotypic genus found in the Peruvian Andes, Bolivia, and Argentina represented by B. nubicola Decne., and Littorella Berg., represented by three closely related species, L. americana Fernald, L. australis Griseb. ex Bentham & Hooker, and L. uniflora (L.) Ascherson. A recent study (Olmstead et al., 2001
) placed Plantaginaceae within Veronicaceae. Since the former name has priority over the latter, some authors have advocated broadening the circumscription of Plantaginaceae to encompass Veronicaceae (Judd et al., 1999
); however, our paper will use the family name "Plantaginaceae" in its historical context to avoid confusion.
Littorella was first described by Bergius (1768)
as a monotypic genus represented by Littorella juncea Berg. However, Bergius listed Plantago uniflora L. (Linnaeus, 1753
) as a synonym of L. juncea in the protologue, thus failing to adopt the earliest available epithet for his species. Linnaeus (1771)
later accepted Littorella as a genus but published an illegitimate name, Littorella lacustris L., for Bergius' taxon, and this name persisted until Ascherson (1864)
published the combination Littorella uniflora (L.) Aschers.
Littorella is characterized by morphological and anatomical characters that are not found elsewhere in the Plantaginaceae. The flowers are monoecious, the fruits contain a single anatropous ovule, and plants are capable of reproducing vegetatively by means of stolons (Tessene, 1968
; Rahn, 1996
; Robe and Griffiths, 1998
; Correa, 1999
). The stems, leaves, and roots of Littorella have an extensive series of internal lacunae, a character state shared only with P. cordata Lam. within Plantaginaceae. Within the genus, plant size, the arrangement and position of the pistillate flowers on the scape, and differences in pedicel length of the staminate flowers are the only morphological character states currently used to separate the species (Fernald, 1918
; Moore, 1983
; Rahn, 1996
). Representatives of the genus are small, herbaceous perennials with an abbreviate stem or occasionally a short caudex, fibrous roots, and frequently adventitious roots. The leaves are rosulate, evergreen, linear, terete to subterete, and glabrous. Littorella uniflora specimens tend to be more robust than those of L. americana and L. australis. In all three species, the staminate flowers are solitary and terminal on short scapes. The pistillate flowers of L. uniflora and L. americana are clustered in whorls of 2–5 in the leaf axils and are subtended by a single bract. The individual flowers are obscured by the leaf sheaths except for the long styles. Pistillate flowers of L. australis occur irregularly grouped along the basal half of the scape or occasionally above the midpoint of the scape (Bentham and Hooker, 1876
). The ovaries in all three species are unilocular and the fruits are small, indehiscent nuts with a thick pericarp, character states shared only with B. nubicola within the Plantaginaceae (Rahn, 1996
). Flower induction in Littorella occurs solely in emersed plants. While many populations are always submersed reproducing strictly by cloning and forming large genets, other populations are subject to emersion due to seasonal changes in water levels allowing flower induction and sexual reproduction (Hostrup and Wiegleb, 1991
; Robe and Griffiths, 1998
). Littorella uniflora commonly flowers and produces mature fruits while L. americana and L. australis are seldom observed in flower and rarely produce mature fruits (Bentham and Hooker, 1876
; Fernald, 1918
; Tessene, 1968
). In greenhouse experiments, Tessene (1968)
found that simultaneously flowering clones of L. americana never set fruit and suggested the lack of mature fruit in the field was due to genetically controlled self-incompatibility.
Littorella has a widely disjunct geographic distribution and it is ecologically significant in some habitats. Littorella uniflora (L.) Ascherson is common in northern Europe and its range extends west to include Iceland and the Azores, south to Gibraltar, and east to the Black Sea. Littorella americana Fernald, once considered one of the rarest plants in North America (Fernald, 1918
), occurs in southeastern Canada from Ontario to Newfoundland and in the northeastern United States from Wisconsin to Maine. Littorella australis Griseb. ex Bentham & Hooker grows in southern Chile and Argentina where it has been seldom collected and in the Falkland Islands where it was once considered rare but is now being increasingly recorded as the result of intensive fieldwork. The biogeographical distribution of Littorella is described as bipolar and circumboreal and is thought to have resulted from long-distance dispersal by birds in the Pleistocene or later (Raven, 1963
; Thorne, 1972
). It is an amphibious genus with the included taxa having both aquatic and terrestrial growth forms that often form large dense mats in, or on shores of ponds, lakes, and along the margins of streams. In some areas Littorella is abundant and forms an important constituent of these ecosystems. As a result, considerable research has been conducted on the physiology and ecology of Littorella uniflora (Hostrup and Wiegleb, 1991
; Christensen et al., 1994
; Nielsen and Sand-Jensen, 1997
; Robe and Griffiths, 1992
) and L. americana (Tessene, 1968
; Boston and Adams, 1986
, 1987
); however, little attention has been given to the systematics and the biogeography of the genus.
A recent phylogenetic study (Rahn, 1996
) has challenged the generic recognition of Littorella and Bougueria. In this study Rahn used 91 characters representing a broad range of morphological, embryological, and chemical data in a cladistic analysis of the family. On the basis of this analysis, Rahn maintained only Plantago at the generic rank. He recognized six subgenera within Plantago and further subdivided the three largest, subg. Plantago, subg. Cornopus (Lam. & DC) Rahn, and subg. Albicans Rahn, into 13 sections and 11 series. In the trees presented by Rahn, subg. Plantago is sister to a clade made up of the remaining five subgenera [subg. Cornopus, subg. Littorella (Bergius) Rahn, subg. Psyllium Juss., subg. Bougueria (Decne.) Rahn, and subg. Albicans]. Within the latter clade, subg. Littorella is sister to subg. Psyllium and subg. Bougueria is sister to subg. Albicans. Because Littorella and Bougueria were both deeply embedded within Plantago, Rahn treated both genera as subgenera, and he referred to the four species involved in these transfers as Plantago uniflora L. (= Littorella uniflora (L.) Aschers.), Plantago americana (Fernald) Rahn, comb. nov. (= Littorella americana Fernald), Plantago araucana Rahn, nomen novum (= Littorella australis Griseb.) and Plantago nubicola (Decne.) Rahn, comb. nov. (= Bougueria nubicola Decne.).
A recent molecular systematics treatment of Plantaginaceae based on internal transcribed spacer (ITS) and trnL-F data (Rønsted, 2002
; Rønsted et al., 2002
) placed Littorella uniflora as sister to the remaining 56 Plantago taxa in the study. Rønsted maintained the subgeneric ranking of Littorella (sensu Rahn, 1996
) stating chemical analyses in previous studies (Andrzejewska-Golec, 1999
; Rønsted et al., 2000
) could be interpreted to support the inclusion of Littorella as a subgenus in Plantago.
Rahn also speculated on the biogeographical center of origin for the subgenus Littorella. In his phylogeny, P. uniflora and P. americana (= L. uniflora and L. americana) are sister species united by two synapomorphies, female flowers in one whorl and the pedicel of the male flower longer than 4 mm (Rahn, 1996
). Rahn hypothesized that P. araucana (= L. australis) is the most primitive of the three species and suggested the subgenus Littorella originated in South America, spread to North America and subsequently to Europe by long-distance dispersal.
Historically, the taxonomic ranking of the North American taxon of Littorella has also been subject to dispute. When first collected in 1868, it was considered conspecific with the European Littorella species and thus was identified as L. uniflora (L.) Ascherson. Fernald (1918)
later noted the American collections differed from L. uniflora in overall size, and in the form of the roots, leaves, peduncles, flowers, and fruits. As a result, he formally recognized the North American taxon by publishing the name Littorella americana Fernald. However, more recent authors in North America have been dubious about Fernald's specific ranking and recognize L. americana either as conspecific with L. uniflora (L.) Ascherson (Bassett, 1973
; Kartesz, 1994
) or as L. uniflora var. americana (Fernald) Gleason (Gleason, 1952
; Voss, 1965
, 1996
; Scoggan, 1979
; Gleason and Cronquist, 1991
). Rahn (1996)
maintained all three species, under his subgenus Littorella, but he noted that they are all closely related. He also stated that his treatment attempted to use accepted names, and he was not undertaking a revision at the species level in the current study.
The present paper reexamines the status of Littorella as a segregate genus, provides new information on its affinities within the Plantaginaceae, and discusses its biogeography. The results presented here are part of an ongoing research project using DNA sequence data to study phylogenetic relationships, biogeography, and character evolution of Plantaginaceae in general. In this study, we construct a phylogeny using ITS sequence data of Littorella and selected representatives from Plantago and compare this molecular phylogeny to Rahn's phylogeny based on morphological, chemical, and embryological data.
The utility of the nuclear-encoded ribosomal (ITS) region in systematics and biogeographic studies has been demonstrated at generic and infraspecific levels for many groups of angiosperms (Baldwin, 1993
; Vargas et al., 1998
, 1999
; Albach and Chase, 2001
; Rønsted, 2002
; Rønsted et al., 2002
). The ease of obtaining, aligning, and interpreting ITS sequences and the rapid concerted evolution of the ITS gene contribute to the usefulness of this gene in phylogenetic analysis (Baldwin, 1995
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Total genomic DNA was extracted from fresh or silica-dried plant material using a standard 2% m/v hexadecyltrimethylammonium bromide (CTAB) protocol (Doyle and Doyle, 1987
). All DNA samples were purified by ultracentrifugation using a CsCl2-ethidium-bromide density gradient (1.55 g/mL). Amplification was carried out in a Perkin-Elmer (Norwalk, Connecticut, USA) model 9700 thermal cycler using 100-µL polymerase chain reaction (PCR). The protocol used 2.5 units of Taq polymerase (Promega, Madison, Wisconsin, USA), 2 µL 4% bovine serum albumin, 2.5 µmol/L MgCl2, and 100 ng of the two PCR primers. The ITS primers used for the initial PCR reaction were AB101 and AB102 (Douzery et al., 1999
). The internal primers ITS2 and 3 (White et al., 1991
) were also used for a few samples. Amplified products were purified using Promega Wizard PCR Minicolumns (Promega, Madison, Wisconsin, USA) in accordance with the manufacturer's protocols.
Cycle sequencing was carried out directly on the purified PCR product using the ABI Prism Big Dye Terminator Cycle Sequencing Ready Reaction kit (Applied Biosystems, Foster City, California, USA), with 10 ng of primer, 3 µL of sequence dilution buffer, and 2 µL of cycle sequence mix in a 20-µL reaction volume. For ITS, primers AB101 and AB102 were used for all taxa, supplemented by the internal forward and reverse primers (ITS2 and ITS3) in templates with long homopolymer A or T regions. Sequencing reactions were purified by ethanol precipitation and run on an ABI Prism 377 automated sequencer (PE Biosystems, Foster City, California, USA). Electropherograms were assembled and edited with Sequencher 3.1 software (GeneCodes, Ann Arbor, Michigan, USA). Sequences were aligned manually and using Clustal W (Thompson et al., 1995
). There were minor differences between the two methods. Manual alignment yielded the shorter trees and was used in analysis.
Phylogenetic analyses were performed using PAUP* 4.b8 (Swofford, 2001
). Starting trees were obtained using random sequence addition, searched using equally weighted maximum parsimony (Fitch, 1971
) with tree bisection-reconnection (TBR) branch swapping and MulTrees and Steepest Descent not in effect. Gaps were inserted at positions where insertions-deletions (indels) occurred and these areas were treated as missing data in the nucleotide matrix (Swofford, 2001
). Indels were scored as binary characters using PaupGap (Cox, 1997
) and appended to the sequence matrix for inclusion in the analysis.
Internal support was assessed by bootstrapping (Felsenstein, 1985
), using equally weighted characters. Bootstrap percentages (BP) for each node were computed after resamplings followed by a maximum parsimony (MP) reconstruction (bootstrap option in PAUP 4.b4, with 500 replicates of heuristic search, one random sequence addition per replicate, TBR branch swapping and maxtrees = 100).
Veronicastrum sibiricum L., Veronica hederaefolia L., Aragoa corrugatifolia Alonso, and Veronica anagallis-aquatica L. were designated as outgroups for all analyses based on the past work of Albach and Chase (2001)
, Olmstead et al. (2001)
, and Bello et al. (2002)
.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Rønsted et al. (2002)
, and Bello et al. (2002)
. Our phylogeny places Veronica and Veronicastrum in a grade at the base of Aragoa and Plantaginaceae. In contrast, previous work of Albach and Chase (2001)
shows Veroniceae forming a monophyletic clade; however, our sampling in Veroniceae is too limited to expect comparable results. In our analysis, Littorella, Plantago, and Bougueria (the three genera formerly regarded as constituting the Plantaginaceae) also from a strongly supported monophyletic group (BP = 100%). Within this clade, Littorella forms a well-supported, monophyletic group (BP = 100%) that is sister to a clade made up of Plantago and Bougueria. The Littorella clade is subdivided into two well-supported subclades, an Old World subclade (BP = 78%) consisting of four accessions of L. uniflora and a New World subclade (BP = 93%) consisting of L. australis and four accessions of L. americana. Within the New World subclade, the four North American accessions of L. americana form a well-supported group (BP = 87%) that is sister to the South American L. australis.
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. Within this clade the two taxa from Plantago sect. Micropsyllium Decne., P. elongata and P. heterophylla, form a strongly supported monophyletic group that is sister to the other representatives of subgenus Plantago (BP = 100%). Considering the remaining taxa from subgenus Plantago, P. rhodosperma to P. tasmanica, there is some indication that Plantago sect. Mesembrynia (Decne.) Rahn and Plantago sect. Oliganthos Baréoud are not monophyletic, but few of the nodes in this portion of the tree receive bootstrap support.
The second major clade, with only weak bootstrap support (BP = 61%), includes the species from P. erecta to P. nubicola. This clade consists of representatives from subgenera Albicans, Psyllium, Bougueria, and Coronopus sensu Rahn (1996)
. Within this clade, the two representatives from subg. Coronopus, P. coronopus and P. maritima, form a small clade that is sister to a larger clade made up of representatives from subgenera Psyllium, Albicans, and Bougueria (BP = 94%). This larger clade contains one representative from subg. Psyllium, P. arborescens, and a representative from the monotypic subg. Bougueria, P. nubicola, and both of these are embedded within an assemblage of taxa from subg. Albicans, rendering the latter paraphyletic. In our phylogeny, Plantago nubicola, historically regarded as the monotypic genus Bougueria or more recently treated as a subgenus of Plantago by Rahn (1996)
, is sister to P. ovata (BP = 63%), a representative of Plantago subg. Albicans sect. Albicans.
Sequence divergence
Uncorrected pairwise distances between taxa, based on the nucleotide characters, ranged from a minimum of 0 to a maximum of 17.4% (Veronicastrum sibricum–P. elongata). Within the in-group, Littorella and Plantago, sequence divergences ranged from 0% to 13.3% (L. australis–P. elongata), with a mean value of 7.99%. The average sequence divergence within Littorella was 0.89% with a minimum of 0% and a maximum of 2.14%. The highest sequence divergence between species of Littorella occurred between L. australis and L. uniflora (2.00–2.14%), the second highest was between L. australis and L. americana (1.71–2.00%), and the lowest was between L. americana and L. uniflora (1.00–1.14%). Sequence divergences between species of Plantago included within this study ranged from a minimum of 0.71% (P. elongata–P. heterophylla) to a maximum of 13.0% (P. elongata–P. nubicola), with a mean of 7.71%. A scatterplot of the number of observed substitutions vs. inferred substitutions for all of the taxa used in this study appears in Fig. 2. This plot shows almost no saturation within Littorella and Plantago. Pairwise comparisons between Littorella or Plantago and taxa from the outgroups (Aragoa, Veronica, or Veronicastrum) show only a slight amount of saturation among transitions, but the level observed appears to be too low to adversely affect phylogenetic reconstruction using maximum parsimony.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Thorne, 1972
). The broad geographic sampling of L. uniflora and L. americana shows little sequence divergence within the species (0.00–0.23% and 0.00–0.12%, respectively). This low sequence divergence may also be due to the fact that many populations of Littorella persist in a vegetative state for many years and the primary mode of reproduction within L. americana and L. australis appears to be vegetative rather than sexual reproduction. This contrasts with most Plantago species, which are often short-lived annuals propagated mainly by seed.
Taxonomic implications
Our molecular phylogeny supports either the generic or subgeneric recognition of Littorella as it is a well-supported monophyletic group that is sister to Plantago. The sister group relationship of Littorella and Plantago has also been determined by plastid DNA sequence data (Rønsted, 2002
; Rønsted et al., 2002
; Albach et al., in press) and chemical analysis (Andrzejewska-Golec, 1999
; Rønsted et al., 2000
). Rahn's study (1996)
illustrates some of the problems encountered in using morphology to infer phylogenetic relationships. Although Rahn considered seed and hair characters the most important criteria in determining the infrageneric phylogeny of Plantaginaceae, he noted that the seeds in Littorella and Bougueria are strongly specialized and are probably not suitable for this purpose. Hair morphology also is not useful in determining the phylogenetic position of Littorella within Plantaginaceae. The two types of trichomes commonly found in Littorella species, one glandular and one nonglandular, occur throughout the Plantaginaceae (Rahn, 1992
; Andrzejewska-Golec, 1998
). Rahn recognized a second type of glandular hair in Littorella that he determined to be similar to a type found in subg. Psyllium and in subg. Albicans sections Hymenopsyllium and Albicans; however, he conceded he found these only in two cases and their size and shape were often more like the common type of nonglandular hairs. In his concluding remarks, Rahn stated the phylogenetic position of Littorella remains especially uncertain because it is based on few characters. As Littorella is a monophyletic group with strong bootstrap support in our molecular analysis, has several morphological character states that distinguish it from Plantago, and has been recognized as a good genus for almost 250 yr, we conclude that Littorella should retain generic status.
In our analysis, Littorella uniflora is sister to the L. americana–L. australis clade and thus L. americana should not be considered conspecific, or afforded varietal status, with L. uniflora. To do so without altering the taxonomic status of L. australis would render L. uniflora paraphyletic. One might argue that, due to the morphological similarities of the three species, the genus should be considered monotypic represented by L. uniflora; however, there are morphological differences that clearly distinguish L. australis from L. americana and L. uniflora. The alternative, an infraspecific ranking, would only lead to more synonyms in the botanical literature and, since these taxa are terminal, no phylogenetic insight would be gained. Accordingly we support the continued recognition of three distinct species of Littorella.
Our molecular phylogeny supports the recent inclusion of Bougueria within Plantago (Rahn, 1996
), though not at the subgeneric level. A recent plastid phylogeny (Rønsted, 2002
; Rønsted et al., 2002
) placed Bougueria within Plantago and sister to subg. Psyllium, thus supporting Rahn's subgeneric recognition. In our phylogeny, the association of P. nubicola and P. ovata is enigmatic as morphologically they are markedly dissimilar. The flowers, capsules, and seeds of P. nubicola are quite different from those of all other species of Plantago or Littorella and, consequently, affinities are difficult to define based on morphology. Rahn (1996)
noted that Bougueria and Plantago subgenus Albicans both have very narrow, multicellular hairs with a short basal cell, and he suggested affinities between the two taxa on this basis. However, from a biogeographical perspective, the association of P. nubicola with P. ovata is difficult to explain as the former is endemic to the Andes of central South America and the latter is native to the Mediterranean area also occurring in western North America as a recent introduction. At present, the origin and evolution of P. nubicola defy explanation and merit further research.
Biogeography
The sister group to Plantaginaceae, Aragoa, is a woody perennial occurring in the Colombian páramo region, a high altitude habitat that occurs in elevations of 3000–5400 m. In comparing Littorella and Aragoa taxa, no indication of the origin of Littorella is given because of striking differences in morphology, habitat requirements, and current geographical locations.
Our molecular phylogeny shows Littorella could not have originated in southern South America and spread to Europe via North America as hypothesized by Rahn (1996)
though it does not eliminate the possibility that Littorella originated in the Southern Hemisphere and spread independently to North America and Europe. It is also possible that Littorella originated in North America and dispersed independently to South America and Europe. However, there are factors that suggest a European origin for the genus is more likely: (1) Location of most successful area—Littorella uniflora is widespread throughout Europe including Iceland and the Azores, while populations of L. americana and L. australis are relatively few in northeastern North America and the Patagonia region of South America, respectively, despite the abundance of suitable habitats. (2) Area with greatest opportunities for dispersal—Littorella uniflora flowers freely, and seed production is common, while flowering and seed production in L. americana and L. australis are rare, offering few opportunities for dispersal. (3) Location of least dependence on a restricted habitat—Littorella uniflora is a generalist occupying a wide variety of climatic zones ranging from arctic to Mediterranean, while L. americana and L. australis are restricted to few climatic zones. (4) ITS sequence divergence—Pairwise distance analysis shows divergence averages of L. uniflora and L. australis are closer to L. americana (1.17 and 1.24%, respectively) than to each other (1.98%), suggesting a direct association of L. uniflora with L. australis is unlikely. Our molecular phylogeny and these four reasons, while independently inadequate, collectively support Europe as the center of origin of Littorella with its path of dispersion being to South America via North America.
It is unlikely that the disjunction of Littorella in the Northern Hemisphere is the result of vicariance. The current eastern range limit of Littorella in the Old World is the Black Sea with no record of the genus having occurred in Asia; thus, a hypothesis of L. americana being a relict of an ancient distribution that extended across Asia and into North America via Beringia is not supported. A recently proposed molecular clock (Rønsted, 2002
) that places the divergence of Aragoa and Plantago at 7.1 million years ago (mya) and the low sequence divergence among Littorella species in our analyses make a vicariance hypothesis involving the de Geer land bridge across the North Atlantic unlikely as this would indicate the North American and European Littorella taxa have been separated at least 25 mya. It is also doubtful the occurrence of Littorella in South America is the result of vicariance as no collections of Littorella have ever been made from the entire area between those proximal to the Canadian/United States border and collections in Patagonia and the Falkland Islands (Rahn, 1996
). Our study concurs with Raven's (1963)
listing of Littorella as having bipolar and circumboreal distribution resulting from long-distance dispersal in the Pleistocene or later.
Conclusions
Despite the intensive study of L. uniflora by European researchers, little is known about Littorella as it occurs in the New World. Once considered rare species, new collections of both L. americana and L. australis are being reported, suggesting a more widespread distribution than previously thought. No doubt, a collection bias exists in that these species mostly occur submerged and are seldom observed emersed and flowering. Also, the lack of competent field botanists in the less populated areas of Patagonia and the Falkland Islands add to the underreporting of Littorella in these regions. Future ecological studies of L. americana and L. australis could yield important insights into the genetic structure of clonal plant populations where sexual recruitment is rare or absent. Our preliminary phylogeny of Plantago indicates that more sampling will be needed before a revised infrageneric classification for the genus can be proposed, and these studies are currently in progress.
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FOOTNOTES |
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4 Author for reprint requests (rghoggard{at}earthlink.net
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Albach D. C. M. M. Martinez-Ortega M. W. Chase In press Veronica: parallel morphological evolution and phylogeography in the Mediterranean. Plant Systematics and Evolution.
Andrzejewska-Golec E. 1998 Microhairs of Littorella uniflora (L.) Asch. (Plantaginaceae). Feddes Repertorium 109: (7–8) 521-526
Andrzejewska-Golec E. 1999 Iridoid glucosides in Littorella uniflora (L.) Ascherson. Acta Societatis Botanicorum Poloniae 68: 267-268[ISI]
Ascherson P. 1864 Fl. Brandenberg 544
Baldwin B. G. 1993 Molecular phylogenetics of Calycadenia (Compositae) based on ITS sequences of nuclear ribosomal DNA: chromosomal and morphological evolution reexamined. American Journal of Botany 80: 222-238[CrossRef][ISI]
Baldwin B. G. 1995 The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden 82: 247-277[CrossRef][ISI]
Bassett I. J. 1973 The plantains of Canada. Canadian Department of Agriculture, Ottawa, Ontario, Canada
Bello M. A. M. W. Chase R. G. Olmstead N. Rønsted D. Albach 2002 The páramo endemic Aragoa is the sister genus of Plantago (Plantaginaceae, Lamiales): evidence from plastid rbcL and nuclear ribosomal ITS sequence data. Kew Bulletin 57: 585-597[CrossRef]
Bentham G. J. D. Hooker 1876 Genera plantarum, vol. II. Lowell Reeve, London, UK
Bergius P. J. 1768 Vetenskap Academiens Handlingar Stockholm xxix: 841.
Boston H. L. M. S. Adams 1986 The contribution of crassulacean acid metabolism to the annual productivity of two aquatic vascular plants. Oecologia 68: 615-622[CrossRef][ISI]
Boston H. L. M. S. Adams 1987 Productivity, growth and photosynthesis of two small "Isoetid" plants, Littorella uniflora and Isoetes macrospora. Journal of Ecology 75: 333-350[CrossRef]
Christensen P. B. N. P. Revsbech K. Sand-Jensen 1994 Microsensor analysis of oxygen in the rhizosphere of the aquatic macrophyte Littorella uniflora (L.) Ascherson. Plant Physiology 105: 847-852[Abstract]
Cox A. V. 1997 PaupGap version 1.0. Computer program available from author, Jodrell Laboratory, Royal Botanic Gardens Kew, London, UK
Correa M. N. 1999 Flora Patagonica. Coleccion Cientifica del Inta, Buenos Aires, Argentina
Douzery E. J. P. A. M. Pridgeon P. Kores H. P. Linder H. Kurzweil M. W. Chase 1999 Molecular phylogenetics of Diseae (Orchidaceae): a contribution from nuclear ribosomal ITS sequences. American Journal of Botany 86: 887-899
Doyle J. J. J. L. Doyle 1987 A rapid DNA procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11-15
Felsenstein J. 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791[CrossRef][ISI]
Fernald M. L. 1918 The North American Littorella. Rhodora 20: 232-233
Fitch W. M. 1971 Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 20: 406-416[CrossRef][ISI]
Gleason H. A. 1952 Illustrated flora of the northeast United States and adjacent Canada. Hafner, New York, New York, USA
Gleason H. A. A. Cronquist 1991 Manual of vascular plants of northeastern United States and adjacent Canada. New York Botanical Garden, Bronx, New York, USA
Hostrup O. G. Wiegleb 1991 Anatomy of leaves of submerged and emergent forms of Littorella uniflora (L.) Ascherson. Aquatic Botany 39: 195-209[CrossRef]
Judd W. S. C. S. Campbell E. A. Kellogg P. F. Stevens 1999 Plant systematics: a phylogenetic approach. Sinauer, Sunderland, Massachusetts, USA
Kartesz J. T. 1994 A synonymized checklist of the vascular flora of the United States, Canada, and Greenland. Timber Press, Portland, Oregon, USA
Linnaeus C. 1753 Species Plantarum, Holmiae
Moore D. M. 1983 Flora of Tierra del Fuego. Missouri Botanical Garden, St. Louis, Missouri, USA
Nielsen S. L. K. Sand-Jensen 1997 Growth rates and morphological adaptations of aquatic and terrestrial form of amphibious Littorella uniflora (L.) Aschers. Plant Ecology 129: 135-140[CrossRef][ISI]
Olmstead R. G. C. W. dePamphilis A. D. Wolfe N. D. Young W. J. Elisons P. A. Reeves 2001 Disintegration of the Scrophulariaceae. American Journal of Botany 88: 348-361
Pilger R. 1937 Plantaginaceae. Das Pflanzenreich. Wilhelm Englemann, Leipzig, Germany
Rahn K. 1992 Trichomes within the Plantaginaceae. Nordic Journal of Botany 12: 3-12
Rahn K. 1996 A phylogenetic study of the Plantaginaceae. Botanical Journal of the Linnean Society 120: 145-198[CrossRef]
Raven P. H. 1963 Amphitropical relationships in the floras of North and South America. Quarterly Review of Biology 38: 151-177[CrossRef][ISI]
Robe W. E. H. Griffiths 1992 Seasonal variation in the ecophysiology of Littorella uniflora (L.) Ascherson in acidic and eutrophic habitats. New Phytologist 120: 289-304
Robe W. E. H. Griffiths 1998 Adaptations for an amphibious life: changes in leaf morphology, growth rate, carbon and nitrogen investment, and reproduction during adjustment to emersion by the freshwater macrophyte Littorella uniflora. New Phytologist 140: 9-23[CrossRef][ISI]
Rønsted N. 2002 Towards a natural classification of Plantago. Royal Danish School of Pharmacy, Copenhagen, Denmark
Rønsted N. M. W. Chase C. D. Albach A. Bello 2002 Phylogenetic relationships within Plantago (Plantaginaceae): evidence from nuclear ribosomal ITS and plastid trnL-F sequence data. Botanical Journal of the Linnean Society 139(4): 323-338[CrossRef]
Rønsted N. E. Gobel H. Franzyk S. R. Jensen C. E. Olsen 2000 Chemotaxonomy of Plantago, iridoid glucosides and caffeoyl phenylethanoid glycosides. Phytochemistry 55: 337-348[CrossRef][ISI][Medline]
Rosatti T. J. 1984 The Plantaginaceae in the southeastern United States. Journal of the Arnold Arboretum 65: 533-562[ISI]
Scoggan H. J. 1979 Flora of Canada. National Museum of Natural Sciences, National Museums of Canada, Ottawa, Ontario, Canada
Swofford D. L. 2001 PAUP: phylogenetic analysis using parsimony, vers. 4.b8. Sinauer, Sunderland, Massachusetts, USA
Tessene M. F. 1968 Preliminary reports on the flora of Wisconsin no. 59: Plantaginaceae—plantain family. Transcripts of the Wisconsin Academy of Science, Arts and Letters 56: 281-313
Thompson J. D. D. G. Higgins T. J. Gibson 1995 Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position, specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673-4680[CrossRef][ISI]
Thorne R. F. 1972 Major disjunctions in the geographic ranges of seed plants. Quarterly Review of Biology 47: 365-411[CrossRef]
Vargas P. B. G. Baldwin L. Constance 1998 Nuclear ribosomal DNA evidence for a western North American origin of Hawaiian and South American species of Sanicula (Apiaceae). Proceedings of the National Academy of Sciences, USA 95: 235-240
Vargas P. C. M. Morton S. L. Jury 1999 Biogeographic patterns in Mediterranean and Macaronesian species of Saxifraga (Saxifragaceae) inferred from phylogenetic analyses of ITS sequences. American Journal of Botany 86: 724-734
Voss E. G. 1965 Some rare and interesting aquatic vascular plants of northern Michigan, with special reference to Cushion Lake (Schoolcraft Co). Michigan Botanist 4: 11-25
Voss E. G. 1996 Michigan flora. Cranbrook Institute of Science Bulletin 61 and University of Michigan Herbarium, Ann Arbor, Michigan, USA
White T. L. T. Bruns S. Lee J. Taylor 1991 Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White [eds.], PCR protocols, 315–322. Academic Press, San Diego, California, USA
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