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The phylogenetic relationships among most metazoan phyla remainuncertain. We obtained large numbers of gene sequences frommetazoans, including key understudied taxa. Despite the amountof data and breadth of taxa analyzed, relationships among mostmetazoan phyla remained unresolved. In contrast, the same genesrobustly resolved phylogenetic relationships within a majorclade of Fungi of approximately the same age as the Metazoa.The differences in resolution within the two kingdoms suggestthat the early history of metazoans was a radiation compressedin time, a finding that is in agreement with paleontologicalinferences. Furthermore, simulation analyses as well as studiesof other radiations in deep time indicate that, given adequatesequence data, the lack of resolution in phylogenetic treesis a signature of closely spaced series of cladogenetic events.
Howard Hughes Medical Institute, Laboratory of Molecular Biology, R. M. Bock Labs, University of Wisconsin–Madison, 1525 Linden Drive, Madison, WI 53706, USA.
* Present address: The Broad Institute of MIT and Harvard, 320Charles Street, Cambridge, MA 02141, USA.
Present address: Departments of Bacteriology and Plant Pathology,University of Wisconsin–Madison, 420 Henry Mall, Madison,WI 53706, USA.
To whom correspondence should be addressed. E-mail: sbcarrol{at}wisc.edu
Detailed knowledge of the phylogenetic relationships among Metazoaand their eukaryotic relatives is critical for understandingthe history of life and the evolution of molecules, phenotypes,and developmental mechanisms. Currently, with the exceptionof the well-resolved phylogenetic history of the deuterostomes(1), the relationships between and within protostome and diploblasticmetazoan phyla remain unresolved (2–5). The uncertaintysurrounding metazoan relationships may result from analyticaland biological factors such as insufficient amounts of availablesequence data, mutational saturation, the occurrence of unequalrates of evolution between lineages, or the rapidity with whichmetazoan phyla diversified (3–7).
Recent investigations concerning two critical variables of phylogeneticexperimental design—the number of taxa and amount of dataused—have guided our approach to metazoan relationships.It has been shown that taxon number may not be as critical adeterminant of phylogenetic accuracy (8, 9) as the choice oftaxa (10). Thus, to investigate relationships among phyla atthe base of the metazoan tree and within protostomes, we selectedmetazoans and closely related eukaryotes that included representativesfrom choanoflagellates, poriferans (one representative fromeach of the three poriferan classes), cnidarians (one representativefrom each of two of the three cnidarian classes), platyhelminths(two representatives), priapulids, annelids, mollusks, arthropods,nematodes, urochordates, and vertebrates (three representatives)(all taxa are listed in table S1).
The use of single or few genes is now recognized to be insufficientfor the confident resolution of many clades (4, 11, 12). Incontrast, analyses of larger amounts of data have robustly resolvedrelationships in many taxonomic groups (11–14), even afterallowance for a high percentage of missing data (12–14).Thus, to increase resolution of metazoan relationships, we usedexperimental and bioinformatic approaches to assemble a datamatrix composed of 50 genes from the 17 selected taxa (15).Gene sequences from five key taxa were obtained through an automatedpolymerase chain reaction and sequencing approach we devisedfor the systematic amplification of large amounts of gene sequencedata from cDNA of any metazoan (15) (table S2). Gene sequencesfrom the 12 other taxa were retrieved through bioinformaticmeans from public databases (15).
A 50-gene data matrix does not resolve relationships among mostmetazoan phyla. Despite the large amount of data from taxa spanningthe Metazoa, analyses of this data matrix and subsets thereofunder maximum likelihood (ML) and maximum parsimony (MP) (15)still failed to resolve most relationships (Fig. 1 and fig.S1). There was no significant support (defined as >70% bootstrapsupport) for the order of relationships between early branchingmetazoans or within protostomes. Resolution of well-established"superclades" (protostomes, bilaterians, vertebrates, and deuterostomes;and metazoans with choanoflagellates as an outgroup) was attainedwith moderate to high support, depending on the optimality criterionused. The recovery of these superclades suggests that our failureto resolve relationships within them is either due to aspectsof our experimental design [such as systematic error artifactsresulting from violation of phylogenetic assumptions (16)] ormay reflect a prevailing limit to the resolution of certainclades in deep time.
Fig. 1. The lack of resolution in phylogenetic relationships among major metazoan phyla. Values above internodes correspond to support values from ML and MP analyses, respectively. Only internodes with significant support in at least one of the two analyses (ML and MP) or internodes present in majority-rule consensus trees of both analyses are drawn. Analyses were also performed by Bayesian inference (15) (fig. S1). Although certain analyses provided strong support for particular clades, analyses of different subsets of taxa produced significantly different and conflicting results (table S3).
[View Larger Version of this Image (32K GIF file)]
One recurrent problem for phylogenetic inference in deep timeis the phenomenon of long branch attraction (17), under whichunrelated taxa with long branches can artifactually be placedtogether. To test whether the inclusion of taxa with long branches[as visually identified on the ML tree (fig. S1)] had an effecton support values, we analyzed the data matrix, excluding long-branchedtaxa singly or in combination. For example, a clade joiningplatyhelminths and nematodes received moderate support, butall taxa in the clade are characterized by conspicuously longbranches (fig. S1). The removal of long-branched taxa had anegligible effect on support for most internodes (table S3).For example, although support for protostomes and bilateriansdid increase after the exclusion of nematode and platyhelminthtaxa, the resolution of nodes within these superclades was notimproved.
Clade support values can be very sensitive to the presence of"rogue" taxa whose placement on the tree may be unstable (17).To test whether the presence of rogue taxa could be responsiblefor the low support in many internodes of the metazoan phylogeny,the least stable metazoan taxa in this data matrix were identifiedusing leaf stability indices (15). Removal of these taxa hada negligible effect on support (table S3). Furthermore, testsof additional parameters, such as deviations in amino acid composition,did not account for the lack of resolution (15). These resultssuggest that the low support values obtained are not due tothe instability (or deviation) of a small subset of taxa butare the result of a systemic lack of support for relationshipsamong most taxa.
Because the choice of taxa did not account for the lack of resolutionin many key branches of the metazoan tree, we then consideredtwo potential analytical explanations: the amount of missingdata contained in the data matrix and the total amount of dataused. By necessity of experimental design, the data matrix lacked,on average, 20% of the potential data per taxon (table S4).However, large data sets can be surprisingly tolerant to a highfraction of missing data (13, 14, 18), and reanalyses of thedata matrix excluding the priapulid and the mollusk (the twotaxa with the highest percentages of missing data; 68 and 54%,respectively) did not lead to noticeable changes in support(table S3). A second potential explanation may be that the datamatrix still contains too few informative characters to robustlyresolve phylogenetic relationships among protostomes and earlybranching metazoans. However, sequence variation is abundantbetween metazoan taxa, with 56% of the 12,060 amino acid sitesbeing variable and 31% of the sites being parsimony-informative(Table 1). Furthermore, MP site pattern and ML mapping (15)analyses suggest that the differences in resolution betweenclades do not result from the number of informative sites perse, but in how these sites are distributed among alternativetopologies (fig. S2). In agreement with these results, two-to eightfold increases in the number of characters resampledby bootstrapping (15) led to small improvements in the resolutionof most internodes (fig. S3 and table S3). These data suggestthat neither the percentage of potential data missing nor thetotal amount of data in this data matrix can explain the lackof resolution among protostomes and early branching metazoans.
Table 1. Statistical attributes of the amino acid sequence data matrix. Numbers of variable, parsimony-informative, and singleton sites for the 50-gene data matrix are shown, including 16 metazoan, 1 choanoflagellate, and 15 fungal taxa. Percentages are reported in parentheses. All statistical attributes for the metazoan taxon set were calculated with choanoflagellates included. The mean observed distance (± standard deviation) corresponds to the average proportion of amino acid sites that are different in all pairwise sequence comparisons in a taxon set. The mean estimated distance (± standard deviation) corresponds to the ML-estimated average proportion of amino acid sites that are different in all pairwise sequence comparisons in a taxon set (15).
Taxon set
Number of sites
Variable sites
Informative sites
Singleton sites
Observed distance
Estimated distance
All taxa
12060
8257 (68%)
6669 (55%)
1588 (13%)
29.2 ± 6.7
35.7 ± 11.1
Metazoa
12060
6782 (56%)
3701 (31%)
3080 (26%)
21.8 ± 4.6
23.4 ± 6.2
Fungi
12060
6533 (54%)
5015 (42%)
1518 (13%)
27.1 ± 5.8
31.7 ± 8.2
A remarkable contrast in phylogenetic resolution between twokingdoms. Given the time since the origin of Metazoa, anotherhypothesis is that mutational saturation (19–21) may haveerased the phylogenetic signal originally contained in proteins'variable sites. Alternatively, the lack of resolution may bethe signature of a closely spaced series of cladogenetic eventsoccurring early in the evolution of Metazoa (7). One means oftesting these alternative explanations is by comparing the phylogenyof Metazoa to that of their natural sister kingdom, the Fungi(22). The validity of this comparison rests on the inferencethat both lineages originated within approximately the samegeological time frame, which is supported by the fossil recordof both Fungi (23) and Metazoa (24, 25), particularly recentfinds in the Doushantuo Formation (551 to 635 million yearsold) (23, 26, 27), as well as molecular clock analyses in whichmultiple representatives of both kingdoms are included (28–30).
The availability of genome sequence data from many species spanningthe fungal kingdom enabled us to sample exactly the same typeand amount of data across Fungi as we did for Metazoa. We generateda data matrix containing 49 of the same 50 genes used for themetazoan phylogeny from a select set of 15 taxa representingmost major taxonomic groups within Ascomycetes and Basidiomycetes(table S1). Examination of evolutionary distances and modelsof amino acid evolution for the 49 orthologs in each of thetwo kingdoms suggests that the tempo and mode of molecular evolutionin this set of 49 genes has remained similar across the twokingdoms (table S5). Furthermore, comparisons of evolutionarydistances within this set of fungi and within their metazoancounterparts suggest that both clades have undergone similaramounts of evolutionary change, with Fungi exhibiting slightlyhigher mean distances [mean observed/estimated distances ±standard error: Metazoa, 21.8 ± 4.6%/23.4 ± 6.2%;Fungi, 27.1 ± 5.8%/31.7 ± 8.2% (Table 1)], a findingconsistent with a similar date of origin (table S6).
Phylogenetic analyses of the data matrix containing both Metazoaand Fungi showed a remarkable contrast in the resolution obtainedwithin each of the two kingdoms. The fungal clade was robustlyresolved, with the overwhelming majority of fungal internodes(11 out of 13) being significantly supported, irrespective ofoptimality criterion used (Fig. 2 and fig. S4). These relationshipsare generally in agreement with previous studies (31). In contrast,again only 4 of 14 metazoan internodes were significantly supportedunder both optimality criteria.
Fig. 2. The contrast in phylogenetic resolution between the clades of Metazoa and Fungi. Values above internodes are as in Fig. 1. Eleven out of 13 internodes in the fungal clade are significantly supported by both optimality criteria (ML and MP), whereas only 4 out of 14 internodes in the metazoan clade are significant. Analyses were also performed by Bayesian inference (15) (fig. S4 and table S3).
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The early history of Metazoa as a radiation compressed in time.The contrast in the resolution of the fungal and metazoan treesshows that neither the type nor the amount of data is a limitto the resolution of relationships within metazoan superclades.Therefore, the explanation for the sharp contrast in resolutionmay lie in differences in the tempo and pattern of cladogenesiswithin the kingdoms. One explanation for the contrasting resolutionobserved in the metazoan and fungal trees may be differencesin "stemminess: (32): a measure of the relative length of internalversus external branches. Theoretical work indicates that theaccuracy of reconstruction is higher for trees exhibiting highstemminess (that is, trees with longer internodes and shorterterminal branches) (32). In agreement with these studies, phylogeneticresolution is higher in the fungal tree, which is characterizedby long internodes (Fiala and Sokal's stemminess index F = 0.201),and poorer in the metazoan clade, where internodes are muchshorter (F = 0.121) (15). These differences in degree of stemminessbetween the two kingdoms are also reflected in the distributionsof parsimony-informative sites (Fungi/Metazoa = 5015/3701 sites)and singleton sites (Fungi/Metazoa = 1518/3080 sites) alongthe branches of the two trees (Table 1).
These contrasts in resolution depth, stemminess, and distributionof site categories between the two kingdoms are consistent witha history of major metazoan lineages characterized by closelyspaced (tempo) series of cladogenetic events (pattern). Paleontologicalevidence also suggests a rapid tempo of cladogenesis near theorigin of Metazoa approximately 600 million years ago, withporiferans (26), cnidarians (33), and at least certain bilaterians(34) making their first appearance within 50 million years.Thus, inferences from these two independent lines of evidence(molecules and fossils) support a view of the origin of Metazoaas a radiation compressed in time.
Identifying the limits to resolution of cladogenetic eventsin deep time by simulation analysis. It has been proposed that,given adequate data, phylogenetic resolution for cladogeneticevents of Cambrian age occurring as close as 1 million yearsapart will be achieved (35). If true, with the amount of dataused here, the lack of observed resolution would indicate extremecompression of the metazoan radiation. Alternatively, the limitof resolution for internodes in deep time may be much largerthan previously suggested.
To better understand the potential limits to the resolutionof series of closely spaced cladogenetic events in deep time,and to explore how to interpret the lack of resolution whenlarge amounts of data are available, we conducted a simulationanalysis. The radiation of mammalian orders is particularlywell suited for addressing this issue because it occurred withina small window of time (42 million years) an estimated 107 millionyears ago (36), with many internodes estimated to span between1 and 10 million years in length. We simulated the effect ofincreasing the elapsed time since the radiation on the phylogeneticaccuracy of internodes within this 42-million-year window, givenadequate data and a rigorous model of sequence evolution (15,20, 37). If the proposed limits of resolution are in fact verysmall, the degree of resolution for all internodes should notbe affected, because all internodes are dated as 1 million yearsin length or longer. However, if the limits of resolution aregreater than has been postulated, then the degree of resolutionfor several internodes should decrease as we move deeper intime.
The results of the simulations show a negative correlation betweenthe amount of time elapsed and the accuracy with which internodesare resolved (Fig. 3 and fig. S5). For example, whereas almostall internodes in simulations assuming a 107-million-year timespan are resolved near 100% accuracy (Fig. 3A), the accuracyof several internodes in data sets simulating the lapse of a600-million-year time span is low (Fig. 3, B to E), contraryto predictions that data matrices of this size and propertiesshould attain accuracy levels of 95% across all internodes (35).These results suggest that the actual limits of resolution forclosely spaced events in deep time is larger than previouslythought (38). To estimate the actual limit of resolution, weplotted the phylogenetic accuracy for each internode againstthe internode's length (in million years), assuming a 600-million-yeartime span. Results suggest that, even when very large data matricesare used, and under simulation assumptions that most likelyrepresent the best of circumstances when compared to biologicaldata, many internodes with lengths much larger than 1 millionyears are resolved with accuracies well below 50% (Fig. 4).Thus, the limit of resolution of large data sets in deep timemay differ by an order of magnitude from previous estimates(35).
Fig. 3. Phylogenetic accuracy is inversely correlated with the length of time elapsed since a closely spaced series of cladogenetic events. A simulation analysis of increasing the age of origin of the 42-million-year window of mammalian order diversification is shown. (A) The best estimate of the mammalian phylogenetic tree at present under the molecular clock assumption (36) (time span of 107 million years). (B) The mammalian phylogenetic tree, assuming a 600-million-year time span. Branch lengths are shown in million-year time units. The topology and branch lengths within the 42-million-year window (left of the dashed grey line) of trees in (A) and (B) are identical. There is a compression in the lengths of internodes in the 42-million-year window of the tree in (B), due to the longer time span elapsed. (C) Graph showing the relationship between phylogenetic accuracy of internodes in the 42-million-year window and total time span simulated, after MP analysis of 100 simulated data matrices, each containing 16,000 characters (of which roughly 6000 are variable). (D) The same graph as in (C), but with simulated data matrices, each containing 73,000 characters (of which roughly 28,000 are variable). Similar results were obtained by neighbor-joining (NJ) analyses (fig. S5). Only 10 exemplar internodes are shown (all the internodes are shown in fig. S5). The numbers of internodes in all panels are according to (36).
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Fig. 4. The limit for resolution of cladogenetic events of Cambrian age, under the best of circumstances, may be an order of magnitude higher than previously thought. The phylogenetic accuracy with which internodes are resolved (the ordinate) is plotted against the length of each internode in million years (the abscissa). Data sets of two different lengths (data set in blue, 16,000 characters, of which 6000 are variable; data set in red, 73,000 characters, of which 28,000 are variable) were generated by simulation, assuming a tree with a 600-million-year time span. For many internodes with lengths much higher than 1 million years, resolution accuracy values are low, irrespective of data set size. Not all internodes of a given age exhibit the same resolution accuracy. For example, certain 3-million-year internodes are resolved with 100% accuracy, whereas other internodes of similar (or greater) age exhibit much lower values of resolution accuracy. Results are shown for analyses using MP [similar results are obtained by NJ analyses (fig. S7)].
[View Larger Version of this Image (11K GIF file)]
The lack of resolution as a signature of events compressed intime. The resolution of other clades of the metazoan tree, inwhich cladogenetic events are thought to be much further apartthan 1 million years, has also proved challenging, despite theuse of large amounts of data. For example, fossil evidence suggeststhat the three major lineages of lobe-limbed vertebrates (lungfish,coelacanths, and tetrapods) first appeared within a time spanof 20 to 30 million years approximately 390 million years ago(39). However, resolution of the relationships among these threelobe-limbed vertebrate lineages has not been obtained, despiteanalyses of more than 40 gene sequences from key taxa (40).The lack of resolution of lobe-limbed vertebrates, of metazoanphyla here and of other problematic groups that diverged indeep time such as the arthropods, coupled with the simulationstudies, suggest that, given adequate sequence data, the lackof phylogenetic resolution is a positive signature of closelyspaced cladogenetic events.
Of course, the ultimate objective of phylogenetics is to resolvethe true branching order within such important groups. So whatare the prospects for doing so? It has been argued that theuse of even more gene sequences will increase the resolutionof such radiations compressed in deep time (35, 40). However,the number of genes identifiable as orthologs, or usable intaxa that diverged in deep time, may actually turn out to beon the order of the number of genes currently being used insome studies (13, 40). If the maximum number of genes that couldfurther be added to existing data matrices is not much greater,even the use of all conserved gene sequences across metazoanphyla or lobe-limbed vertebrates may not suffice for accuratereconstruction of certain clades. Furthermore, although increasingthe gene number greatly reduces sampling error (11), the vulnerabilityto systematic error artefacts also increases (16), perhaps explaininghow different phylogenetic analyses can reach contradictinginferences with absolute support (41–43). In such cases,the use of alternative types of molecular characters, such asrare genomic changes (44–46), and the development of morerealistic models of character evolution (47) may hold the keyto further progress in resolving closely spaced ancient diversificationevents.
References and Notes
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38. We also conducted simulations in which the effect of increasing elapsed time on phylogenetic accuracy was measured, using trees in which all branches are proportionally scaled as time span increases. Results from these simulations show that most internodes are resolved near 100% accuracy, irrespective of time span simulated (fig. S6 and table S8). These results, combined with the lack of resolution within superclades of the metazoan tree, argue against models of metazoan radiation in which the temporal window of diversification is much larger (48).
39. J. A. Clack, Gaining Ground: the Origin and Evolution of Tetrapods (Indiana Univ. Press, Bloomington, IN, 2002).
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47. A goodness-of-fit test using parametric bootstrapping (15) showed that even the best-fit model of sequence evolution does not adequately describe the evolution of the sequence data from these 32 fungal and metazoan taxa (fig. S8).
49. We thank D. Arendt for providing RNA for Platynereis dumerilii; C. Ané for providing the modified version of the Seq-Gen simulation software with an implementation of a covarion model; and B. Prud'homme, B. Williams, and T. Rokas for comments on the manuscript. A.R. was funded by a Human Frontier Science Program Long-Term Fellowship. This work was funded by the Howard Hughes Medical Institute.
Received for publication 29 June 2005. Accepted for publication 4 November 2005.
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Present address: Departments of Bacteriology and Plant Pathology, University of Wisconsin–Madison, 420 Henry Mall, Madison, WI 53706, USA. 
To whom correspondence should be addressed. E-mail: 
