| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Botany, Duke University, Durham, North Carolina 27708-0338 USA
Received for publication April 6, 2000. Accepted for publication June 20, 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
1000 species distributed pantropically, the genus Piper is one of the most diverse lineages among basal angiosperms. To rigorously address the evolution of Piper we use a phylogenetic analysis of sequences of the internal transcribed spacers (ITS) of nuclear ribosomal DNA based on a worldwide sample. Sequences from a total of 51 species of Piper were aligned to yield 257 phylogenetically informative sites. A single unrooted parsimony network suggested that taxa representing major geographic areas could potentially form three monophyletic groups: Asia, the South Pacific, and the Neotropics. The position of Pothomorphe was well supported among groups of New World taxa. Simultaneous phylogenetic analysis of an expanded alignment including outgroups suggested that taxa from the South Pacific and Asia formed a monophyletic group, provisionally supporting a single origin of dioecy. Within the Neotropical sister clade, resolution was high and strong bootstrap support confirmed the monophyly of several traditionally recognized infrageneric groups (e.g., Enckea [including Arctottonia], Ottonia, Radula, Macrostachys). In contrast, some of the species representing the highly polytypic subgroup Steffensia formed a clade corresponding to the previously recognized taxon Schilleria, while others were strongly associated with several of the more specialized groups of taxa. The distribution of putatively derived inflorescence and floral character states suggested that both umbellate and solitary axillary inflorescences have multiple origins. Reduction in anther number appears to be associated with highly packaged inflorescences or with larger anther primordia per flower, trends that are consistent with the suppression of later stages of androecial development.
Key Words: flower evolution • inflorescence evolution • ITS sequences • Piper • Piperaceae
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Soltis, Soltis, and Chase, 1999
). One view on the phylogenetic position of Piperaceae is among a diverse assemblage of dicots termed "paleoherbs" (Donoghue and Doyle, 1989
; Loconte and Stevenson, 1991
), plants that resemble monocots in certain vegetative features (e.g., adaxial prophyll, scattered vascular bundles). More recently, the Piperaceae and related families (e.g., Aristolochiaceae, Saururaceae, Lactoridaceae) have been shown to form the sister group to Winterales (Soltis, Soltis, and Chase, 1999
; Qiu et al., 1999
). The high species diversity within Piper is unique among the traditional Magnoliidae, providing a noteworthy example of an increase in diversification rate at the base of the angiosperms (see Sanderson and Donoghue, 1994
).
Piper species are distributed pantropically (Fig. 1) and take the form of shrubs, herbs, and lianas common in the understory of lowland wet forests. The greatest diversity of Piper species occurs in the American tropics (700 spp.), followed by Southern Asia (300 spp.), where the economically important species Piper nigrum L. (black pepper) and P. betle L. (betel leaf) originated. Patterns of distribution of Piper species vary from being locally endemic to widespread. There are several species restricted to a specific center of diversity (e.g., Andes, Central America) and others occur throughout the Neotropics or the Paleotropics. Piper is often a dominant element in the understory of tropical forests and found to be one of the five most speciose genera in select Neotropical forests (Gentry, 1990
). Not surprisingly, Piper species are of great ecological importance and have been considered "key" species on the basis of their association with frugivorous bats (Fleming, 1981, 1985
; Bizerril and Raw, 1998
).
|
; Miquel, 1843–1844
), within the current circumscription of the genus. Five of these taxa continue to be accepted today: Piper, Pothomorphe, Macropiper, Ottonia, and Zippelia (see Tebbs, 1993a
). The most recent revision (DeCandolle, 1923
) recognized most of the same groupings, but at the sectional level. These first monographs of Piper were based primarily on stamen number and position, carpel number, floral bract morphology, inflorescence position, and leaf venation. After these treatments three additional genera, Arctottonia (Trelease, 1930
), Sarcorhachis (Trelease, 1927
), and Trianaeopiper (Trelease, 1928
), were recognized from the Neotropics, and Penninervia was recognized from the Philippines at the sectional level (Quisumbing, 1930
). More recent taxonomic studies have abandoned DeCandolle's system citing the difficulty of evaluating floral characters from herbarium specimens (Trelease and Yuncker, 1950
; Burger, 1971
). For example, Yuncker (1973)
recognized fewer segregates using inflorescence position, a character he considered to be more conservative in its variation. As a result, the infrageneric taxonomy of Piper is unsettled, and most local treatments have described species without reference to subgeneric affiliation (Yuncker, 1953, 1972, 1973
; Backer and Bakhuizen van der Brink, 1963
; Burger, 1971
; Steyermark, 1984
; Chew, 1972
; Howard, 1973
; Liu and Wang, 1975
; Long, 1984
; Green, 1994
; Verdcourt, 1996
; Yongqian, Nianhe, and Gilbert, 1999
).
|
; Callejas, 1986
; Lei and Liang, 1998
) have shown that the androecium develops bilaterally with stamens initiated in pairs or individuals (see Fig. 2). Stamen initiation begins with a lateral pair followed by a single median anterior and then a single median posterior (where they occur), whereas in species with six stamens, the final pair is initiated in an anterior–lateral position. Three or four carpels are initiated simultaneously from a gynoecial ring (Tucker, 1982
; Lei and Liang, 1998
).
|
). Pollen-collecting bees have been observed visiting the inflorescences of certain Piper species (Semple, 1974
; Marquis, 1988
; Bornstein, 1989
), and the tightly congested arrangement may be advantageous since the bees can collect pollen from a virtually seamless inflorescence surface. Inflorescence type in Piper varies in position (axillary or terminal), length (from 2–3 cm to 150 cm long), presentation (erect or pendulous), color (cream to red), and number of spikes (single or umbellate; see Fig. 2). Given the minute size of Piper flowers, changes in floral structure may be evolutionarily less important than variation in inflorescence type. It is likely that pollination and dispersal biology have been influenced more by whole inflorescence structure rather than individual flower structure (Thies, Kalko, and Schnitzler, 1998
).
The only previous cladistic analysis of Piper used morphological characters to suggest two major clades dividing Paleotropical and Neotropical taxa into 25 subgenera with little resolution among them (Callejas, 1986
). More recently a broader morphological cladistic study of the Piperales including segregates of Piper found support for two clades within Piperaceae: Piper + Peperomia and Pothomorphe + Macropiper (Tucker, Douglas, and Liang, 1993
). Under this interpretation, part of Piper is more closely related to Peperomia than to other groups traditionally recognized within the genus. The primary goal of this study is to develop a phylogenetic hypothesis for Piper based on a broad sampling from throughout its distribution using nucleotide data from the internal transcribed spacer (ITS) of the nuclear ribosomal DNA. The ITS region has been widely used for species level phylogenetic analysis (Baldwin, 1993
; Sang et al., 1994
; Baldwin et al., 1995
; Kron and King, 1996
; Manos, 1997
) and preliminary data indicate resolution within Piper is possible (Jaramillo and Manos, 1998
). The specific objectives were to: (1) identify major clades within Piper, (2) reexamine previous classifications and the characters used to delimit traditionally recognized taxa, (3) test the traditional taxonomic dichotomy between geographic regions within Piper, and (4) examine the role of floral and inflorescence structure in the diversification of Piper.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
to consider all segregates of Piper as infrageneric groups (Table 1). At least four species were sampled from nonmonotypic groups. For widely distributed species, 2–3 plants were sampled from widespread localities to test for intraspecific variation. Plant material was collected from naturally occurring populations, although a few species were cultivated in botanical gardens. A list of species sampled, along with collection localities, vouchers, and accession numbers is provided in Table 2. For members of segregate genera that do not have a valid synonym within Piper, the most current classification was used (e.g., Macropiper, Smith, 1975
). For every species included, floral and inflorescence structure was documented using field-collected material, and the consistency of trait expression was verified in monographic treatments and herbarium collections.
|
; Qiu et al., 1999
; Soltis, Soltis, and Chase, 1999
) and macrosystematic taxonomic treatments (Cronquist, 1981
; Takhtajan, 1997
). The broader relationships within Piperaceae are not well established and are currently the subject of DNA sequence-based investigations (Jaramillo, unpublished data).
Total DNA was extracted from fresh or silica gel-dried leaves using the 2x CTAB (hexadecyl trimethyl ammonium bromide) method of Doyle and Doyle (1987)
, or Dneasy Plant Mini kit (Qiagen Corporation, Valencia, California, USA). Amplification of the complete ITS region was done using one of two pairs of primers ITS5-LS4R or LEU1-ITS4 (Baldwin, 1992
; LEU1, Baldwin, 1993
). For all taxa the following sequencing primers were used: ITS5, ITS4, ITS3, and ITS2 (Baldwin, 1992
). Sequencing reactions were prepared using the ABI Prism Dye Terminator Cycle Sequencing Reaction Kit, according to the protocols provided by the manufacturer. Double-stranded products were sequenced in all cases. Resulting sequences were assembled using Sequencher (Gene Codes Corporation, Ann Arbor, Michigan, USA) and deposited in GenBank (see Table 2 for accession numbers).
Sequence analysis
Sequences were aligned using CLUSTALX (Thompson et al., 1997
) and modified by visual inspection. Two different alignments were used: Data Set 1 included only Piper species and Data Set 2 included Piper species and the five outgroups. Because outgroup sequences were very divergent from ingroup sequences, it was necessary to introduce additional gaps to the alignment of Data Set 1. In particular, three sections of the alignment were ambiguous between Piper species and outgroups. Given that these regions included several informative sites within Piper, the ambiguously aligned bases that roughly correspond to these sites in outgroup sequences were scored as missing. Phylogenetic analyses were performed with PAUP* (Swofford, 1998
) using the maximum parsimony algorithm with gaps treated as missing data. Parsimony analyses were performed using heuristic searches with 100 random addition replicates, TBR branch swapping, MULPARS, steepest descent, and Goloboff fitness (k = 2; Goloboff, 1997
). Branches with a minimum length of zero were collapsed using the "amb-" option (Nixon and Carpenter, 1996
). Clade support was examined using 500 bootstrap replicates (Felsenstein, 1985
) and a complete heuristic search. Sequence distance matrices also were calculated using PAUP*.
Because it is well known that moderate to high levels of sequence divergence between ingroup and outgroup could potentially lead to spurious rooting of the ingroup topology (e.g., Wheeler, 1990
), the following options outlined by Nixon and Carpenter (1996)
were used: (1) examine unrooted trees derived from analysis of Data Set 1; (2) use Lundberg rooting (Lundberg, 1972
), which derives a root for the unrooted tree by parsimoniously attaching outgroup states, read as ancestral states, to a particular network; and (3) examine the rooted trees derived from analysis of Data Set 2 using various combinations of potential outgroups. For Lundberg rooting, three outgroup taxa were used (Peperomia, Sarcorhachis, and Saururus) to define ancestral states.
To explore flower and inflorescence evolution, select character states were mapped onto a simplified phylogeny using MacClade (Maddison and Maddison, 1992
). The phylogeny conserved the topology obtained in the final analysis and included taxa representing both unique and broadly representative combinations of character states.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
The alignment of Data Set 2 included all outgroup taxa and 773 nucleotide sites. A total of 332 (42.9%) informative sites were included in the phylogenetic analysis. Sequence divergence among the Piper species ranged from 3.8% for sister species P. munchanum and P. augustum to 29.5% between Paleotropical and Neotropical species P. bavinum–P. ubatubensis to >40% for outgroup–ingroup comparisons (Peperomia elongata vs. P. amoenum).
Phylogenetic analysis
Parsimony analysis of Data Set 1 recovered one most parsimonious tree of 837 steps. The unrooted tree does not support the paraphyly of taxa representing major geographical areas, thus as depicted these groups correspond to three potentially monophyletic clades: Asia, the South Pacific, and the Neotropics (Fig. 3). Within these clades several well-supported subclades were found to correspond with traditional subgeneric groupings: Enckea (including Arctottonia), Ottonia, Radula, Pothomorphe (including P. auritum), Macrostachys, Schilleria, Macropiper, and Penninervia. Other taxa representing subgenera Trianaeopiper and Steffensia are shown to be polyphyletic. The ITS data provided strong bootstrap support (>85%) for the following clades: Asian, South Pacific, Neotropical, Schilleria, Pothomorphe, Macrostachys, Radula, Macrostachys-Radula, Ottonia, Enckea, Ottonia-Enckea, and Penninervia. Within the Neotropical clade, species belonging to the broadly delimited subgenus Steffensia were found to be intermixed with taxa corresponding to various subgenera of Piper. Species of the less speciose and more narrowly defined subgenus Trianaeopiper also are widely placed. In the South Pacific clade, species of the subgenus Macropiper formed a monophyletic subclade sister to the cultivated P. methysticum (kava-kava).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
, we found support for a broad concept of Piper, including the placement of Pothomorphe among traditionally recognized groups of Neotropical taxa. Our data independently support the morphological analysis of Callejas (1986)
emphasizing the sharp distinction in floral biology where Asian and South Pacific taxa are dioecious, while all Neotropical taxa are bisexual. Given the difficulty in confidently resolving the relationships among the three major clades, it is unclear whether dioecy is a synapomorphy for Asian and South Pacific Piper. Our findings also demonstrate that the few pantropically distributed species of Piper represent recent introductions. This is clear from the strong association of samples of P. umbellatum and P. aduncum from the Philippines with their conspecifics from the Neotropics. With respect to the pantropical distribution of the genus, phylogenetic evidence suggests a continuous ancestral presence of Piper on the land areas of the Southern Hemisphere, a result consistent with vicariance rather than dispersal.
One of the most controversial taxonomic issues within Piper has been the appropriate rank at which to recognize infrageneric groups and closely related genera such as Macropiper and Sarcorhachis (Miquel, 1843–1844
; DeCandolle, 1923
; Trelease and Yuncker, 1950
). Initial attempts to align ITS sequences among all potentially related taxa revealed patterns of sequence divergence that may serve as a preliminary guide in determining the phylogenetic limits of Piper. Using the criterion of alignability, segregate genera such as Sarcorhachis and Zippelia appear to be distantly related to Piper, whereas Macropiper is more likely to represent a segregate within an expanded concept of the genus. Further support for an expanded phylogenetic circumscription of Piper will require a broad phylogenetic survey of Piperales using placeholders from the three groups resolved here (Jaramillo, unpublished data). Nevertheless, provisional recognition of the three major groups as subgenera within Piper establishes a working framework to recognize additional subclades at the sectional level.
Neotropical clade
Our results resolve two major clades and six well-supported subclades that correspond to many of the traditionally recognized subgenera within Neotropical Piper. The Enckea subclade was found to include species of the subgenus Arctottonia (the pedicellate Piper species of Mexico; Bornstein, 1989
). Prior to the description of Arctottonia at the genus level by Trelease (1930)
, species of this group were included either in Enckea or Ottonia. Arctottonia species were included in Enckea (Kunth, 1839)
on the basis of reproductive characters, such as number of stamens and carpels and floral bract morphology, and in Ottonia (Presl, 1849)
because pedicellate flowers occur in species of both groups. Enckea species are shrubs distinguished by palmately veined leaves, inflorescences with widely spaced bisexual flowers bearing four stamens and three carpels, each subtended by a cucullate bract. Molecular evidence confirms that Arctottonia is more closely related to Enckea than to Ottonia, in agreement with vegetative morphology (e.g., leaf venation and growth habit) and geographic distribution. Enckea and Arctottonia species are found primarly in Central America, while Ottonia species occur mainly in the Atlantic Forest of Brazil (Trelease, 1930
; Callejas, 1986
; Bornstein, 1989
). Thus, traditional definitions of Arctottonia and Enckea should be reconsidered.
Ottonia species are defined by pinnately veined leaves and lax inflorescences with bisexual flowers bearing four stamens and four carpels, each subtended by a cucullate bract. Although the flowers of many Ottonia species are pedicellate, in a considerable number of species flowers are sessile. An interesting result is the close relationship of Enckea and Ottonia. While Trelease (1930)
had noted that Arctottonia was closer to Enckea, he considered Ottonia to have more in common with the generalized morphology of Steffensia species. Kunth (1839)
, however, suggested that the only difference between Ottonia and Enckea (as defined in his treatment) was the type of leaf venation. Our results suggest that Trelease's (1930)
reliance on leaf venation differences among Neotropical Piper, and in this particular example where Enckea has palmate veins while Ottonia is pinnate, highlights one source of systematic bias. As noted by Kunth (1839)
, Enckea and Ottonia present the same floral morphology: flowers with generally four stamens, three to four carpels, subtending cucullate bracts, and a lax inflorescence.
Although both of these clades include taxa with pedicellate flowers, it is premature to suggest the condition defines the clade. In Ottonia, the pedicels are formed by zonal growth below the gynoecium (Callejas, 1986
), whereas pedicel formation in Enckea is unstudied. Further studies of the development of pedicellate flowers could clarify whether the loss of pedicels in these taxa is derived. The evolution of pedicellate flowers may have been facilitated by the lax flower arrangement within the inflorescence. Potential advantages of pedicellate flowers cannot be assessed since little is known about the pollination or dispersal ecology of these species. The few studies that have observed pollination in species of subgenus Ottonia indicated that they are visited by generalist pollinators (e.g., flies, bees, and butterflies; De Figuereido and Sazima, 2000
), while only bees were observed visiting the inflorescences of Arctottonia (Bornstein, 1989
).
Species forming the Radula clade represent some of the most commonly encountered of all Neotropical Piper. Most species of Radula are shrubby and possess a generalized set of features including thin, elliptic, membranaceous leaves with unequal bases, and straight or curved inflorescences with tightly congested flowers (but see Tebbs, 1993b
). Radula were described originally as a section of Steffensia (= Artanthe; Miquel, 1843–1844
) and typically occurs in open areas or disturbed habitats. Their widespread presence throughout the Neotropics may be attributed to dispersal by bats along roadsides. The sister group to Radula is Macrostachys, a small group of species generally characterized as treelets with large, lobulate leaves, and long pendulous inflorescences bearing tightly congested flowers (but see Tebbs, 1989
). These two clades share tightly congested inflorescences, a character found only in Neotropical species of Piper and probably related to pollination by pollen-collecting bees (Burger, 1971
).
The Pothomorphe clade includes P. auritum (subg. Steffensia) in addition to the two species traditionally considered within this group (e.g., P. umbellatum and P. peltatum). The traditional concept of Pothomorphe recognized the presence of umbellate axillary inflorescences as a defining feature. Many authors have also noted that the inflorescence of Pothomorphe is a truncated axillary branch with reduced internodes and terminal inflorescences (Burger, 1971
; Callejas, 1986
; Tebbs, 1993b
). Pothomorphe species are shrubs, with palmately veined leaves borne on vaginated petioles. The flowers are tightly congested in the inflorescence, each bearing two stamens (four stamens in P. auritum) and three carpels that are subtended by marginally ciliate hypopeltate bracts. Curiously, species of Pothomorphe also occur in Asia and Africa. Their presence in the Old World reflects recent introductions, most likely by humans who used the plants in traditional medicines (Ehringhaus, 1997
).
The results of this study do not support the monophyly of all Steffensia sampled. Most species of Steffensia do form a clade, but several others are associated with either Pothomorphe or the Macrostachys + Radula clade (Fig. 3). Steffensia is the largest group within Piper (300 spp.), and its defining features, such as the shrubby habit, plinerved to pinnately nerved leaves, and flowers with four to five stamens and three carpels, appear to represent many of the plesiomorphic states within the genus. Miquel (1843–1844
) described ten sections within Steffensia based mainly on vegetative characters. The species of Steffensia that form one of the clades resolved here have lax inflorescences and correspond to species recognized within the genus Schilleria (Kunth, 1839)
. Increased sampling is needed across Miquel's sections emphasizing the diversity in the Atlantic Forest of Brazil, Amazonia, and the Caribbean.
The genus Trianaeopiper, endemic to the Chocó Region of northwestern South America and described by Trelease (1928)
for specimens with a single axillary inflorescence, appears to be polyphyletic (Fig. 3). Comparative studies of the inflorescence structure in these species suggest differences in shape and orientation, despite apparent similarities in position, as well as variation in the packaging of flowers (Jaramillo and Callejas, unpublished data). There may be multiple origins of axillary inflorescences among the diverse lineages present in the extremely wet forests of the Chocó.
South Pacific Islands clade
This small group includes three species of the traditionally recognized genus Macropiper, plus Piper methysticum, the source of kava-kava. Macropiper are differentiated from the other species of Piper in having axillary umbellate inflorescences, similar to those in Pothomorphe, but with unisexual flowers. Recent reviews of the taxonomy and morphology of Macropiper disagree on the interpretation of the inflorescence. Smith (1975)
suggested that the inflorescence is truly axillary, whereas Gardner (1997)
argued that it originated through reduction of axillary branches.
Recent studies of P. methysticum suggest a distant relationship to Macropiper on the basis of its terminal inflorescence and presence of kavalactones (Lebot and Lévesque, 1989
). Our study suggests P. methysticum is related to Macropiper rather than to other Asian species of Piper. To elucidate the phylogenetic relationships of South Pacific Piper and clarify the origin of the unique inforescence type in Macropiper, greater sampling is needed within the 40 species of South Pacific Piper.
The Asian clade
We included mainly samples from the larger groups of Asian Piper and resolved four well-supported subclades, but it is difficult to assign them to any traditionally recognized groupings. Taxonomic treatments of Piper in Asia have included from one to two broadly defined subgenera plus a few small segregates. On the basis of floral bract morphology, Miquel (1843–1844)
defined two major groups within the Asian species, Chavica (with hypopeltate bracts) and Piper (with oblong bracts adnate to the rachis). DeCandolle (1923)
grouped all of these species regardless of bract morphology into section Piper. The results from this study suggest that bract type is not a good diagnostic character since the phylogenetic reconstruction shows that species with adnate bracts (e.g., P. nigrum and P. korthalsii; see Fig. 3) are found in both major clades of Asian Piper. The two species of section Penninervia sampled (P. celtidiforme and P. penninerve) form a well-supported clade. These species are climbers, with pinnately nerved leaves and highly enlarged anther connectives. Although there are other Asian species of Piper with pinnately veined leaves, they are mostly shrubs and probably distantly related to Penninervia. Piper korthalsii, the only member of subgenus Sarcostemon, which is distinguished by having only one stamen, formed the sister species to P. urdanetanum, a species with three stamens. There are only two species of Piper with a single stamen: P. korthalsii and the Neotropical P. kegelii ("subgenus" Nematanthera). Assuming that the Neotropical–Asian split holds throughout the genus, two origins of this derived state are likely within Piper.
Floral and inflorescence evolution
Our developing phylogenetic hypothesis of Piper has confirmed the monophyly of several traditionally recognized groups (e.g., Ottonia, Macrostachys, Macropiper), while indicating that other groups, such as Steffensia and Trianaeopiper are polyphyletic. Interestingly, taxa traditionally placed within Steffensia, the most generalized group of Piper with respect to flower morphology, form the most basal lineages in each major clade of Neotropical taxa. In the context of phylogeny, patterns of floral and inflorescence evolution appear to generally support the derived status of several of the traditionally recognized groups, in addition to suggesting multiple origins for certain specialized character states (Fig. 4). For example, the evolution of dioecy may define Old World Piper, but we note that the unsampled African species of Piper may be monoecious or dioecious, thus potentially complicating the otherwise clean distinction between Old and New World taxa. A polyphyletic origin of Africa Piper could be used to argue for long-distance dispersal, while a shared history with Neotropical taxa would suggest an independent origin of dioecy.
|
17 species described in Trianaeopiper; however, this trait also appears to have multiple origins (Fig. 4). The precise nature of axillary inflorescences in Piper remains poorly understood. Morphological studies have shown that the axillary inflorescences in Macropiper and Pothomorphe represent axillary branches with reduced internodes (Burger, 1971
; Gardner, 1997
). Callejas (personal communication) also suggested that the inflorescences in Trianaeopiper are derived from reduced axillary branches.
There are several lines of evidence suggesting that the tight packaging of floral primordia in developing inflorescences may be associated with reduction in stamen number. Tucker (1982)
suggested that this general trend is probably a result of spatial constraints leading to the suppression of later developmental sequences. Stamens in Piper are initiated successively by pairs or individuals (Fig. 2), thus flowers with fewer stamens have lost pairs or single anthers that develop later in species with higher numbers. Outgroups to Piper are consistent in their expression of loosely packaged flowers with higher numbers of stamens. In Neotropical Piper, tightly congested inflorescences have evolved numerous times and a general reduction to four stamens is apparent for most taxa, except for Pothomorphe in which only the lateral pair develop (see Figs. 2 and 4). Although the unisexual flowers of Asian species have one to three stamens, their inflorescences bear loosely arranged flowers. In this case reduction of stamen number may be related to spatial constraints associated with larger stamen primordia. The larger stamens found in the Neotropical taxa Trianaeopiper bullatum and P. filistilum also may explain why their loosely arranged flowers possess only three stamens (see Fig. 4).
The tendency of having tightly packaged flowers has been associated with pollination by pollen-collecting bees (Burger, 1971
). Studies comparing the pollination biology of species of Piper with and without tightly congested inflorescences may provide additional perspective on patterns of diversification within the genus. A working hypothesis would state that Piper species with tightly congested inflorescences have a more specialized guild of pollinators than Piper species with lax inflorescences. One future goal is to use phylogeny as a tool to design a sampling strategy for the comparative study of the regulation of organ number and size that would be coupled with field observations on pollinator diversity for the same set of species. An integrative model for relating spatial constraints to shifts in pollinators could begin to elucidate some of the evolutionary forces responsible for the exceptional diversity within Piper.
|
FOOTNOTES |
|---|
2 Author for correspondence (e-mail: maj3{at}duke.edu
, tel.: 919-660-7359).
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Baldwin, B. G. 1992 Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Molecular Phylogenetics and Evolution 1: 3–16[CrossRef][Medline]
———. 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]
———, M. J. Sanderson, J. M. Porter, M. F. Wojciechowski, C. S. Campbell, and M. J. Donoghue. 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]
Bizerril, M. X. A., and A. Raw. 1998 Feeding behaviour of bats and dispersal of Piper arboreum seeds in Brazil. Journal of Tropical Ecology 14: 109–114
Bornstein, A. J. 1989 Taxonomic studies in the Piperaceae—I. The pedicellate Pipers of Mexico and Central America (Piper subg. Arctottonia). Journal of the Arnold Arboretum 70: 1–55[ISI]
Burger, W. C. 1971 Piperaceae. In W. C. Burger [ed.], Flora Costaricensis, Fieldiana Botany 5: 5–218
Callejas, R. 1986 Taxonomic revision of Piper subgenus Ottonia (Piperaceae). Ph.D. dissertation, City University of New York, New York, New York, USA
Chase, M. W., et al. 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528–580[CrossRef][ISI]
Chew, W.-L. 1972 The genus Piper (Piperaceae) in New Guinea, Solomon Islands and Australia, 1. Journal of the Arnold Arboretum 53: 1–25[ISI]
Cronquist, A. 1981 An integrated system of classification of flowering plants. Columbia University Press, New York, New York, USA
deCandolle, C. 1923 Piperacearum clavis analytica. Candollea 1: 65–415
de Figuereido, R. A., and M. Sazima. 2000 Pollination biology of Piperaceae species in southeastern Brazil. Annals of Botany 85: 455–460
Donoghue, M. J., and J. A. Doyle. 1989 Phylogenetic analysis of angiosperms and the relationships of Hammameliidae. In P. R. Crane and S. Blackmore [eds.], Evolution, systematics, and fossil history of the Hammamelidae, vol. 1, 17–45. Clarendon, Oxford, UK
Doyle, J. J., and J. L. Doyle. 1987 A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15
Ehringhaus, C. 1997 Medicinal uses of Piper spp. (Piperaceae) by an indigenous Kaxinawa community in Acre, Brazil: ethnobotany, ecology, phytochemistry and biological activity. MSc thesis, Florida International University, Miami, Florida, USA
Felsenstein, J. 1985 Confidence limits on phylogenies: an approach using bootstrap. Evolution 39: 783–791[CrossRef][ISI]
Fleming, T. H. 1981 Fecundity, fruiting pattern, and seed dispersal in Piper amalago (Piperaceae), a bat dispersed tropical shrub. Oecologia 51: 42–46
———. 1985 Coexistence of five sympatric Piper (Piperaceae) species in a tropical dry forest. Ecology 66: 688–700[CrossRef][ISI]
Gardner, R. O. 1997 Macropiper (Piperaceae) in the south-west Pacific. New Zealand Journal of Botany 35: 293–307[ISI]
Gentry, A. H. 1990 Floristic similarities and differences between southern Central America and upper Central Amazonia. In A. H. Gentry [ed.], Four Neotropical rainforests, 141–157. Yale University Press, New Haven, Connecticut, USA
Goloboff, P. A. 1997 Self-weighted optimization: tree searches and character state reconstructions under implied transformation costs. Cladistics 13: 225–245[CrossRef][ISI]
Green, P. S. 1994 Piperaceae. In Flora of Australia, 49: 46–50. Australian Biological Resources Study, Canberra, A.C.T., Australia
Howard, R. A. 1973 Notes on the Piperaceae of the Lesser Antilles. Journal of the Arnold Arboretum 54: 377–411[ISI]
Jaramillo, M. A., and P. S. Manos. 1998 Preliminary phylogenetic studies of the genus Piper (Piperaceae) using ITS sequence data. Abstract, American Journal of Botany 80: 137[CrossRef]
Kron, K. A., and J. M. King. 1996 Cladistic relationships of Kalmia, Leiophyllum and Loiseleuria (Phyllodoceae, Ericaceae) based on rbcL and nrITS data. Systematic Botany 21: 17–29[CrossRef][ISI]
Kubitzki, K., J. G. Rohwer, and V. Bittrich [eds.]. 1993 Flowering plants. Dycotyledons. Magnoliid, Hamamelid and Caryophyliid families. Springer Verlag, Berlin, Germany
Kunth, K. 1839 Bemerkungenüber die Familie der Piperaceen. Linnaea 13: 562–726
Lebot, V., and J. Lévesque. 1989 The origin and distribution of kava (Piper methysticum Forst. f. and Piper wichmannii C.DC, Piperaceae): a phytochemical approach. Allertonia 5: 223–280
Lei, L.-G., and H.-X. Liang. 1998 Floral development of dioecious species and trends of floral evolution in Piper sensu lato. Botanical Journal of the Linnean Society 127: 225–237[CrossRef]
Liu, T.-S., and F.-L. Wang. 1975 Piperaceae. In H.-L. Li. [ed.], Flora of Taiwan, vol. 2, 556–565. Epoch Publishing Company, Taipei, Taiwan
Loconte, H., and D. W. Stevenson. 1991 Cladistics of the Magnoliidae. Cladistics 7: 267–296
Long, D. G. 1984 Piperaceae. In A. J. C. Grierson and D. G. Long [eds.], Flora of Bhutan, vol. 1 (2), 342–351. Royal Botanical Garden, Edinburgh, UK
Lundberg, J. G. 1972 Wagner networks and ancestors. Systematic Zoology 21: 398–413[CrossRef][ISI]
Maddison, W. P., and D. R. Maddison. 1992 MacClade: analysis of phylogeny and character evolution, version 3. Sinauer, Sunderland, Massachusetts, USA
Manos, P. S. 1997 Systematics of Nothofagus (Nothofagaceae) based on rDNA spacer (ITS): taxonomic congruence with morphology and plastid sequences. American Journal of Botany 84: 1137–1155[Abstract]
Marquis, R. J. 1988 Phenological variation in the neotropical understory shrub Piper arieianum: causes and consequences. Ecology 69: 1552–1565[CrossRef][ISI]
Miquel, F. A. G. 1843–1844 Systema Piperacearum. Kramer, Rotterdam, The Netherlands
Nixon, K. C., and J. M. Carpenter. 1996 On consensus, collapsability, and clade concordance. Cladistics 12: 305–321[CrossRef][ISI]
Presl, C. B. 1849 Epimeliae botanicae. A. Haase, Prague, Czechoslovakia
Qiu, Y.-L., L. Jungho, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. ZImmer, Z. Chen, V. Savolalnen, and M. W. Chase. 1999 The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404–407
Quisumbing, E. 1930 Philippine Piperaceae. The Philippine Journal of Science 43: 1–246
Sanderson, M. J., and M. J. Donoghue. 1994 Shifts in diversification rate with the origin of angiosperms. Science 265: 1590–1593
Sang, T., D. J. Crawford, S.-C. Kim, and T. F. Stuessy. 1994 Radiation of the endemic genus Dendroseris (Asteraceae) on the Juan Fernandez Islands: evidence from sequences of the ITS regions of nuclear ribosomal DNA. American Journal of Botany 81: 1494–1501[CrossRef][ISI]
Semple, K. S. 1974 Pollination of Piperaceae. Annals of the Missouri Botanical Garden 61: 868–871[CrossRef][ISI]
Smith, A. C. 1975 The genus Macropiper (Piperaceae). Botanical Journal of the Linnean Society 71: 1–38
Soltis, P. A., D. E. Soltis, and M. W. Chase. 1999 Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402: 402–404
Steyermark, J. A. 1984 Piperaceae. In Flora of Venezuela, vol. II, 2nd part. Instituto Nacional de Parques, Editoral Fundación, Caracas, Venezuela
Swofford, D. L. 1998 PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4.0. Sinauer Associates, Sunderland, Massachusetts, USA
Takhtajan, A. 1997 Diversity and classification of flowering plants. Columbia University Press, New York, New York, USA
Tebbs, M. C. 1989 Revision of Piper (Piperaceae) in the New World. 1. Review of characters and taxonomy of Piper section Macrostachys. Bulletin of the Natural History Museum of London 19: 117–158
———. 1993a Piperaceae. In K. Kubitzki, J. G. Rohwer, and V. Bittrich [eds.], Flowering plants. Dycotyledons. Magnoliid, Hamamelid and Caryophyliid families. Springer Verlag, Berlin, Germany
———. 1993b Revision of Piper (Piperaceae) in the New World, 3. The taxonomy of Piper sections Lepianthes and Radula. Bulletin of the Natural History Museum of London 23: 1–50
Thies, W., E. W. Kalko, and H. U. Schnitzler. 1998 The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behavioral Ecology and Sociobiology 42: 397–409
Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997 The CLUSTALX. WINDOWS interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 16–50
Trelease, W. 1927 The Piperaceae of Panama. Contributions the United States National Herbarium 26: 15–50
———. 1928 Trianaeopiper, a new genus of Piperaceae. Proceedings of the American Philosophical Society 67: 47–50
———. 1930 The geography of American peppers. Proceedings of the American Philosophical Society 69: 309–327
———, and G. T. Yuncker. 1950 The Piperaceae of northern South America. University of Illinois Press, Urbana, Illinois, USA
Tucker, S. C. 1982 Inflorescence and floral development in the Piperaceae, III. Floral ontogeny of Piper. American Journal of Botany 69: 1389–1401[CrossRef][ISI]
———, A. W. Douglas, and H.-X. Liang. 1993 Utility of ontogenetic and conventional characters in determining phylogenetic relationships of Saururaceae and Piperaceae (Piperales). Systematic Botany 18: 614–641[CrossRef][ISI]
Verdcourt, R. 1996 Piperaceae. In R. M. Polhill [ed.], Flora of Tropical East Africa. Royal Botanical Gardens, Kew, UK
Wheeler, W. C. 1990 Nucleic acid sequence phylogeny and random outgroups. Cladistics 6: 363–368
Yongqian, C., X. Nianhe, and M. G. Gilbert. 1999 Piperaceae. In W. Zheng-yi and P. H. Raven [eds.], Flora of China, Cycadaceae through Fagaceae, 110–129. Science Press, Beijing and Missouri Botanical Garden Press, Saint Louis, Missouri, USA
Yuncker, T. G. 1953 The Piperaceae of Argentina, Bolivia and Chile. Lilloa 27: 97–303
———. 1972 The Piperaceae of Brazil, I. Piper—Group I, II, III, IV. Hoehnea 2: 19–366
———. 1973 The Piperaceae of Brazil, I. Piper—Group V, Ottonia, Pothomorphe, Sarcorhachis. Hoehnea 3: 29–284
This article has been cited by other articles:
|
|
 |
|
  P. K. Endress and J. A. Doyle Reconstructing the ancestral angiosperm flower and its initial specializations Am. J. Botany, January 1, 2009; 96(1): 22 - 66. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Arias and J. H. Williams Embryology of Manekia naranjoana (Piperaceae) and the origin of tetrasporic, 16-nucleate female gametophytes in Piperales Am. J. Botany, March 1, 2008; 95(3): 272 - 285. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Y. Smith and R. A. Stockey Establishing a fossil record for the perianthless Piperales: Saururus tuckerae sp. nov. (Saururaceae) from the Middle Eocene Princeton Chert Am. J. Botany, October 1, 2007; 94(10): 1642 - 1657. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Wanke, L. Vanderschaeve, G. Mathieu, C. Neinhuis, P. Goetghebeur, and M. S. Samain From Forgotten Taxon to a Missing Link? The Position of the Genus Verhuellia (Piperaceae) Revealed by Molecules Ann. Bot., June 1, 2007; 99(6): 1231 - 1238. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. J. Tepe, M. A. Vincent, and L. E. Watson Stem diversity, cauline domatia, and the evolution of ant-plant associations in Piper sect. Macrostachys (Piperaceae) Am. J. Botany, January 1, 2007; 94(1): 1 - 11. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||
Trianaeopiper, 
Sarcostemon, 
Penninervia. See 