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Systematics and Phytogeography |
Museum of New Zealand Te Papa Tongarewa, P.O. Box 467, Wellington, New Zealand
Received for publication November 7, 2004. Accepted for publication June 2, 2005.
ABSTRACT
Species status cannot be adequately determined when partitions are based on only a single morphological character. For instance, the sympatry of plants with broad and narrow pinnules in the fern Asplenium hookerianum sensu lato from New Zealand creates the impression that two entities are present. The narrow-pinnuled plants are sometimes segregated as a distinct species, A. colensoi. However, this variation in pinnule morphology could equally be infraspecific, and only additional data can resolve this uncertainty. Analyses using AFLP DNA-fingerprinting and DNA sequencing of the chloroplast trnL-trnF region indicate that genetic variation in A. hookerianum sensu lato is not concordant with pinnule morphology. Consequently, the recognition of A. colensoi is not supported.
Key Words: AFLP • Aspleniaceae • Asplenium colensoi • Asplenium hookerianum • New Zealand • pinnule morphology • species taxonomy • trnL-trnF
The vast majority of species that have been described taxonomically are based completely on morphological data. Even with the advent of genetic analyses, which although powerful, are relatively laborious and expensive, the bulk of species' taxonomy in the foreseeable future is likely to have its foundations in morphology. Morphologically based species taxonomy can be straight-forward (and highly accurate) when individuals are concordantly partitioned into groups (i.e., species) by several assumedly independent characters. However, taxonomic decision-making is less clear for partitions based on variation in only a single character, even if the difference is discrete and state assignment unambiguous; are two separate species present, or just one polymorphic species?
The ferns Asplenium hookerianum Colenso and A. colensoi Colenso, published conjointly by William Colenso in 1845
, are just such an example of the difficulty of determining whether variation in a single morphological character is infra- or interspecific. In accordance with the morphology of the holotype specimens, these names have been used for plants with broad (hookerianum) or narrow (colensoi) pinnules (the ultimate segments of the frond). However, aside from this usually obvious difference in pinnule morphology (see later), little else appears to separate these plants. Consequently, their appropriate taxonomic status has been uncertain, and they have been variously retained as distinct species (Hooker, 1860
; Hooker and Baker, 1868
, 1874
; Crookes, 1963
) or treated as varieties of the same species (e.g., W. Hooker, 1854
; J. Hooker, 1854
; Moore, 1859
; Thomson, 1882
; Field, 1890
; Cheeseman, 1906
, 1925
; Dobbie, 1921
; Allan, 1961
). Asplenium hookerianum var. colensoi (Colenso) T. Moore is the correct varietal-level combination.
Recent treatments (e.g., Brownsey, 1977
, 1998
; Brownsey and Smith-Dodsworth, 1989
, 2000
) have formally recognized only Asplenium hookerianum, noting it to be a polymorphic and variable species, with the epithet colensoi being mentioned only in passing. However, the practice of contemporary New Zealand botanists is just as varied as earlier authors: some treat "hookerianum" and "colensoi" as distinct species, some regard them as varieties, while others recognize only A. hookerianum.
Broad-pinnuled hookerianum and narrow-pinnuled colensoi plants are both distributed throughout much of New Zealand. The former also occur in Australia, but are very rare (Brownsey, 1998
). In New Zealand, the broad-pinnuled hookerianum predominates, being the only morphology found at many sites, while it is rare for narrow-pinnuled colensoi plants to be present alone. In addition, the two morphologies are found together at many sites throughout New Zealand. In such sympatric instances, the broad-pinnuled hookerianum is usually the most abundant, no ecological separation is apparent, and the morphological differentiation typically provides a convincing impression of two discrete entities, between which there are few, or even no, morphological intermediates.
Field (1890)
and Cheeseman (1906)
referred to the occasional existence of plants with both broad-pinnuled and narrow-pinnuled fronds. We know of no large specimens that support this observation, although small, narrow-pinnuled colensoi plants sometimes have amongst their smallest fronds some tending towards the broad-pinnuled hookerianum morphology. It is not unusual to find at sympatric sites plants that appear to bear two discrete pinnule morphologies. However, on closer inspection these different pinnule morphologies are invariably revealed to arise from separate plants that are simply growing so close together that their fronds are entangled.
Here we quantify the differences between the hookerianum and colensoi pinnule morphologies. With the aim of extending the analysis of their taxonomic status beyond a single variable morphological character, we also test whether these pinnule morphologies are associated with genetic variation as assayed by AFLP DNA-fingerprinting (Vos et al., 1995
) and DNA sequencing of the chloroplast trnL-trnF region (Trewick et al., 2002
). If hookerianum plants from a particular site are more closely related not to colensoi plants with which they grow, but to hookerianum plants from other sites, and/or if this is also the case for colensoi plants, then the different pinnule morphologies might be taken to constitute distinct species.
MATERIALS AND METHODS
Morphology
The morphology of 212 specimens held by WELT (herbarium abbreviations follow Holmgren et al., 1990
) of A. hookerianum sensu lato (with rachises > 6.5 cm) was investigated. These were each determined by simple visual inspection to have either a colensoi, ambiguous, or hookerianum pinnule morphology. Then the width of the widest pinnule over 1 mm in length from the basal acroscopic secondary pinnae of the three most basal primary pinnae on one side of the frond was measured and averaged for each specimen.
AFLP DNA-fingerprinting
Plants were investigated from seven sites in New Zealand (Fig. 1, Table 1): Puhoi (Puh), Lake Opouahi (Opo), Monckton (Mon), Kaikoura (Kai), Banks Peninsula (Ban), Peel Forest (Pee), and Lake Hawea (Haw). Two samples with unambiguous hookerianum morphology and two with unambiguous colensoi morphology were sampled from each site, except for the Pee site from which only a single sample of each morphology was available and the northern Puh site where only the hookerianum morphology occurs. No samples were included from Australia because of the extreme rarity there of Asplenium hookerianum. The samples are referenced here in the format Opo-4H, denoting: the site, a unique number for that site, and their pinnule morphology (H = hookerianum; C = colensoi). Also included for comparison were 21 widely distributed samples of A. bulbiferum G. Forst., the nearest known tetraploid relative of A. hookerianum sensu lato (Perrie and Brownsey, 2005
; vouchers held at WELT, and collection details available from the corresponding author).
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, except primers with four selective bases were employed together with a more stringent selective-PCR protocol based on O'Hanlon and Peakall (2000
; 94°C for 2 min; 13 cycles of 94°C for 30 s, 65°C for 30 s, reducing by 0.7°C per cycle, and 72°C for 1 min; 25 cycles of 94°C for 30 s, 56°C for 30 s, and 72°C for 1 min; and finally 72°C for 3 min). The EcoRI selective primers were fluorescently labeled, and two selective primer combinations were used: EcoRI-ATAG (Fam label) and MseI-CTCG, and EcoRI-AATA (Vic label) and MseI-CTCG. For each sample, 0.33 µL from both 20 µL selective reactions were combined and visualized using a capillary ABI3730 Genetic Analyzer (Applied Biosystems, Foster City, California, USA). Peaks with fragment lengths between 50 and 500 base pairs in the resulting electropherograms were scored with Genemapper 3.0 (Applied Biosystems). Duplicate samples were included to assess reproducibility.
The program PAUP* 4.b10 (Swofford, 2002
) was used under a maximum parsimony criterion to conduct heuristic searches of the AFLP data, with tree-bisection-reconnection branch-swapping and 1000 random addition replicates. 1000 nonparametric bootstrap replicates, each with 10 random addition replicates, were used to evaluate bootstrap support (BS). Pertinent aspects of the phylogenetic analysis of AFLP data are discussed by Koopman et al. (2001)
, Perrie et al. (2003)
, and Goldman et al. (2004)
. In the present instance, if the broad-pinnuled hookerianum and narrow-pinnuled colensoi plants constitute different species, it might be expected that they would be recovered as separate groups in the parsimony analysis of the AFLP data. A further expectation is that this separation would have strong bootstrap support, resulting from the common hierarchical signal anticipated across characters when relationships are divergent, as is generally the case between species (Perrie et al., 2003
; see also Lindqvist et al., 2003
; Richardson et al., 2003
). The inclusion of A. bulbiferum, whose divergence from A. hookerianum sensu lato is not in doubt, acts as a "positive" control on our methodological approach.
An analysis of molecular variance (AMOVA) was also performed, using Arlequin 2.0 (Schneider et al., 2000
; significance assessed with 10 000 nonparametric permutations), with the A. hookerianum sensu lato samples grouped either by pinnule morphology or collection site. A substantial portion of the variation in the AFLP data set might be expected to be partitioned between the broad-pinnuled hookerianum and narrow-pinnuled colensoi plants if they represent separate species.
DNA sequencing
Aligned DNA sequences for the chloroplast trnL-trnF region (= trnL intron + trnL 3'-exon + trnL-trnF intergenic spacer) were obtained as described by Perrie and Brownsey (2004)
for the same 23 samples of A. hookerianum sensu lato analyzed by AFLP. GenBank accession numbers are listed in Table 1.
Relationships amongst the trnL-trnF haplotypes were assessed with an exhaustive search under a maximum parsimony criterion with PAUP* 4.b10 (prior to which, redundant sequences were identified and removed using MacClade 4.0; Maddison and Maddison, 2000
), and with the network methods implemented by SplitsTree 4.b4 (using split-decomposition and Hamming distances; Huson, 1998
; http://www-ab.informatik.uni-tuebingen.de/software/ jsplits/welcome_en.html) and TCS 1.17 (statistical parsimony; Clement et al., 2000
). Arlequin was used to conduct AMOVAs with the samples grouped either by morphology or site (10 000 permutations to assess significance).
RESULTS
Morphology
Examples of the hookerianum and colensoi pinnule morphology are given in Fig. 2. Of the 212 WELT specimens of A. hookerianum sensu lato, 149 were determined to have the broad-pinnuled hookerianum morphology, 58 the narrow-pinnuled colensoi morphology, and five were ambiguous. Pinnule width measurements of these plants indicated no quantitative discontinuity between those determined by eye as having hookerianum or colensoi morphology, but were clearly multimodal (Fig. 3).
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; Bonin et al., 2004
). Scoring of the A. hookerianum sensu lato samples produced 244 polymorphic AFLP characters, of which 184 were parsimony-informative. Maximum parsimony analysis of these data recovered three trees of 623 steps (CI = 0.39, RI = 0.51, RC = 0.20), one of which is shown in Fig. 4; the others differed in the arrangement of some of the Kai, Ban, and Pee samples (not shown). In none of these trees were the samples separated into two groups corresponding to those with hookerianum and colensoi morphologies. The few internal branches that received strong bootstrap support were mostly grouping samples from the same collection site. When a constraint was enforced to recover the two pinnule morphology groups separately, eight trees of 679 steps were recovered (CI = 0.36, RI = 0.44, RC = 0.16).
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When the A. hookerianum sensu lato samples were grouped by pinnule morphology, AMOVA partitioned 0% (P = 0.44) of the AFLP genetic variation between the two groups, and 100% within. When the samples were grouped by site irrespective of pinnule morphology, 29% (P < 0.0001) of the AFLP variation was partitioned between the seven sites, and 71% within.
DNA sequencing
Seven sites containing substitutions (one of these polymorphic sites had three different nucleotides) and one 4-bp microsatellite insertion were present within the chloroplast trnL-trnF DNA sequence region of the A. hookerianum sensu lato samples. These defined nine trnL-trnF region haplotypes. The microsatellite, found in Ban-2C and Ban-4C, was recoded as a substitution for the analyses.
Similar relationships between these haplotypes were inferred by maximum parsimony, statistical parsimony, and split-decomposition. However, the presence of three states at one polymorphic site introduces the possibility of incompatibility, which is only represented in the splits-graph (Fig. 5). SplitsTree depicts the three "splits" at the three-state site with branches of (arbitrary) length 0.5. One of these 0.5 length branches (that splitting Puh-1H, Opo-1H, Opo-3H, Pee-1H, Haw-1H, and all of the Mon samples from the remainder, which is not present in the maximum parsimony or statistical parsimony trees) is in conflict with the branch that splits Puh-1H, Haw-1H, all of the Opo samples, and all of the Mon samples from the remainder, and this incompatibility is represented by the box in Fig. 5.
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DISCUSSION
No absolute discontinuity was found in the measurements of pinnule width in A. hookerianum sensu lato, which is also manifested in the occasional presence of morphological intermediates at some sympatric sites (sometimes interpreted as hybrids: e.g., in schedula AK 220462, WELT P9728). Nevertheless, the measurements of pinnule width are clearly multimodal, and support field observations that the majority of specimens can be readily assigned to either broad-pinnuled hookerianum or narrow-pinnuled colensoi morphologies. This is consistent with the idea that two species may be present.
However, the samples of A. hookerianum sensu lato are not grouped by pinnule morphology in either of the AFLP DNA-fingerprinting or the chloroplast trnL-trnF DNA sequence data sets. Constraining the two pinnule-morphology groups to be separate in the maximum parsimony analysis of the AFLP data adds 56 steps (c. 9%). This increase seems considerable, but its statistical significance cannot (unfortunately) be assessed with Kishino-Hasegawa or Templeton tests because the most parsimonious trees were only identified a posterioi (Goldman et al., 2000
). In contrast to the lack of separation between the A. hookerianum sensu lato pinnule-morphologies, these analyses do recover the A. bulbiferum samples as a distinct group, and with strong (100%) bootstrap support. As with the AFLP data, there is no separation of the pinnule-morphology states in the tree and network analyses of the trnL-trnF sequence data. Further, the AMOVA analyses indicate that site of origin, irrespective of pinnule-morphology, provides a much better explanation of the genetic variation than pinnule-morphology in both the AFLP (29% cf. 0%) and trnL-trnF (58% cf. 3%) data sets.
Although our genetic sample set is small, it does encompass a considerable area in which broad-pinnuled hookerianum and narrow-pinnuled colensoi plants occur together. It seems very unlikely that the addition of more samples (including those from Australia, where only broad-pinnuled plants occur) would change our findings that genetic variation in A. hookerianum sensu lato is not concordant with pinnule morphology. Indeed, the AMOVAs clearly indicate that the assayed genetic variation is more strongly associated with geography than pinnule morphology; that is, plants from the same site, irrespective of their pinnule morphology, are generally more closely related to one another than they are to plants with the same pinnule morphology from other sites.
Consequently, we believe there is no justification for recognizing the narrow-pinnuled colensoi plants as a distinct species. Rather, A. hookerianum sensu lato is a striking example of a polymorphic species that has two discrete pinnule morphologies at many sites where it occurs. (This differentiation is not so apparent when morphological variation across many localities is taken into account; Fig. 3).
Infraspecific recognition of the narrow-pinnuled colensoi plants may be appropriate, if only to clearly denote that this obvious morphological variation is not associated with a specific boundary. The combination A. hookerianum var. colensoi already exists, but, even within the localized context of New Zealand, the definition of the taxonomic rank of variety is so variable and ambiguous that it renders the entities delimited as varieties difficult to interpret and compare. However, the pinnule variation in A. hookerianum sensu lato, being sympatric and infraspecific, is akin to recent New Zealand cases resolved at the level of forma [e.g., Hebe amplexicaulis (J.B. Armstr.) Cockayne et Allan f. hirta Garn.-Jones et Molloy (Garnock-Jones and Molloy, 1982
); Mazus novaezeelandiae W.R. Barker subsp. impolitus Heenan f. hirtus Heenan (Heenan, 1998
); Xeronema callistemon W.R.B. Oliv. f. bracteosa (L.B. Moore) de Lange et E.K. Cameron (de Lange and Cameron, 1999
)]. Nevertheless, we resist making a new combination for the narrow-pinnuled colensoi plants at the rank of forma until a greater consistency in the application of the varietal and forma ranks is achieved.
The frequent close proximity of plants with broad-pinnuled hookerianum and narrow-pinnuled colensoi morphology indicates that their difference does not have a simple environmental cause and that there is probably a genetic component to the morphological variation in A. hookerianum sensu lato (albeit one not associated with a species boundary). It may be comparable to the allelic variation at a single gene reported in Scottish populations of the fern Athyrium distentifolium Opiz by McHaffie et al. (2001)
. However, other than anecdotal reports that the narrow-pinnuled colensoi state breeds true from spore, the actual genetic basis of pinnule variation in Asplenium hookerianum sensu lato has not been investigated. Any explanation will also need to account for occasional narrow-pinnuled analogues in the octoploid A. gracillimum Colenso, which have at times been referred to as A. bulbiferum var. tripinnatum Hook. f. (e.g., Crookes, 1963
; although incorrectly in view of the type of the latter name). Asplenium gracillimum is seemingly an allo-octoploid of the tetraploids A. bulbiferum and A. hookerianum (Perrie and Brownsey, 2005
) and may have inherited the propensity for pinnule variation from the latter.
The parsimony analysis of the AFLP data suggested that the two plants with narrow-pinnuled colensoi morphology sampled at each of the Ban, Haw, and Opo sympatric sites were particularly closely related (cf. strong bootstrap support and short terminal branches; see Fig. 4). This is possibly a reflection of the relative rarity of this morphology at these sites. Hence, if pinnule variation is indeed genetically based, pairs of plants with the colensoi morphology will tend to share more recent ancestry than is the case for randomly selected pairs from the population as a whole (where the pairs will be mostly of two plants with the more abundant hookerianum morphology).
Our sample set was designed to test the species status of the broad-pinnuled and narrow-pinnuled plants, rather than to assess the population genetics of A. hookerianum sensu lato. Nevertheless, substantially greater population structuring is evident in the AMOVA of the trnL-trnF chloroplast sequence than in that of the AFLP nuclear genome data (58% vs. 29% variation partitioned between populations). Although homosporous fern spores contain both the chloroplast and nuclear genomes, spore immigrants alighting in established gametophyte populations may be inclined to maleness, particularly in species with antheridiogen systems. If the chloroplast is maternally inherited, as reported for one European species of Asplenium (Vogel et al., 1998
), any such male-predisposition for immigrant spores would reduce the effective dispersibility of the chloroplast relative to the nuclear genome and render population structuring lower in the latter. More detailed sampling of A. hookerianum and of other ferns would be desirable to test the generality of this pattern.
Much of the New Zealand flora appears to be of recent origin (Winkworth et al., 2002
), and few studies have detected substantial infraspecific DNA sequence diversity. Consequently, the chloroplast genetic variation found in A. hookerianum sensu lato presents an unusual opportunity for subsequent detailed investigation (e.g., Templeton, 2004
), particularly with respect to how the distributions of New Zealand's plants have been affected by the region's recent glacial history (McGlone et al., 2001
; Gardner et al., 2004
), a question which to date has received little phylogeographic study.
FOOTNOTES
1 The authors thank David Glenny and Matt Renner for assisting with the collection of samples, Lorraine Berry for helping with the fluorescent AFLP procedure, and Michael Bayly, David Glenny, and Peter de Lange for discussion of the variety and forma ranks. Helpful comments from anonymous reviewers and the editorial staff improved the manuscript. This work was funded by the New Zealand Foundation for Research, Science and Technology (contract MNZX0201). 
2 Author for correspondence (e-mail: leonp{at}tepapa.govt.nz
)
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