*Department of Biological Sciences, University of Alberta, Canada;
Department of Botany, University of Washington;
Department of Botany, University of Toronto, Canada
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Abstract |
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Introduction |
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The amount of signal that outgroups provide regarding the root location, and whether this reflects history or spurious long-branch problems, are addressed relatively rarely (see Stiller and Hall 1999
; Barkman et al. 2000
; Qiu et al. 2001
; Huelsenbeck, Bollback, and Levine 2002
, for recent examples). One recent theoretical framework, the Relative Apparent Synapomorphy Analysis (RASA)based methods of Lyons-Weiler, Hoelzer, and Tausch (1996
, 1998)
and Lyons-Weiler and Hoelzer (1997)
, provides a tree-independent approach for assessing the amount and quality of rooting signal. However, this general approach has recently attracted some criticism (see Simmons et al. 2002
). We do not address RASA-based methods here but instead explore some tree-based methods for examining different rooting possibilities when the unrooted ingroup topology is known with some confidence, as it is with the pickerelweed family, Pontederiaceae. There is substantial ambiguity in the location of the root of Pontederiaceae (Eckenwalder and Barrett 1986
; Kohn et al. 1996
; Barrett and Graham 1997
; Graham et al. 1998
), but the monophyly of the family is very robustly supported (Graham and Barrett 1995
), unrooted trees of this family are well corroborated by multiple, highly congruent lines of evidence from the chloroplast genome, and they find strong support from bootstrap analysis of the chloroplast data (Graham et al. 1998
). Rooting ambiguity thus appears to derive solely from a weakness in the rooting signal provided by the available outgroup sequences.
Recent studies indicate that this family of aquatic monocots has its closest living relatives among the commelinoid monocots, a very large and diverse array of taxa that includes the grasses, sedges, gingers, and palms (reviewed in Graham and Barrett 1995
). Several subtle nonmolecular characters indicate a relatively close relationship of Pontederiaceae with Haemodoraceae and Philydraceae (or both) (e.g., Simpson 1987
; Steinecke and Hamann 1989
; Tillich 1994
, 1995
; Givnish et al. 1999
), whereas various molecular studies suggest that Commelinaceae may be the sister-group to Pontederiaceae and that Hanguanaceae is related to all four families (e.g., Chase et al. 1995
, 2000
; Givnish et al. 1999
). The most recent classification scheme of the monocots (Chase et al. 2000
) includes these five families in the order Commelinales, as the sister-group of Zingiberales (the gingers and relatives; see also Stevenson et al. 2000
).
However, these higher-order relationships find only weak support from the available data. The five families of the Commelinales are all quite distinct from one another from morphological and molecular perspectives (e.g., Dahlgren, Clifford, and Yeo 1985
, pp. 149150, 323344, 374387; Duvall et al. 1993
), and estimates of their age based on rbcL data suggest that they diverged from one another in the late Cretaceous (Bremer 2000
). In the case of Pontederiaceae at least, this may predate substantially the diversification of the extant members of the family (see Barrett and Graham 1997
). This evolutionary distinctness may explain why numerous permutations of relationships among the members of Commelinales and relatives have been observed in phylogenetic studies based on different sets of taxa and various molecular and morphological markers (e.g., Chase et al. 1993
, 1995
, 2000
; Graham and Barrett 1995
; Davis et al. 1998
; Givnish et al. 1999
; Stevenson et al. 2000
; Neyland 2002
). Most of these data sets provide very poor bootstrap support for any particular relationship in the order, and they neither indicate strong support for the sister-group status of any particular taxon to Pontederiaceae nor of any particular root position within the family (Kohn et al. 1996
; Barrett and Graham 1997
; Graham et al. 1998
).
It is therefore of interest to ask how much signal the nearest outgroups provide for rooting Pontederiaceae, compared with those less closely related, and to investigate whether the optimal rootings determined using the nearest outgroups are a consequence of long-branch attraction. A related goal is to clarify the position of Pontederiaceae in monocot phylogeny. Several authors (e.g., Hillis 1996
; Graybeal 1998
; Soltis et al. 1998
; Swofford and Poe 1999
) have also noted that adding taxa and characters (or both) to a phylogenetic analysis can improve the accuracy of phylogenetic estimation, and so it would be valuable to address the extent to which adding data (genes or outgroups) improves our ability to assess where the root split of the family lies. We address these questions by sampling multiple outgroup taxa to Pontederiaceae for two chloroplast genes across a broad sample of monocots. Although our study focuses exclusively on this small family of commelinoid monocots, the insights gained from exploring rooting in this family are likely to be broadly applicable to any phylogenetic study where ambiguity in tree rooting may be a function of distantly related outgroups.
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Materials and Methods |
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Rooting Experiments
An unrooted, most-parsimonious topology of 24 taxa of Pontederiaceae derived from three chloroplast data sets (fig. 2 in Graham et al. 1998
) was chosen to perform a series of rooting experiments for real and random outgroup sequences using PAUP*. This unrooted tree is one of the ten most-parsimonious trees found using a chloroplast restriction-site data set (Kohn et al. 1996
) and is nearly identical in topology to trees inferred from a combined analysis of ndhF and rbcL (Graham et al. 1998
). The same topology was also inferred from parsimony analysis of various combinations of the three chloroplast data sets that included the restriction-site data set, and most branches on it were robustly supported by parsimony bootstrap analyses of the three data sets combined (Graham et al. 1998
).
Rooting experiments were performed using various outgroups (both individually and in combination) chosen to represent closely and distantly related taxa in the commelinoid monocots and elsewhere. Artificial outgroup sequences were also constructed to mimic real outgroups that have had their phylogenetic signal completely eroded by the passage of time. These random sequences were generated using MacClade version 3.07 (Maddison, W. P. and Maddison, D. R., 1992
), with base frequencies determined from a broad sample of monocots (A, 28%; C, 18%; G, 21%; T, 32%). No significant heterogeneity in base frequencies was detected across pairwise comparisons of the taxa (
2 = 25.73, P = 0.999, df = 144). A reduced two-gene matrix for Pontederiaceae comprising the characters variable in the family was appended to random sequences of the same length. These characters were considered because they all have the potential to be parsimony-informative in the context of data sets that include outgroup taxa.
One set of parsimony analyses was performed to explore the extent to which random outgroup sequences preferentially root on long branches. The unrooted topology of Pontederiaceae that we chose from Graham et al. (1998)
was enforced as a backbone constraint in a series of parsimony-based Branch-and-Bound searches that permitted individual random outgroups to attach to one or more optimal root position(s). The frequency of favored rootings on each branch in the unrooted ingroup topology was noted, with fractional scores assigned when a random sequence hit multiple optimal branches.
Variation in the degree of suboptimality across the possible roots for the ingroup topology was also assessed for a variety of real and random outgroup combinations. Tree scores for different rootings were estimated for individual random outgroups (maximum parsimony only) and using a variety of real outgroups (maximum parsimony and likelihood). The 45 possible roots of the 24-taxon ingroup topology were generated using the "All rootings" option in MacClade. The resulting NEXUS text files were edited to include different outgroup possibilities. For the parsimony analyses, tree scores for the different possible root positions were determined with all characters equally weighted and unordered. Models for the likelihood-based rooting analyses were chosen using the hierarchical likelihood ratio tests described in Huelsenbeck and Crandall (1997)
. The hierarchy of models tested was the same as the example given in Huelsenbeck and Crandall (p. 453; fig. 4), except that (1) the "General time-reversible" (GTR) model was substituted for the HKY85 model used there; (2) a model with a clock was not assessed; and (3) the final paired hypotheses compared here considered models with and without invariable sites.
Model parameters were estimated from the data using the unrooted topology of Pontederiaceae for the combined two-gene data set and also separately for each individual gene. These models and parameter estimates were used in all subsequent likelihood analyses that included the (real) outgroups. The models chosen using the likelihood ratio tests were the "GTR + + I" model for the rbcL data set and the combined rbcL and ndhF data set, and the "GTR +
" model for the ndhF data set (P < 0.01 for all significantly different comparisons with Bonferonni corrections performed; results not shown). The former model accommodates unequal base composition, the proportion of invariable characters (I), and nonuniform substitution rates within and between nucleotide characters (the GTR matrix was used to address uneven character-state transition rates, and the gamma [
] shape distribution parameter [
] was used to accommodate among-site rate variation); the latter model differs only by not directly accounting for invariable sites.
Evidence for the existence of historical signal in real outgroups concerning the position of the root of the ingroup tree has come from comparisons among real and random outgroup sequences of the decrease in parsimony observed between the optimal and next best rootings (Miyamoto and Boyle 1989
). We extend this logic by examining all suboptimal rootings for random outgroup sequences. For each outgroup sequence, parsimony scores for all possible rootings were compared with that of the optimal root. The resulting rooting penalties required to place the root in suboptimal locations (the score of the suboptimal root location minus score of the optimal root location) were ranked, with tied ranks being broken arbitrarily. The mean and standard deviation in the rooting penalty across the random outgroups for each rank were compared with the penalty for the corresponding rank for the real outgroups. For each real outgroup or outgroup combination considered here, Shimodaira-Hasegawa tests with RELL (resampling estimated log-likelihood) estimates of the test distribution (Shimodaira and Hasegawa 1999
and see Goldman, Anderson, and Rodrigo 2000
) were also performed to assess the null hypothesis that all 45 possible rootings of the Pontederiaceae subtree were equally good explanations of the data.
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Results |
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More than 70% of the "hits" by random outgroups were on the three longest branches within the unrooted ingroup, which range in length from 1620 steps under ACCTRAN optimization (these three branches attracted 16%, 20% and 35% of the hits, respectively; fig. 2
). Wheeler (1990)
predicted that the probability of a random sequence rooting on a given ingroup branch should be proportional to its length. This relationship holds for the terminal branches in figure 2
(correlation between length and number of hits: r = 0.743, P < 0.001, df = [24 terminal branches - 2] = 22). However, the relationship breaks down completely for the nonterminal branches (r = 0.331, P = 0.142, df = [21 - 2] = 19). Most nonterminal branches that were of the same order of length as the longest three had few or no hits from the random sequences sampled here (fig. 2
). These disfavored branches include the one preferred by the real outgroups under maximum parsimony (fig. 1
) and the neighboring branch favored under maximum likelihood for most outgroup combinations (see below). These two branches have a parsimony-based length of 15 and 6 steps, respectively, on the unrooted tree under ACCTRAN optimization. A range of other branches were also favored as optimal rooting locations by the random outgroup sequences, but each of these accounted for less than 5% of the total hits. In total, less than 10% of the branches favored as root locations by random outgroups occurred on nonterminal branches on the unrooted topology, despite their representing more than 40% of the total tree length and comprising half of the top ten branch lengths on the unrooted topology under ACCTRAN optimization.
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The same general patterns held in the likelihood analyses. Of those outgroup combinations examined, the experiment involving the composite Commelinales outgroup (Commelinaceae, Philydraceae, Haemodoraceae and Hanguanaceae) rejected a substantial fraction of suboptimal root locations (20 of 44 suboptimal roots; figs. 4 and 5 ; table 2 ). In general, the roots rejected by the different outgroup permutations considered here were also subsets of those rejected using the composite Commelinales outgroups and both genes combined (bracketed values in table 2 ). Some other outgroups performed as well as this or better (summarized in figs. 4 and 5 ; table 2 ), including one of the four Commelinales taxa when used individually as an outgroup family (Anigozanthos, representing Haemodoraceae). For the other three families of Commelinales (Commelinaceae, Hanguanaceae and Philydraceae, represented by Tradescantia, Hanguana and Philydrum, respectively), only a handful of candidate roots in Pontederiaceae could be rejected using the exemplar genera individually as outgroups (table 2 ). However, in combination, the exemplars from these families can reject as many or more branches as the four outgroups combined: one example, the combination of Commelinaceae and Hanguanaceae, is shown in figures 4 and 5 and table 2 .
Two of the most distantly related outgroup cases examined (Acorus by itself and the two representatives of Poaceae considered together) were not able to reject any root candidates (table 2 and fig. 4 ). The two Poaceae taxa are on relatively long branches within the commelinoid monocots (fig. 1 ), and Acorus is presumed to be the sister-group of the rest of the monocots here. However, one noncommelinoid outgroup case considered here (the two representatives of Asparagales taken together) was able to reject a substantial fraction of the root locations (13 of 20) rejected by the four outgroups used together (table 2 and fig. 4 ).
When the rooting experiment with the four Commelinales taxa was repeated using individual genes, a smaller subset of these candidate roots could be rejected than was possible with the two genes considered together (table 2 ). The penalties observed using each gene individually were nonetheless highly correlated to those observed using both genes together (table 2 ). A similarly strong correlation to this case was also seen with regard to rooting penalties for all permutations of outgroup taxa, genes, and optimality criteria considered. Thus, this correlation was apparent even where no or few roots could be rejected using likelihood (e.g., for the four Commelinales considered together but using rbcL alone, or for Acorus or Poaceae using both genes; table 2 ). In comparison to other outgroups, the slopes of the likelihood-penalty surface were flattest for the latter two cases (Poaceae and Acorus; fig. 4 ).
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Discussion |
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Signal and Bias in the Closest Relatives of Pontederiaceae for Rooting the Family
Poor support for the root of Pontederiaceae is not a function of uncertain relationships within the family because the two ingroup branches created at the root split using the real outgroups (fig. 1
) correspond to a single very strongly supported branch in the unrooted version of the tree (Graham et al. 1998
). This lack of robust rooting support is similar to that observed with random outgroups. To demonstrate this, a subset of random outgroup sequences were employed as outgroups in parsimony-based bootstrap analyses. For seven out of 10 random sequences examined, no single ingroup branch was favored by
50% of bootstrap replicates (results not shown). Support for the remaining three cases was in the 60%85% range, representing only moderately robust rootings by random outgroups. Thus, although long-branch attraction may influence rooting decisions in Pontederiaceae (fig. 2
), it is unlikely to result in a robustly supported wrong answer, at least at the current level of nucleotide sampling.
The comparable bootstrap support for rootings seen with real and random outgroups begs the question of whether any signal remains in the real outgroups for rooting Pontederiaceae. Comparisons of the degree of suboptimality of correspondingly ranked alternative rootings for real and random outgroup sequences demonstrate that the real outgroups do possess significant historical signal (fig. 3
). The idea of investigating the various rooting possibilities of outgroups on unrooted trees goes back to Lundberg (1972)
. This approach was recommended by Nixon and Carpenter (1993)
and Swofford et al. (1996)
when it is suspected that long branches connecting the ingroup and outgroups may distort the estimation of phylogenetic relationships within the ingroup, above and beyond uncertainty over the point of root attachment. Miyamoto and Boyle (1989)
were the first to explore the rooting potential of random outgroups (using "Lundberg rooting experiments") as a baseline for comparing the behavior of divergent real sequences. They cite Rohlf and Fisher (1968)
in this regard, but the latter authors used random sequences for a quite different purpose. Recent studies that examine the rooting potential of random versus real sequences include Sullivan and Swofford (1997)
and Stiller and Hall (1999)
. The parsimony-based test used here to assess rooting signal is based on the one suggested by Miyamoto and Boyle (1989)
, but we had to examine rootings substantially less optimal than the first suboptimal root to demonstrate phylogenetic signal among the real outgroups for rooting Pontederiaceae (fig. 3
).
Likelihood-based explorations of the possible rootings (table 2 and figs. 4 and 5 ) further confirm that many candidate root locations in the family are significantly poorer explanations of the data than the optimal cases (figs. 4 and 5 ). Both parsimony- and likelihood-based methods using the four closest outgroup families in tandem suggest that roughly half of all possible root locations within the family can be rejected with confidence by these outgroups.
Several lines of reasoning lend credence to the optimal roots favored by the real outgroups, despite their lack of robust support by bootstrap analysis or the Shimodaira-Hasegawa tests. First, the optimal roots favored by the real outgroups under maximum parsimony and likelihood (figs. 2
and 5
) are preferred by none of the random outgroups considered here (fig. 2
). Second, although real outgroups do not reject the three roots favored by most of the random outgroups, at an alpha level of 0.05, these rooting possibilities are generally not in the top 20% of rooting candidates favored by real outgroups (fig. 4
). Third, a substantial fraction of the homoplasy accumulated independently in different outgroups (that fraction of homoplasy not shared through common ancestry) should erode signal concerning the root of Pontederiaceae but in different ways in each terminal outgroup lineage. Although the signal that we detected was weak (sometimes to the point of not being able to reject any alternative rooting position), the pattern of rooting preference was still highly consistent among real outgroups (see the correlations listed in table 2
), despite these substantial and presumably independent opportunities in each lineage for the accumulation of misinformative characters (e.g., Swofford et al. 1996
), and for the loss of informative characters due to multiple hits. Because there has been little detectable erosion in the rooting correlations due to substitutions on the terminal Commelinales branches, it seems reasonable to assume that the rooting signal in toto among these outgroups has not been substantially biased by long-branch effects in the sense of Felsenstein (1978)
and Hendy and Penny (1989)
.
One previously published root of Pontederiaceae based on a restriction-site data set (Kohn et al. 1996
) was on a branch favored by many of the random outgroups (labeled "c" in fig. 2
). The possibility that this was an artifactual rooting was noted by Kohn et al. It has been suggested that restriction-site data generally have minimal utility at deeper levels of phylogenetic analysis (Olmstead and Palmer 1994
; Soltis and Soltis 1998
), and this may be the case with regard to outgroup-based rooting of Pontederiaceae. For the purposes of the evolutionary reconstructions that Kohn et al. were examining, their overall results did not differ markedly from those performed using the root indicated with the DNA sequence data (Kohn et al. 1996
; Barrett and Graham 1997
). However, even if root estimation has been nudged only slightly off course, this may reduce the utility of the phylogenetic inference in other reconstructions of character evolution, or for other purposes, such as the generation of classifications that better reflect phylogeny. Pursuing a more confident inference of root placement for Pontederiaceae is thus a crucial goal for future study.
Future Prospects
Using the four outgroup representatives in Commelinales as a composite outgroup was more useful for rejecting suboptimal roots than most of these outgroup families used individually (table 2
). For example, when exemplars representing Commelinaceae or Hanguanaceae were used individually, we were able to reject only a few suboptimal root positions. In combination however, the discriminatory power of these two families was among the very best of those examined (table 2
and figs. 4
and 5
). Breaking long branches by further addition of taxa should therefore improve our ability to infer the root of Pontederiaceae. This general result has been noted by many workers (e.g., Graybeal 1998
; Hillis 1998
). However, Smith (1994
; and see Hendy and Penny 1989
) pointed out that it is better to have a denser representation of outgroups in the sister-group than to sample heavily in less closely related taxa. Although we agree in principle that multiple taxa should be sampled in the sister-group (where practical or possible), sampling somewhat more distantly related taxa is important too because this should help break up the branch between the ingroup root and the sister-group.
Sampling outgroups beyond the sister-group serves a further purposeit helps test the idea that the sister-group really is the sister-group. It may not always be clear in advance what the sister-group is, as was the case here. The sequences examined here for the exemplar of Commelinaceae, the family suggested by previous molecular studies to be the sister-group of Pontederiaceae (e.g., Chase et al. 1995
) retained little robust signal when used individually to root the family, although they performed very well in combination with another poorly performing outgroup family (Hanguanaceae). Before we can add a denser sampling of taxa within the sister-group and other close relatives of Pontederiaceae, we need to more confidently identify the sister-group of the family. An ongoing study of commelinoid monocot phylogeny based on multiple genes is aimed at addressing this question. Preliminary results (S. W. Graham, unpublished data) provide extremely strong support for Haemodoraceae as the sister-group of Pontederiaceae (and intriguingly, the single representative of this family examined in the current study, Anigozanthos, rejected as many root positions as the four Commelinales outgroups combined; table 2
). Adding further genes should further improve our ability to reject suboptimal roots, as the combined discriminatory power of two genes was substantially greater than for either gene individually, in terms of the number of ingroup roots that could be rejected with confidence (table 2
).
Future taxon sampling within Pontederiaceae should focus on sampling those branches that could not be rejected with confidence. Currently unsampled members of Pontederiaceae are likely to place in sectors of the tree that have been rejected as rooting candidates here (see Barrett and Graham 1997
), and so these unsampled lineages are unlikely to include the point of attachment of the root. It is noteworthy that the candidate branches that cannot be rejected with confidence as points of attachment for the root of Pontederiaceae are largely restricted to the interior backbone of the unrooted tree. This backbone is generally strongly disfavored by random outgroup roots, suggesting that if the true root of a clade is to be found on its nonterminal branches (as may be the case here), long-branch attraction is unlikely to generate an artifactual rooting that suggests otherwise. The tendency observed here for random long-branches to disfavor interior parts of the unrooted tree, and to have no rooting preference on the interior backbone based on branch length, has not been noted previously. It would be valuable to explore this property in other phylogenies to determine if it is a widespread phenomenon.
Analytical Simplifications and Consequences
To facilitate tree-score estimation in a reasonable time frame, parameters for the likelihood model were estimated using the Pontederiaceae subtree only, and these values were used in all subsequent likelihood analyses. To investigate whether it would make a substantial difference to estimate model parameters directly, the Shimodaira-Hasegawa analyses were repeated for one of the outgroup cases (Philydrum, with both genes considered simultaneously), but with the "GTR + + I" model parameters estimated separately for each root position. Estimated model parameters (not shown) were neither found to differ substantially across rootings nor to those estimated using the Pontederiaceae subtree alone. The number and identity of significantly suboptimal roots according to the Shimodaira-Hasegawa tests were also found to be very similar to those obtained when parameters were derived from the Pontederiaceae subtree alone (results not shown). The use of this analytical shortcut therefore likely has little or no effect on our overall conclusions.
Appropriate corrections to significance levels are made in Shimodaira-Hasegawa's test to account for the multiple comparisons being performed (Goldman, Anderson, and Rodrigo 2000
), in our case across the 45 possible root positions. However, multiple sets of Shimodaira-Hasegawa tests were performed using different outgroup combinations, and it would also be valuable to correct the significance levels to take account of this level of hypothesis testing. However, because tests using related outgroups are likely to be strongly correlated (table 2
), adjusting the alpha-level to account for multiple tests is probably not appropriate, and it is not clear what the appropriate correction would be.
Goldman, Anderson, and Rodrigo (2000)
emphasize the importance of an honest choice of a priori hypothesis topologies to the conclusions generated using the Shimodaira-Hasegawa test. We erred on the side of being conservative here and considered all possible rooted versions of the unrooted topology of Pontederiaceae. However, the test assumes that the topologies considered include the true one (Goldman, Anderson, and Rodrigo 2000
), and our results should be viewed with the caveat that although the true, unrooted chloroplast phylogeny of Pontederiaceae is likely very similar in shape to the unrooted topology considered here, it is not guaranteed to be identical to it.
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Conclusions |
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Acknowledgements |
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Footnotes |
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Keywords: phylogenetic signal
rooted trees
unrooted trees
outgroup
Pontederiaceae
monocotyledons
long-branch attraction
Address for correspondence and reprints: Sean W. Graham, Department of Biological Sciences, CW405 Biological Sciences Centre, University of Alberta, Edmonton, Alberta, Canada T6G 2E9. swgraham{at}ualberta.ca
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