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Phylogeny, species richness, and ecological specialization in Cyperaceae tribe Cariceae.

Introduction

Species-rich genera of plants, especially those with broad geographic distribution, are both a challenge and an opportunity for the integration of ecological and evolutionary perspectives on diversity. Phylogenetic analysis is complicated not only by the sheer size of the genus but also by the difficulty of finding gene regions with sufficient variability to resolve such a large number of species. Nevertheless, a phylogenetic perspective is essential for exploring two fundamental ecological and evolutionary questions related to diversity, adaptation, and community assembly: Why are there so many species and why do plants grow where they do? A robust phylogenetic hypothesis can identify rapidly evolving lineages that may be the result of adaptive radiation. Geographic patterns, environmental correlates of distribution, and plant traits can be mapped on the phylogeny to explore the processes of speciation and adaptive radiation. Phylogenetic information is needed to study the apparently conflicting predictions from niche theory and the principle of competitive exclusion on the one hand (niche differentiation), and the idea that close relatives share many genes and should therefore share adaptations to similar environments on the other (niche conservatism; cf. Silvertown et al., 2001; Ackerly, 2003; Chase & Leibold, 2003; Cavender-Bares et al., 2004; Wiens & Graham, 2005). Niche differentiation and niche conservatism give different predictions about the congruence of evolutionary relationship (as demonstrated by phylogeny) and ecological relationship (as demonstrated by co-occurrence within a habitat).

If niche differentiation is an important part of the speciation process in plants, we expect to see divergence between sister-species pairs on at least one niche axis (sensu Hutchinson, 1957) if they both continue to occupy the same region. Similarly, if niche differentiation plays a critical role in adaptive radiation, we expect to see segregation along environmental gradients within lineages that show rapid radiation within a particular geographic area. On the other hand, sister species that occupy different continents or regions separated by dispersal barriers may or may not show niche differentiation, depending on the relative similarity of the habitats in each region. Our expectation is conditioned by our knowledge of the temporal and spatial scales at which the species under consideration interact.

Niche conservatism is the tendency for species to share ecological traits due to common ancestry (reviewed by Wiens & Graham, 2005). If niche conservatism is a significant evolutionary force in plants, then we would expect to see consistency within lineages in habitat preferences and in the traits that allow germination and persistence in these habitats (Cavender-Bares et al., 2004). We might expect niche conservatism with respect to traits that are difficult to evolve and that allow survival in a habitat. Different degrees of drought tolerance, shade-tolerance, frost-tolerance, and tolerance of flooded, anaerobic conditions have evolved in different plant groups and these physiological traits determine the habitats in which they can best compete. On the other hand, most habitats are heterogeneous mosaics of microhabitats differing in soil texture, fertility, and water-holding capacity and in characteristics that affect nutrient availability such as pH and amount of organic matter and we would expect divergence in traits that allow coexistence within the habitat. When congeneric species co-occur in such heterogeneous habitats, we are more likely to see niche segregation on gradients of soil pH, fertility, and moisture than to see niche conservatism in these features.

Cyperaceae tribe Cariceae, comprising ca. 2,100 species occurring in a wide range of habitats on six continents, is an excellent system for investigation of the issues described above. Recognition of a close relationship between the species-rich genus Carex and four smaller genera in tribe Cariceae, and the hypothesis of a reduction series in inflorescence structure from Schoenoxiphium through Kobresia and Uncinia to Carex, dates to early classifications of the Cyperaceae (Kukenthal, 1909). Recent phylogenetic hypotheses based on DNA sequence comparisons have underscored the closeness of the relationship, but called into question the proposed evolutionary scenarios (e.g., Yen & Olmstead, 2000; Roalson et al. 2001; Starr et al., 2004; Waterway & Starr, 2007). From these studies, it is clear that the tribe as a whole is monophyletic. Three major lineages have been identified within it. Carex subg. Vignea, with only minor modifications, is monophyletic in all molecular studies to date (Hendrichs et al., 2004; Ford et al., 2006; Waterway & Starr, 2007). The monophyly of the largest clade (ca. 1,400 species), combining subgenera Carex and Vigneastra, is also strongly supported. The third clade recovered in most molecular analyses of the tribe, but with weak or no support for its monophyly, includes all other genera of tribe Cariceae along with several Carex species having reduced inflorescences, particularly the androgynous unispicate Carex species (Starr et al., 2004). Previous studies have not provided strong support for the relationships among these three clades, which apparently diverged early in the evolution of the group. However, the numerous Asian species, and groups proposed as primitive based on morphological considerations, such as sections Decorae and Siderostictae (Egorova, 1999), have not yet been included in published DNA-based phylogenetic studies.

In this paper, we present a new phylogenetic hypothesis for Cyperaceae tribe Cariceae based on DNA sequence comparisons among 140 species representing the major clades found in our preliminary analyses of nearly 400 species from five continents. Using this hypothesis and previous work, we illustrate both niche conservatism and niche differentiation at different temporal and spatial scales within the tribe, and suggest directions for further research integrating ecological and phylogenetic data to study the evolution of diversity.

Materials and Methods

To construct a backbone tree of reasonable size for analysis, we selected 140 species (Table 1) representing the major clades found in preliminary analyses of nearly 400 species of tribe Cariceae from North America, Europe, Japan, Africa, Australia and New Zealand. Clades within tribe Cariceae were sampled roughly in proportion to their species richness. Four outgroup genera were included, chosen from among those identified as part of the same clade by Dhooge (2005). We sequenced three nuclear ribosomal spacers, ITS l, ITS2 and ETS-1 f, known to be variable within and between major clades of Cariceae, along with the trnL intron and trnL-trnF intergenic spacer from the chloroplast genome, which exhibit more variation between clades (Waterway & Starr, 2007) (Table 1).

For new sequences reported in this paper, total DNA was extracted from fresh or silica-dried leaves using a modified CTAB protocol implemented on an AutoGen 850 automated DNA extractor after 2 rain of grinding with zirconium beads in tubes chilled with liquid nitrogen on an AutoGrinder 48 (Autogen, Inc., Holliston, MA). The DNA regions were amplified and sequenced using protocols detailed in Waterway and Starr (2007). Sequence data are deposited in Genbank (Table 1).

We assembled the DNA fragments into contigs and edited them with ChromasPro 1.32 (Technelysium Pty Ltd.) prior to alignment using ClustalX 1.81 (Thompson et al., 1997). Inferred insertion or deletion events (indels) were coded using the simple gap-coding method of Simmons and Ochoterena (2000) as implemented in GapCoder (Young & Healy, 2003). We conducted several heuristic searches of both separate and combined data matrices, with and without indel characters, using the maximum parsimony criterion in Paup * 4.0b10 (Swofford, 2002), with 1 to 1,000 addition sequence replicates with limits on time or number of trees saved per replicate. For the combined data matrix including indels, the shortest trees (length 5,738) were found using either 100 addition sequence replicates and saving a maximum of 200 trees per replicate (2,697 shortest trees), or 1,000 addition sequence replicates, saving 5 trees per replicate (4,995 shortest trees). To evaluate branch support for these trees, we ran 10,000 bootstrap replicates, saving only one tree per replicate (MULTREES = off) (cf. DeBry & Olmstead, 2000). We also conducted Bayesian analysis on the combined data matrix (nucleotide characters only) using MrBayes 3.012 (Ronquist &

Huelsenbeck, 2003) with three partitions, one for each gene region. We used a general time-reversible model, allowing a varying proportion of invariant sites and estimating variation in substitution rate across sites using a gamma distribution (GTR + I + G) for ITS and trnL and a similar general time-reversible model, but without including the proportion of invariant sites in the model (GTR + G), for ETS, as chosen by MrModelTest 2.2 (Nylander, 2004) based on hierarchical likelihood ratio tests. Parameters were set to vary independently within each gene region. We ran two simultaneous independent analyses from different random starting trees using four chains of Metropolis-coupled Monte Carlo simulations for 1,800,000 generations, sampling one tree each 100 generations and discarding the first 6,000 trees of each run. The 12,000 trees generated after convergence were summarized with a 50% majority rule consensus tree in Paup* 4.0b10 to assess the posterior probabilities of each clade.

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The Core Carex clade, with many strongly supported branches of closely related species, is used to illustrate the concepts of niche conservatism and niche differentiation. Geographic range and rough estimates of distribution along gradients of moisture and insolation for species of the Core Carex clade were added to one of the most parsimonious trees. Geographic range was determined from the World Checklist of Monocotyledons compiled by the Royal Botanic Gardens, Kew (www.rbgkew.org.uk/wcsp/monocots). Data on ecological tolerances is based on our own field experiences and information in recent floras (e.g., Jermy et al., 1982; Owhi, 1984; Egorova, 1999; Ball & Reznicek, 2002; Hoshino et al., 2002).

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Results

Contributions of each gene region to the combined data matrix with 2,826 nucleotide positions and 344 indels are given in Table 2. Twenty-nine percent of the nucleotide positions and 48% of the indel characters were parsimony-informative, giving a total of 988 parsimony-informative characters in the combined matrix. The largest proportions of invariant sites were in the 5.8S ribosomal gene and in the trnL region. Parsimony analyses of each gene region independently gave less resolved trees than the combined analyses. The large number of taxa combined with relatively low variability in each DNA region precluded formal testing for incongruence, but visual inspection revealed few conflicts in tree topology. Exceptions will be noted where relevant in the subsequent paragraphs. Results from Bayesian and parsimony analyses of the combined data were similar, but more clades were strongly supported in the Bayesian analysis.

One of the 2,697 shortest trees from parsimony analysis of the combined data matrix is illustrated in Figs. 1 ,2, 3, 4. This particular tree was chosen for illustration because it is very close to the 50% majority rule tree calculated to summarize the Bayesian posterior probabilities so branch support from both analyses can be shown on it. Note that many of the branches collapse in the strict consensus tree based on parsimony analysis of the combined data matrix (shown as dotted lines in the Figs. 2, 3, 4). We focus our discussion on branches with strong to moderate support.

Figure 1 shows branch lengths and names for the major clades following the nomenclature of Waterway & Starr (2007) and Figs. 2, 3, 4 show branch support and names of species with their geographic distributions and rough estimates of their positions on both moisture (diamonds) and insolation (squares) gradients for the Core Carex clade (Figs. 3 and 4). For ease of discussion, capital letters are used to reference each clade arising from the backbone (whether statistically supported or not) within the Core Carex clade in Fig. 1 and corresponding letters are used on the branches in Figs. 3 and 4 to indicate these same clades. In addition to the bootstrap support values shown above branches having >50% bootstrap support in the parsimony analysis, clade posterior probabilities greater than 95% (from the Bayesian analysis) are shown with black circles and those from 91-94% with gray circles below the branches in Figs. 2, 3, 4. Bootstrap support values and Bayesian clade posterior probabilities should not be interpreted as equal. Simulation studies by Zander (2004) indicate that minimum values required for a 95% confidence interval are between 88 and 100% for bootstrap percentages and between 0.91 and 1.00 for Bayesian clade posterior probabilities. We use these values as criteria for describing clades as strongly or well supported, and describe those with bootstrap values between 75 and 87 as having moderate or good support, and those between 55 and 74 as weakly or poorly supported.

As in all previous analyses, tribe Cariceae was strongly supported as monophyletic no matter which of the four outgroup genera was used to root the tree. Four major clades within the tribe, including a strongly supported new clade positioned as sister to the rest of tribe Cariceae, were recovered in both parsimony and Bayesian analyses of the combined data matrix (Figs. 1 and 2). Two species of section Siderostictae formed the new early-diverging clade that received 100% bootstrap support in all analyses, including those using each gene independently. Both the Vignea clade and the Core Carex clade also received very strong support in all analyses, but the Caricoid clade did not (Figs. 2 and 3). Support for grouping Vignea, Caricoid and Core Carex clades as sister to the Siderostictae clade was 100% in all analyses but no pairing of any two of the three larger clades was supported. Within the Caricoid clade, the only strongly supported groups in this limited sampling were the Uncinia clade and the pairing of C. backii (section Phyllostachyae) with Cymophyllus fraserianus. All other branches collapsed in the strict consensus tree based on parsimony analysis of the combined data matrix (Fig. 2).

Within the Vignea clade, support was strong for the tristigmatic species Carex gibba as sister to all other Vignea species and sections Glareosae, Ovales, and Stellulatae were all strongly supported as monophyletic. Other strongly supported groups were: 1) the C. rosea complex (section Phaestoglochin); 2) two Australasian species of section Heleoglochin (=section Paniculatae Kunth) (C. appressa and C. secta); 3) C. sparganioides (section Phaestoglochin) and C. vulpinoidea (section Multiflorae); and 4) C. chordorrhiza (section Chordorrhizae) and C pseudocuraica (section Holarrhenae) which are similar in growth form and habitat. Even with the limited sampling here, it is apparent that sections Phaestoglochin, Heleoglochin, Vulpinae and possibly Deweyanae are polyphyletic.

Within the Core Carex clade, branch lengths along the backbone of the clade are very short and all collapse in the strict consensus tree from the combined parsimony analysis except the branch supporting most Core Carex species as sister to clade A (C. eburnea and C. cruciata), the branch supporting clade D (the Porocystis clade, see below), and the branch supporting clade K (Figs. 3 and 4). However, more than 20 subclades, each represented in this analysis by only two to four species, are very strongly supported and correspond to groups that also share structural similarities. We describe these below within the lettered clades labeled in Figs. 1, 3, and 4.

Clade A (Fig. 3) groups Carex cruciata (subg. Vigneastra), a large subtropical species from Southeast Asia with branching inflorescences and inflorescence prophylls, with C. eburnea (subg. Carex), a small temperate species with very short, few-flowered spikes. Support for this branch is strong in the Bayesian analysis but moderate at best (77%) in the parsimony analyses. The long branch-lengths and morphological dissimilarity suggest that the grouping may be an example of long-branch attraction, rather than close relationship.

Clade B (Fig. 3) is a diverse assemblage of species including six groups strongly supported in both parsimony and Bayesian analyses of the combined data set: 1) Carex depauperata (section Depauperatae) with C. flacca (section Thuringiaca); 2) C cherokeensis and C. obispoensis (section Hymenochlaenae s. str.); 3) C. fernaldiana and C Joliosissima (section Mitratae); 4) C communis, C. peckii, and C pensylvanica (section Acrocystis); 5) C heteroneura and C media (section Racemosae); and 6) C boottiana, C. laticeps, C papillaticulmis, and C subdita (section Rhornboidales). Two species of subgenus Vigneastra (C. baccans and C. filicina) and two species of section Clandestinae (C. digitata and C. lanceolata), as well as C. glacialis (section Lamprochlaenae) also form part of Clade B, but there is no clear support for their relationships to each other, nor for clade B as a whole in any of the analyses. Two of these groups, sections Mitratae and Rhomboidales are predominantly Asian species from forested habitats. Carex depauperata and C. flacca both grow in relatively dry, open to partially shaded sites associated with limestone substrates. Sections Acrocystis and Racemosae are both large groups with diverse habitat affinities and both are polyphyletic when more species are sampled (M. J. Waterway, unpubl.).

Clade C1 (Fig. 3) comprises two strongly supported clades, one combining the structurally similar sections Carevanae, Granulales, and Griseae, and the other representing section Aulocystis. Species of section Aulocystis grow in open moist to wet habitats of western North America while sections Careyanae, Granulates, and Griseae are predominantly eastern North American forest species. Together with monotypic section Collinsiae (endemic to shaded peatlands in eastern North America), these two disparate groups form clade C1, which has 100% bootstrap support and clade posterior probability of 1.0. Clade C1 is also strongly supported by ETS data alone, moderately supported by ITS data alone, but not supported by the trnL region, although the subclades are well supported by trnL data. Sections Bicolores, Laxiflorae and Paniceae make up Clade C2 which shows an early divergence into two subclades, one predominantly from North America and the other predominantly Asian. The majority of species in this clade are shade-tolerant forest species from eastern North America or eastern Asia, but there are also a few circumboreal species of peatlands or other moist open sites. None of the single-gene analyses show any support for combining clades C1 and C2 into Clade C, but the branch supporting Clade C has 95% posterior probability in the Bayesian analysis of the combined data set.

Clade D (Fig. 4) is a strongly supported group of eastern North American species drawn from four different currently recognized sections (Hallerianae, Hirtifoliae, Hymenochlaenae, Porocystis). Most of these species are shade-tolerant and generally occupy forested habitats. Branch lengths in this group are very short, suggesting recent divergence. Most of these species are shade-tolerant and generally occupy upland forested habitats.

Clade E (Fig. 4) has good support in the combined analyses. Section Rostrales forms one strongly supported subclade and species classified in geographically widespread sections Spirostachyae, Ceratocystis, Rhynchocystis, and Sylvaticae comprise its sister group. There is strong support for pairing sections Rhynchocystis and Sylvaticae in the same subclade, but only weak support for any other relationship within clade E. Species of section Rostrales usually grow in or near wetlands, Carex sylvatica and C. pendula are typically in forests, while C. flava and C. punctata are more common in open or partially shaded moist to wet sites.

Only two species, Carex pedunculata (section Clandestinae) and C. picta (section Pictae), form clade F (Fig. 4), strongly supported in all analyses of the combined matrix and supported by single gene analyses except for the trnL-trnF region. Both species occupy upland forested areas in eastern North America.

Clade G (Fig. 4) is a heterogeneous assemblage of mostly Asian and Eurasian species, but also including Carex scabrata (section Anomalae) and C. vestita (section Paludosae) endemic to eastern North America. This clade and most subclades within it have strong support in the Bayesian analysis, but moderate to no support from the parsimony analyses. Eastern Asian species in this group are from sections Confertiflorae and Molliculae with the exception of C. latisquamea which is currently classified in section Carex.

Clade H (Fig. 4) is another heterogeneous group without significant branch support for the clade or its subclades, except for two species of section Limosae and their sister-group relationship with Carex stylosa (section Racemosae) and C. prasina (section Hymenochlaenae)(Bayesian posterior probability = 0.94). Carex scirpoidea is part of this clade in the tree illustrated in Fig. 4, but does not consistently assume this position. This dioecious unispicate species is strongly supported within the Core Carex clade but there is no support for a close relationship with any other species sampled. Carex limosa and C. magellanica (section Limosae) along with C. stylosa occur in open boreal peatlands while C. prasina grows in wet shady places in eastern North America. Other species in clade H also occupy either open wetland sites or wet places in forests, including the two representatives of section Phacocystis (C. gynandra and C. nigra), two species of section Squarrosae (C. squarrosa and C. typhina) and the closely related C. shortiana, plus C. joorii (section Glaucescentes) and C. macrochaeta (section Limosae).

Clade K (Fig. 4) is also composed predominantly of wetland species. This is a strongly supported group comprising species from sections Vesicariae, Paludosae, Lupulinae, and Carex. Support for sectional groups within clade K (except section Vesicariae) is moderate to strong in this small sampling of the clade, but breaks down when more species from these groups are added to the analysis (M. J. Waterway, unpubl.). This clade includes species from six continents including those from Asia, Australasia, Europe, and North America shown in Fig. 4.

Wetland species that tolerate water-saturated soil or submerged conditions are found mostly in clades H and K, including species in sections Vesicariae, Paludosae (in part), Carex, Limosae, Phacocystis, Squarrosae, and Lupulinae. The branch combining clades H and K does not have significant bootstrap support in parsimony analyses of the combined dataset, but in the Bayesian analysis it has a posterior probability of 0.99. Several species-pairs in this group are from different continents (M. J. Waterway, unpubl.), including the Carex trichocarpa/C, drymophila pair shown here (Fig. 4) which occur in North America and Eurasia, respectively, but show very little molecular or morphological divergence.

A quite different trend can be seen among species of forested habitats. Groups composed primarily of forest species tend to be from a single geographical area. For example, sections Rhomboidales and Mitratae are eastern Asian forest groups, while the Careyanae-Griseae-Granulares clade and the Porocystis clade are restricted to eastern North America and Central America.

Discussion

Siderostictae Clade

Adding a variety of Eastern Asian species to the phylogenetic analysis of tribe Cariceae sheds new light on the evolution of the group. While the overall topology of trees in this study is similar to that presented in Waterway and Starr (2007), the addition of section Siderostictae as the earliest diverging group within the tribe, and the presence of Asian species in well-supported positions at the base of both the Vignea clade and the core Carex clade, suggest an Asian origin for the tribe. Based on ITS and ETS sequence data, other species in the eastern Asian section Siderostictae (C. tumidula Ohwi, C. okamotoi Ohwi, and C. ciliatomarginata Nakai) are also part of this early-diverging clade (T. Hoshino, unpubl.). Species of section Siderostictae have leaves much broader than in most carices, androgynous spikes often binate or ternate at the inflorescence nodes, beakless perigynia with obtuse pistillate scales, and they occasionally have rachillae with terminal male flowers protruding from the perigynia. While Kukenthal (1909) and Koyama (1962) grouped these broad-leaved sedges with broad-leaved species from North American forests (present sections Careyanae and Laxiflorae), Egorova (1999) considered androgynous spikes, multiple spikes at a single node, and persistent rachillae bearing male flowers or floral scales as primitive characters and therefore treated section Siderostictae as a primitive group. Results presented here suggest that the broad-leaved growth form has evolved multiple times as an adaptation to shady conditions in forests. On the other hand, the primitive characters listed by Egorova (1999) can each be found in early diverging lineages of one or more of the other three major clades, and it is not so difficult to envision species with these characters as progenitors of the tribe. Small numbers of large chromosomes also characterize section Siderostictae and Tanaka (1939) found C. siderosticta to have the lowest chromosome number in the genus (n = 6).

Other implications for classification and chromosomal evolution will be discussed elsewhere in the context of more complete sampling of each major group. Our goal in this paper is to illustrate the potential for using the developing phylogenetic hypothesis for tribe Cariceae in investigations of ecological and evolutionary questions and we will confine the rest of the discussion to these issues.

Niche Conservatism

Two trends, one related to flooding tolerance and one related to shade tolerance, are suggested by the backbone tree presented in this paper. Within the Core Carex clade, species of wetland habitats, especially those that tolerate persistently water-saturated soil or root below the water table along lakeshores or in wetlands, are found in relatively few clades, with most of them in clades H and K (Fig. 4). Broader sampling of this group (M. J. Waterway, unpubl.) reveals that the large majority of true wetland species in subgenus Carex are found in these clades. Clade G also has a few flood-tolerant species, as well as those that grow in wet places in forests. Two small sections, Aulocystis (clade C1) and Rostrales (clade E), are also predominantly wetland species. Clade C2 also has a few peatland species, but the majority of species in that group grow in forests. This clustering of wetland species within particular clades and the prevalence of flood-tolerant species in each of these groups suggest niche conservatism in traits related to flooding tolerance. Several traits that appear to be adaptive in wetland situations are common in these clades: rhizomatous growth form that allows rapid colonization of standing water; aerenchyma tissue in roots, rhizomes and culms, allowing tolerance of the anaerobic conditions at submerged sites; and inflated perigynia giving the buoyancy necessary for water dispersal. The presence of sister species from different continents in clade K (e.g., C. trichocarpa and C. drymophila) suggest recent long-distance dispersal between continents for at least some wetland sedges. Egorova (1999) cites examples of dispersal of hydrochorous Carex species by muskrat and elk, by adherence to the legs of waterfowl, and by ducks that forage on the fruits. The feasibility of intercontinental sedge dispersal by migrating waterfowl was shown by de Vlaming and Proctor (1968) who demonstrated viability of Carex and other sedge diaspores after more than 24h in the digestive systems of mallard ducks and suggested that these highly resistant seeds were an adaptive trait in wetland sedges.

Shade-tolerant species in the Core Carex clade also have a clustered distribution on the cladogram (Figs. 3 and 4). The Careyanae-Griseae-Granulares clade, the Porocystis clade, much of the Bicolores-Laxiflorae-Paniceae clade, and the C. pedunculata-C, picta clade are most commonly found in shaded forest habitats in North America. Similarly, eastern Asian groups like the Mitratae clade, the Rhomboidales clade, and the Confertiflorae-Molliculae species in clade G, are also most frequent in forests. Many of these species have relatively broad leaves typical of shaded habitats, long arching culms that facilitate gravity-dispersal away from the parent plant or elaisomes for dispersal by ants (Handel et al., 1981). Independent evolution of these shade-tolerant lineages on different continents suggests early disjunction and either the retention of ancestral shade tolerant traits from a shade-tolerant progenitor, or convergent evolution in response to shaded conditions, indicating niche conservatism at one or both time scales.

Niche Differentiation

Niche differentiation or niche segregation along environmental gradients is expected to evolve among closely related species as part of the speciation process (Levin, 2004). A complete and fully resolved phylogeny is needed to identify sister-species pairs and sets of closely related species that result from adaptive radiation to test this hypothesis. Our backbone tree includes only a few sister-species pairs to illustrate niche differentiation. Much more ecological data is available for boreal and temperate peatland species than for any other group of sedges. Species of tribe Cariceae often make up 20-30% of the flora in these habitats and dominate large areas within them (Anderson et al., 1996; Gignac et al., 2004; Dabros & Waterway, 2008). Despite the large number of studies of peatlands in Canada (reviewed by Gignac et al., 2004), few studies focus explicitly on testing niche differentiation.

Based on data on water pH and rooting depth from 114 randomly selected field samples of each of four species from 29 fens in subarctic Quebec (Sehefferville region, 54[degree] 47'N, 66[degree]50'W), Dabros and Waterway (2004) used a multivariate analysis of variance to demonstrate significant differences in both pH and rooting depth between closely related species C. limosa and C. magellanica (section Limosae) and between C. livida and C. vaginata (section Paniceae). Further investigation of these two species pairs in a controlled greenhouse experiment testing the effect of water depth and nutrient levels on growth revealed that, although C. livida grew in significantly wetter sites in Schefferville fens than C. vaginata, both species grew best when rooted several centimeters above the water table and both did very poorly when rooted below the water table, at depths similar to those found for C. livida in the field (Dabros, 2004; Dabros & Waterway, in prep.). In contrast, C. limosa and C. magellanica each grew best in the controlled experiment when rooted at water depths approximating those where they are found in nature. Dabros (2004) interpreted these results as an indication that C. limosa and C. magellanica, which are sister-species (Clade H, Fig. 4), demonstrate niche differentiation that likely evolved during speciation. On the other hand, C. livida and C. vaginata, more distant relatives, but still within the same clade (Clade C2, Fig. 3), have similar fundamental niches but different realized niches (sensu Hutchinson, 1957); their lack of co-occurrence in nature suggests that current competitive interactions (both with C. vaginata and with other fen plants) force C. livida to grow in deeper water (where few species can survive) rather than rooting above the water table, which is where it grew best in the experiment.

This detailed study of two species pairs is just one example from many possible within peatland habitats. Within section Limosae, not only did C. limosa and C. magellanica differ in pH and rooting depth in relation to the water table, but a third species in this small clade, C. rariflora, differed from C. limosa on the rooting depth gradient and from C. magellanica on the pH gradient (Dabros & Waterway, 2008). Within section Stelludatae, C. exilis and C. interior had similar rooting depth but C. exilis grew under more acidic conditions than C. interior. Eriophorum angustifolium and E. viridi-carinatum also segregated on the pH gradient but not the rooting depth gradient. Overall, 75% of the species pairs from the same clade segregated along one or both of these gradients in the Schefferville fens. One interesting counter-example is the lack of segregation along either depth or pH gradients between the very closely related species C. rostrata and C. utriculata.

Among upland forest species, clear examples of niche differentiation between sister species are less common. Vellend et al. (2000), in a detailed study of 17 environmental variables characterizing the microhabitats of four upland forest species in an old-growth forest rich in sedges, used multivariate analysis to demonstrate differences in environmental preferences among species. Carex platyphylla and C. plantaginea (closely related species in section Careyanae) were most clearly differentiated. Latremouille and Waterway (in prep.) characterized the light, soil, and moisture conditions for 19 Carex species in an adjoining floodplain and upland forest. They were able to show clear differentiation between sister-species C. grayi and C. intumescens (Clade K, Fig. 4) in soil pH preference, as well as differences between this species pair and other species in the wetland clade along correlated gradients of soil moisture and proportion of organic matter. In contrast, they could not find clear segregation along any of these environmental gradients between closely related species pairs in the upland forest.

Future Prospects

This study illustrates the potential for using tribe Cariceae to investigate fundamental ecological and evolutionary questions, but much more work is needed to realize this potential. The backbone cladogram presented here, with only a few representatives in each clade, can only suggest geographic and ecological patterns. It is a necessary start toward the fully resolved cladogram including all species in tribe Cariceae that is needed for appropriate statistical testing of niche conservatism and niche differentiation using null models and permutation tests (see Hipp, this volume). More complete sampling is needed to accurately identify sister species and to determine the complete set of species in each clade. The backbone cladogram identifies major clades that can be studied independently using DNA regions like ETS-If and ITS, which are variable even among closely related species. However, additional sequences from more conservative DNA regions, such as chloroplast genes, spacers, and introns are needed to determine the relationships among the major clades within the tribe, and among subclades within each major clade. A complete phylogenetic hypothesis for tribe Cariceae seemed impractical just 10 years ago, but now ITS and ETS-1f have been sequenced for more than 25% of the tribe with more work in progress in several laboratories.

A greater challenge is to gather comparable ecological data for a large number of species. Compilations like that of Ellenberg (1991) for vascular plants of central Europe and Busch (2001) for European sedges and the recent emphasis in the ecological community on gathering comparative data on the functional traits of plants (Westoby et al., 2002) are steps in the right direction, but more purposefully collected, comparable data on patterns of co-occurrence in Carex communities are also needed. Answering the fundamental evolutionary questions posed here will require the integration of geographical, ecological and trait data on plant species with information about their phylogenetic relationships.

Acknowledgments We thank T. Katsuyama, M. J. Lechowicz, and Y. Takashima for help with field sampling; Y. Berube, N. Blackstock, P. de Lange, J. Dragon, T. Eades, P. Hyatt, S. Mills, and T. W. Smith for providing Carex leaves in silica gel and associated voucher specimens; Y. Berube, Y. Chtompel, G. Johnson, P. Talbot, G. Taylor, M.-E. Rheault, and C. Cho for assistance with DNA extraction, amplification and sequencing; the Genome Quebec laboratory at McGill University for DNA sequencing; J. Starr for permission to use three sequences from Starr, Harris & Simpson, in press; A. Dabros and C. Latremouille for data on environmental preferences; and the Natural Sciences and Engineering Research Council of Canada, the Canadian Foundation for Innovation, and the Fonds Qurbecois de la recherche sur la nature et les technologies (Quebec) for financial support.

Published online: 5 December 2008

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Marcia J. Waterway (1,3) * Takuji Hoshino (2). Tomomi Masaki (2)

(1) Plant Science Department, Macdonald Campus, McGill University, 21111 Lakeshore Road,, Ste. Anne de Bellevue, QC H9X 3V9, Canada

(2) Department of Biosphere-Geosphere System Science, Okayama University of Science, Ridai-Cho 1-1, Okayama 700-0005, Japan

(3) Author for Correspondence: e-mail: marcia.waterway@mcgill.ca
Table 1 Classification and Accession Data for Voucher Specimens for
DNA Sequences Used in this Study

Carex L.

subg. Carex

sect. Acrocystis Dumort., C. communis L. H. Bailey, CANADA: Quebec,
Mont St. Hilaire, Waterway MSH92.93 (MTMG), DQ998906, DQ998853,
DQ998959; C. peckii Howe, CANADA: Quebec, Phillipsburg, T. Eades
01.2005 (MTMG), DQ998940, DQ998886, DQ998993; C. pensylvanica Lam.,
CANADA: Quebec, Mont St. Hilaire, Waterway 99.013 (MTMG),
(AY757622, AY757682, AY757550); sect. Albae (Ascherson & Graebner)
Kirk., C. eburnea Boott, CANADA: Quebec, Chelsea, Waterway s.n.
(MTMG), DQ998912, DQ998859, DQ998965; sect. Anomalae J. Carey, C.
scabrata Schwein., CANADA: Quebec, Mont St. Hilaire, Waterway
99.001 (MTMG), (AY757585, AY757646, AY757512); sect. Aulocystis
Dumort., C. fissuricola Mack., USA: California, Mono Co., Waterway
2000.156 (MTMG), (AY757617, AY757678, AY757544); C. luzulina Olney,
USA.: California, Plumas Co., Waterway 99.077 (MTMG), DQ998929,
DQ998876, DQ998982; sect. Bicolores (Tuckerman ex L. H. Bailey)
Rouy, C. aurea Nuttall, CANADA: Montreal Island, Bare d'Urfe,
Waterway 99.010 (MTMG), DQ008901, DQ998848, DQ998954; sect. Carex,
C. drymophila Turcz., JAPAN: Hokkaido, Akkeshi-cho, Homakaigawa
River, Waterway 2004.348 (MTMG), DQ998911, DQ998858, DQ998964; (7.
latisquamea Kom., JAPAN: Honshu, Gunma Pref., Naganohara-cho,
Waterway 2004.277 (MTMG), DQ998927, DQ998874, DQ998980; C.
trichocarpa Muhl. ex Willd., USA: Virginia, Montgomery Co.,
Blacksburg, Waterway 2000.092 (MTMG), (AY757570, AY757632,
AY757497); sect. Careyanae Kuk., C. digitalis Willd., U.S.A: New
York, Seneca Co., Waterway 98.062 (MTMG), DQ998908, DQ998855,
DQ998961; C. plantaginea Lam., CANADA: Quebec, Hudson, Waterway
2000.002 (MTMG), (AY757613, AY757674, AY757540); sect. Ceratocystis
Dumort., C. flava L., CANADA: Quebec, Mont Rigaud, Waterway
2001.086 (MTMG), (AY757596, AY757657, AY757523); sect.
Chlorostachyae Tuckerman ex Meinshausen, C. capillaris L., CANADA:
Quebec, Schefferville, Waterway 97.075 (MTMG), DQ998905, DQ998852,
DQ998958; sect. Clandestinae G. Don, C. digitata L., UNITED
KINGDOM: England, Lancashire, Silverdale, Eaves Wood, N. Blackstock
s.n. (MTMG), (AY757624, AY757684, AY757552); C. lanceolata Boott,
JAPAN: Honshu, Okayama Pref., Maniwa-gun, Myoren, Waterway 2004.206
(MTMG), DQ998924, DQ998871, DQ998977; C. pedunculata Muhl. ex
Willd., CANADA: Quebec, Hudson, Waterway 2000.001 (MTMG),
(AY757623, AY757683, AY757551); sect. Collinsiae (Mack.) Mack., C.
collinsil Nutt., New Jersey: Bass River State Forest, Waterway
98.086 (MTMG), (AY757616, AY757677, AY757543); sect. Confertiflorae
Franch., C. brownii Tuckerm., JAPAN: exhort Okayama Univ. of
Science, Waterway 2004.231 (MTMG), DQ998904, DQ998851, DQ998957; C.
dispalata Boott, JAPAN: Honshu, Okayama Pref., Maniwa-shi, Myoren,
Waterway 2004.198 (MTMG), DQ998909, DQ998856, DQ998962; C.
ischnostachya Steud., JAPAN: Honshu, Kyoto Pref., Kyoto,
Yoshidayama, Waterway 2004.257 (MTMG), DQ998922, DQ998869,
DQ998975; sect. Depauperatae Meinsh., C. depauperata Curt. ex
With., (I) UNITED KINGDOM: England, exhort Godalming, Surrey, UK
garden, exhort Edge Hill, B. Phillips s.n. (MTMG) (AY757621,
AY757549) (2) UNITED KINGDOM, England, Rich 01 (OXF) (AY241985);
sect. Glaucescentes Reznicek, C. joorii L.H. Bailey, USA: Alabama,
Macon Co., Waterway 2000.054 (MTMG), DQ998923, DQ998870, DQ998976;
sect. Granulares (O. Lang) Mack., C. granularis Muhl. ex Willd.,
USA: Virginia, Montgomery Co., Blacksburg, Waterway 2000.095
(MTMG), DQ998919, DQ998866, DQ998972; sect. Griseae (L. H. Bailey)
Kirk., C. oligocarpa Willd., U.S.A.: Illinois, Union Co., Waterway
98.030 (MTMG), (AY757615, AY757676, AY757542); sect. Hallerianae
(Ascherson & Graebner) Rouy, C. dasycarpa Muhl., USA: Alabama,
Holmes Co., T. Smith ALHODa5 (MTMG), DQ998907, DQ998854, DQ998960;
sect. Hirtifoliae Reznicek, C. hirtifolia Mack., USA: Illinois,
Union Co., Waterway 98.029 (MTMG), (AY757611, AY757672, AY757538);
sect. Hymenochlaenae (Drejer) L. H. Bailey, C. arctata Boott,
CANADA: Quebec, Mont St. Hilaire, T Eades 004.2004 (MTMG),
DQ998900, DQ998847, DQ998953; C. cherokeensis Schwein., USA:
Florida, Holmes Co., Waterway 2000.044 (MTMG), (AY757619, AY757680,
AY757546); C. debilis Michx., USA: North Carolina, Jackson Co.,
Waterway 2002.018 (MTMG), (AY757608, AY757669, AY757535); C.
gracillima Schwein., CANADA: Quebec, Mont St. Hilaire, T. Eades
01.2004 (MTMG), DQ998918, DQ998865, DQ998971; C. mendocinensis
Olney ex W. Boott, USA: California, Mendocino Co., Waterway 99.036
(MTMG), (AY757609, AY757670, AY757536); C. obispoensis Stacey, USA:
California, San Luis Obispo Co., Roalson 1413 (RSA), (AY757620,
AY757681, AY757547); C. prasina Wahl., USA: Virginia, Rockbridge
Co., Waterway 2000.080 (MTMG), (AY757593, AY757654, AY757520);
sect. Lamprochlaenae (Drejer) L. H. Bailey, C. glacialis Mack.,
CANADA: Quebec, 25 km N of Schefferville, Waterway 2001.114 (MTMG),
(AY757625, AY757685, AY757553); sect. Laxiflorae (Kunth) Mack., C.
albursina E. Sheldon, USA: Illinois, Jackson Co., Waterway 98.050
(MTMG), (AY757626, AY757686, AY757554): C. blanda Dewey, USA:
Illinois, Jackson Co., Waterway 98.044 (MTMG), (AY757627, AY757687,
AY757555); sect. Limosae (Heuffel) Meinsh., C. limosa L. CANADA:
Quebec, Chisasibi, C. Novo 1.15 (MTMG), (AY757595, AY757656,
AY757522); C. macrochaeta C. A. Mey., USA: Alaska, Glen Alps, near
Anchorage, J. Dragon 03-74 (VT), DQ998931, DQ998878, DQ998984; C.
magellanica Lain. subsp, irrigua (Wahl.) Hiitonen, CANADA: Quebec,
Schefferville region, Waterway 97.090 (MTMG), (AY757594, AY757655,
AY757521 ); sect. Lupulinae J. Carey, C. grayi J. Carey, USA:
Illinois, Jackson Co., Waterway 98.036 (MTMG), (AY757580, AY757642,
AY757507); C. intumescens Rudge, USA: South Carolina, Monticello,
Waterway 2000.014 (MTMG), (AY757579, AY757641, AY757506); C.
lupulina Muhl. ex Willd., CANADA: Quebec, Hull, Lac Leamy, Waterway
97.127 (MTMG), (AY757576, AY757638, AY757503); sect. Mitratae G.
Don, C. fernaldiana H. Levet Vaniot, JAPAN: Honshu, Gunma Pref.,
Usui-gun, Matsuida-cho, Waterway 2004.269 (MTMG), DQ998913,
DQ998860, DQ998966; C. foliosissima F. Schmidt, JAPAN: Honshu,
Kyoto Pref., Ashiu Forest, Waterway 2004.239 (MTMG), DQ998916,
DQ998863, DQ998969; sect. Molliculae Ohwi, C. doniana Spreng.,
JAPAN: Honshu, Hyogo Pref., Mt. Hyounosen, Waterway 2004.301
(MTMG), DQ998910, DQ998857, DQ998963; C. mollicula Boott, JAPAN:
Honshu, Hyogo Pref., Mt. Hyounosen, Waterway 2004.299 (MTMG),
DQ998933, DQ998879 DQ998986; sect. Paludosae G. Don, C.
acutiformiss Ehrh., UNITED KINGDOM: England, exhort Edge Hill,
source: Lancashire, Silverdale, N. Blackstock s.n. (MTMG)
(AY757583, AY757644, AY757510); C. lasiocarpa Ehrh., USA:
Washington, Chelan Co., Fish Lake, Waterway 97.061 (MTMG),
DQ998925, DQ998872, DQ998978; C. pumila Thunb., JAPAN: Hokkaido,
Nemuro-cho, Lake Furen, Waterway 2004.322 (MTMG), DQ998943,
DQ998889, DQ998996; (7. riparia Curtis, UNITED KINGDOM: England,
Warwickshire, Kenilworth Castle, N. Blackstock s.n. (MTMG),
(AY757571, AY757633, AY757498); C. vestita Willd., USA: New
Hampshire, Rockingham Co., Waterway 2001.088 (MTMG), (AY757581,
AY757643, AY757508); sect. Paniceae G. Don, C. biltmoreana Mack.,
USA: North Carolina, Jackson Co., Waterway 2002.019 (MTMG),
DQ998902, DQ998849, DQ998955; C. filipes Franch. & Sav., JAPAN:
Honshu, Nagano Pref., Karuizawa-cho, Waterway 2004.289 (MTMG),
DQ998914, DQ998861, DQ998967; C. laxa Wahlenb., JAPAN: Hokkaido,
Akkeshi-cho, near Homakaigawa River, Waterway 2004.349 (MTMG),
DQ998928, DQ998875, DQ998981: C. livida (Wahl.) Willd., USA: New
Jersey, Burlington Co., Waterway 98.078 (MTMG), (AY757628,
AY757688, AY757556): C. panicea L., UNITED KINGDOM: England, New
Bridge, Dartmoor Natl. Park, Ashton 12Sep2000 (MTMG), DQ998937,
DQ998883, DQ998990; C. parciflora Boott, JAPAN: Honshu, Hyogo Pref,
Mr. Hyounosen, Waterway 2004.300 (MTMG), DQ998939, DQ998885,
DQ998992: C. vaginata Tausch, CANADA: Labrador, ca. 12 km E of
Schefferville, Waterway 97,085 (MTMG), (AY757629, AY757689,
AY757557); sect. Phacocystis Dumort., C. gynandra Schwein., CANADA:
Quebec, Mont St. Hilaire, Waterway 99.004 (MTMG), DQ998920,
DQ998867, DQ998973; C. nigra (L.) Reichard, UNITED KINGDOM:
England, exhort Edge Hill, originally from nr. Clitheroe,
Lancashire, M. Dean s.n. (MTMG), DQ998934, DQ998880, DQ998987;
sect. Phyl1ostachyae Tuckerm. ex Kuk., C. backii Boott, CANADA:
Quebec, Mont St. Hilaire, Waterway 98.003 (MTMG), (AY757402,
AY757398, AY757494); sect. Pictae Kuk., C. picta Steud., USA:
Alabama, Winston Co., Waterway 2002.053 (MTMG), DQ998941, DQ998887,
DQ998994; sect. Porocystis Dumort., C. pallescens L., CANADA:
Quebec, Lac Memphremagog, Y. Berube 99.019 (MTMG), (AY757612,
AY757673, AY757539); C. swanii (Fern.) Mack. (1) USA: Illinois,
Pope Co., Waterway 98.024 (MTMG), (AY757603, AY757530); (2) USA:
Virginia, Floyd Co., Waterway 2000.134 (MTMG) (AY757664); sect.
Racemosae G. Don, C. heteroneura W. Boott, USA: California, Lassen
Co., Waterway 2000.151 (MTMG), DQ998921, DQ998868, DQ998974; C.
media R. Br. in Richardson, USA: Alaska, Bonanza Creek, S. Mills
97.03 (MTMG), DQ998932, DQ998898, DQ998985; C. stylosa C. A. Meyer,
CANADA: Quebec, Schefferville region, Waterway 97.095 (MTMG),
(AY757591, AY757652, AY757518); sect. Rhomboidales Kuk., C.
boottiana Hook. & Arn., JAPAN: cultivated at Okayama Univ. of
Science, originally from Kyushu, Kagoshima Pref., Satamisaki,
Waterway 2004.233 (MTMG), DQ998903, DQ998850, DQ998956; C. laticeps
C. B. Clarke ex Franch., JAPAN: Honshu, Okayama Pref., exhort
Okayama Univ. of Science, Waterway 2004.232 (MTMG), DQ998926,
DQ998873, DQ998979; C. papillaticulmis Ohwi, JAPAN: Honshu, Kyoto
Prof., Ashiu Forest, Waterway 2004.238 (MTMG), DQ998938, DQ998884,
DQ998991: C. subdita Ohwi, JAPAN: Honshu, Okayama Pref., Aidagun,
Yoshida, Waterway 2004.237 (MTMG), DQ998948, DQ998894, DQ999001;
sect. Rhynchocystis Dumort., C. pendula Hudson, UNITED KINGDOM:
England, Devon, Slapton Ley Field Centre, S. Watson-Jones s.n.
(MTMG), (AY757600, AY757661, AY757527); sect. Rostrales Meinsh., C.
folliculata L., USA, New Jersey, Burlington Co., Waterway 98.094
(MTMG), (AY757601, AY757662, AY757528); C. michauxiana Boeck.,
CANADA: Quebec, Mont Tremblant, Gold & Pushkar 22 (MTMG),
(AY757602, AY757663, AY757529); sect. Scirpinae (Tuckennan) Kuk.,
C. scirpoidea Michx., CANADA: Quebec, 25 km N of Schefferville,
Waterway 2001.113 (MTMG), EF014489 (AY757582, AY757509); sect.
Shortianae (L. H. Bailey) Mack., C. shortiana Dewey, USA: Illinois,
Pope Co., Waterway 98.023 (MTMG), (AY757586, AY757647, AY757513);
sect. Siderostictae Franch., C. pachygyna Franch. & Say., JAPAN:
Honshu, Okayama Pref., Okayama-shi, Kakehata, Waterway 2004.225
(MTMG), DQ998936, DQ998882, DQ998989; C. siderosticta Hanee, JAPAN:
Honshu, Gunma Pref., Usui-gun, Matsuida-cho, Waterway 2004.268
(MTMG), DQ998946, DQ998892, DQ998999: sect. Spirostachyae (Drejer)
L. H. Bailey, C. punctata Gaudin, UNITED KINGDOM: England, exhort
Sandy Hills Bay, Dumfries & Galloway, exhort Edge Hill, C. Smith
s.n. (MTMG), (AY757598, AY757659, AY757525); sect. Squarrosae J.
Carey, C. squarrosa L., USA: Illinois, Pope Co., Waterway 98.020
(MTMG), (AY757587, AY757648, AY757514); C. typhina Michx., USA:
South Carolina, Manchester State Forest, Waterway 2000.016 (MTMG),
(AY757588, AY757649, AY757515); sect Sylvaticae Rouy, C. sylvatica
Huds., SWITZERLAND: forest near Basel, Lechowicz s. n. (MTMG),
(AY757599, AY757660, AY757526); sect. Thuringiaca G. Don, C. flacca
Schreber, UNITED KINGDOM: England, exhort Edge Hill originally from
Ainsdale Local Nature Reserve, Merseyside (MTMG), DQ998915,
DQ998862, DQ998968; sect. Vesicariae (Heuffel) J. Carey, C. comosa
Boott, CANADA: Quebec, Iberville, St. Armand, Y. Berube 99.035
(MTMG), (AY757575, AY757637, AY757502); C. hystericina Muhl. ex
Willd. USA: Virginia: Montgomery Co., Waterway 2000.096 (MTMG),
(AY757574, AY757636, AY757501); C. oligosperma Michx., CANADA:
Quebec, Schefferville region, Waterway 2002.091 (MTMG), (AY757578,
AY757640, AY757505); C. retrorsa Schwein., CANADA: Quebec, Hull,
Lac Leamy, Waterway 97.125 (MTMG), (AY757577, AY757639, AY757504);
C. tuckermanii Dewey, CANADA: Quebec, Hull, Lac Leamy, Waterway
97.128 (MTMG),(AY757573; AY757635, AY757500); subg. Psyllophora
(Degl.) Peterm. (= subg. Primocarex Kuk.) sect. Dornera Heuff., C.
nigricans C.A. Meyer, CANADA: British Columbia, Mount Revelstoke
National Park, Ford 9720, (WIN) (AY242042, AY242043); (2)
(AF164929); sect. Leptocephalae L.H. Bailey, C. leptalea Wahlenb.,
USA: Maine, Oxford Co., Waterway 2001.099 (MTMG), (AY757630,
AY757690, AY757559); Co pauciflora Lightf., CANADA: Quebec, 20 km N
of Schefferville, Waterway 2002.098 (MTMG), (AY757631, AY757691,
AY757569); sect. Psyllophora (Degl.) Koch, C. pulicaris L., UNITED
KINGDOM: England, Yorkshire Dales National Park, Starr 98001 &
Scott, (FHO) (AY242018, AY242019, AY757563); sect. Rupestres
(Tuckerm.) Meinsch., C. rupestris, FRANCE: Col de Galibier,
Playford 9801 (FHO), (AY244521, AY244522); (2) (AF164934);

subg. Vignea (P. Beauv. ex Lestib. f.) Peterm.

sect. Chordorrhizae (Heuffel) Meinsh., C. chordorrhiza L.f.,
CANADA: Quebec, Schefferrville region, Waterway 2001.107 (MTMG),
(AY757409, AY757389, AY757485); sect. Curvulae Tuckerm. ex Kuk., C.
curvula All., FRANCE: Col du Galibier, Playford 9803 et al., (FHO)
(AY242030, AY242031, AY757564); sect. Deweyanae (Tuckerm. ex Mack.)
Mack., C. bromoides Schkuhr ex Willd., CANADA: Quebec, Mont St.
Hilaire, Waterway 98.004 (MTMG), (AY757404, AY757378, AY757474); C.
deweyana Schw., CANADA: Quebec, Mont St. Hilaire, Waterway 98.005
(MTMG), (AY757412, AY757379, AY757475); sect. Foetidae (Tuckerm. ex
L.H. Bailey) Kuk., C. maritima Gunnerus, CANADA: Yukon, Kluane
Lake, Waterway 96.098 (MTMG), (AY757421, AY757397, AY757493); sect.
Gibbae Kuk., C. gibba Wahlenb., JAPAN: Honshu, Kyoto Pref., Kyoto
Univ. Campus, Waterway 2004.259 (MTMG), DQ998917, DQ998864,
DQ998970; sect. Glareosae G. Don, C. canescens L., CANADA: Quebec,
Mont Tremblant, A. Bond s.n. (MTMG), (AY757406, AY757384,
AY757480); C. heleonastes L.f., CANADA: Quebec, Schefferville
region, Waterway 97.078 (MTMG), (AY757418, AY757388, AY757484); C.
trisperma Dewey, CANADA: Quebec, Duhamel near Lac Dore, Y Berube
99.032 (MTMG), (AY757429, AY757387, AY757483); sect. Heleoglochin
Dumort., C. appressa R. Br., NEW ZEALAND: exhort. Auckland
University Campus, Waterway 2004.007 (MTMG), DQ998899, DQ998846,
DQ998952; C. decomposita Muhl., USA: South Carolina, Manchester
State Forest, Waterway 2000.011 (MTMG), (AY757411, AY757376,
AY757472); C. diandra Schrank, JAPAN: Hokkaido, Kushiro Mire,
Waterway 4009 (MTMG), (AY757413, AY757377, AY757473); C. secta
Boott, NEW ZEALAND: ex hort. Auckland Regional Botanic Garden,
Waterway 2004.021 (MTMG), DQ998945, DQ998891, DQ998998; sect.
Holarrhenae (Doell) Pax, C. pseudocuraica F. Schmidt, JAPAN:
Hokkaido, Nemuro-cho, NW of Tomochiri, Waterway 2004.334 (MTMG),
DQ998888, DQ998995, DQ998942; sect. Macrocephalae Kuk., C.
macrocephala Willd. ex Spreng., JAPAN: Hokkaido, Nemuro-cho, Lake
Furen, Waterway 2004.320 (MTMG), DQ998877, DQ998983, DQ998930;
sect. Multiflorae (J. Carey) Kuk., C. vulpinoidea Michx., USA:
California, Mendocino Co., Waterway 99.033 (MTMG), (AY757430,
AY757372, AY757468); sect. Ovales Kunth, C. bicknellii Britton,
CANADA: Quebec, cultivated in greenhouse, Waterway s.n. (MTMG),
(AY757403, AY757392, AY757488); C. projecta Mack., USA: Maine,
Oxford Co., Waterway 2001. 097 (MTMG),(AY757423, AY757391,
AY757487); sect. Phaestoglochin Dumort., C. radiata (Wahl.) Small,
CANADA: Quebec, Bale d'Urfe, Montreal, Waterway 99.006 (MTMG),
(AY757424, AY757396, AY757492); C. rosea Schkuhr ex Willld.,
CANADA: Quebec, Mont St. Hilaire, M. Lechowicz s.n. (MTMG),
(AY757425, AY757395, AY757491); C. sparganioides Muhl. ex Willd.,
CANADA: Quebec, Mont St. Hilaire, Waterway 2003.025 (MTMG),
DQ998947, DQ998893, DQ999000; sect. Physoglochin Dumort., C.
gynocrates Wormsk. ex Drejer, CANADA: Quebec, Schefferville region,
A. Dabros s.n. (MTMG), (AY757417, AY757383, AY757479); sect.
Remotae (Ascherson) C. B. Clarke, C. remota L., SWITZERLAND: NE of
Geneva, Dabros s.n. (MTMG), DQ998944, DQ998890, DQ998997; sect.
Stellulatae Kunth, C. echinata Murray, USA: Maine, Oxford Co.,
Waterway 2001.101 (MTMG), (AY757415, AY757381, AY757477); C. omiana
Franch. & Sav., JAPAN: Honshu, Okayama Pref., Maniwa-gun, Myoren,
Waterway 2004.197 (MTMG), DQ998935, DQ998881, DQ998988; sect.
Vulpinae (Heuffel) H. Christ, C. crus-corvi Shuttleworth, USA:
Illinois, Jackson Co., Waterway 98.037 (MTMG), (AY757410, AY757373,
AY757469); C. stipata Muhl. ex Willd., USA, California, Plumas Co.,
Waterway 99.072 (MTMG), (AY757426, AY757375, AY757471);

subg. Vigneastra (Tuck.) Kuk. (= subg. Indocarex (Baill.) Kuk.)

sect. Baccantes (T. Koyama) P.C. Li, C. baccans Nees, TAIWAN: Wu
Lai, Taipei, Yen 078, (WTU) (AF027449, AF027488 AY241994,
AF191814); sect. Indicae Tuckema., C cruciata Wahlenb., MALAYSIA:
Mulu National Park, Sarawak, Yen 075, (WTU) (AF027450, AF027489,
AY241995, AY757558); C. filicina Nees, TAIWAN: Yang Ming Shan
National Park, Da Tun Shan, Yen 0076, (WTU) (AY241996, AY241997);
(2) CHINA: Sichuan, (AF284879).

Cymophyllus Mack.

C. fraserianus (Ker-Gawler) Kartesz & Gandhi, (1) USA: Tennessee,
Blount Co., along road to Cades Cove, Sharp s.n. (cultivated at K),
Start 98024 ex RBG Kew (FHO) (AY241969, AY241970); (2) USA:
Tennessee, Carter Co., Waterway 2000.113 (MTMG), (AY757431,
AY757399, AY757495).

Kobresia Willd.

subg. Compositae (C. B. Clarke) Kukkonen, K. laxa Nees, INDIA:
Sikkim, North District, Long & Noltie s.n.. E.E.N.S. No. 211, (E)
(AY241975, AY241976); (2) (AF164943); subg. Kobresia sect.
Kobresia, K.

myosuroides (Viii.) Fiori, (1) FRANCE: Col du Galibier, Playford
9804 et al., (FHO) (AY242036, AY242037, AY757566); (2) (AF284985):
K. simpliciuscula (Wahlenb.) Mack., CANADA: British Colombia, Yoho
National Park, Ford 9710, (FHO) (AY241971, AY241972); (2)
(AF164948).

Schoenoxiphium Nees

S. filiforme Kuk., SOUTH AFRICA: Eastern Cape, Drakensbergs,
Phillipson 666, (PRE) (AY242020, AY242021); (2) SOUTH AFRICA:
Browning 699 (NU) (AF164951); S. lehmannii (Nees) Steud., SOUTH
AFRICA: Natal Province, Ngoye Forest Reserve, Williams 1007, (PRE)
(AY242026, AY242027, AY757560); S. sparteum (Wahlenb.) C. B.
Clarke, SOUTH AFRICA: Orange Free State, Ladybrand, De Lange FA 57,
(PRE) (AY242022, AY242023, AY757561).

Uncinia Pets.

subg. Eu-Uncinia Kuk. sect. Platyandrae C. B. Clarke, U. phleoides
(Cav.) Pers., CHILE: Isla Grande de Chiloe, P. N. de Chiloe, Vann
9801, (FHO) (AY012670, AY012671); (2) CHILE: Hortus Botanicus
Valdiviensis (WTU) (AF164931). U. uncinata Kuk., NEW ZEALAND: North
Island, Auckland Ecological Region, P. de Lange s.n., (AY242054,
AY244543); (2) U.S.A.: Hawaii, K. Millam s.n. (WTU), (AF164932).

Outgroups

Dulichium arundinaceum (L.) Britton, CANADA: Ontario, Cooper Marsh,
S. Lancaster, Waterway 2003.052 (MTMG), DQ998949, DQ998895,
DQ999002; Eriophorum angustlfolium Honck., CANADA: Quebec, Squaw
Lake, Schefferville region, Waterway 2001.118 (MTMG), DQ998950,
DQ998896, DQ999003; Eriophorum vaginatum L., (1) UNITED KINGDOM:
England, Start 98007 and Scott, (FHO) (AY242008, AY242009) (2)
CANADA: Quebec, Schefferville region, Waterway 2002.094, (MTMG),
(AY757692). Trichophorum alpinum (L.) Pers., CANADA: Quebec,
Schefferville region, Waterway 2001.110 (MTMG), (AY757432,
AY757400, AY757496); Trichophorum cespitosum (L.) Hartm., CANADA:
Quebec, Schefferville, Dabros s.n. (MTMG), DQ998951, DQ998897,
DQ999004.

Species classified in tribe Cariceae are arranged alphabetically
within generic, subgeneric and sectional groups, followed by the
six outgroup species in alphabetical order. Generic delimitation
follows Kukenthal (1909) and Ball et al. (2002), while subgenera
follow the circumscriptions of Kukenthal (1909) and Zhang (2001),
except where modified by Egorova (1999). Sectional placement
follows Ball et al. (2002) for North American and circumboreal
species, Egorova (1999) for Eurasian species, Dai & Liang (2000)
and Hoshino et al. (2002) for East Asian species, and Zhang (2001)
for Kohresia. GenBank numbers representing sequences from Waterway
and Starr (2007), Starr et al. (1999, 2003, 2004, 2008), Yen and
Olmstead (2000), or Roalson et al. (2001) are given in parentheses.
Locality, collector with number, and herbarium acronym (Holmgren et
al., 1990) are reported where possible. GenBank accession numbers
are ordered as ITS, ETS-1f, trnL-trnF. Individuals of the same
species, sampled from different localities are numbered (1) and
(2). Generic, subgeneric, and species names are shown in bold

Table 2 Characteristics of the Three Gene Regions Used in the Analysis

Character set Aligned Ambiguous Variable Parsimony-
 length sites (#) sites (#) informative
 (bp or #) sites (#)

ETS1f nucleotides 688 10 460 359
ETS1f indels 113 8 105 57
ITS nucleotides 729 14 309 245
ITS indels 99 15 84 41
trnL nucleotides 1,453 20 389 220
trnL indels 165 10 155 66
Total 3,247 57 1,502 988

The ITS region includes intergenic spacers ITS 1 and ITS2 and the 5.8S
nuclear ribosomal gene. The trnL region includes the trnL intron, 51
by of the trnL 3' exon, and the trnL-trnF intergenic spacer.
Ambiguous regions were removed from the data set prior to analysis and
are not included in the numbers of variable and parsimony-informative
characters
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Article Details
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Author:Waterway, Marcia J.; Hoshino, Takuji; Masaki, Tomomi
Publication:The Botanical Review
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2009
Words:9937
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