© 2005 Society of Systematic Biologists
Poriferan mtDNA and Animal Phylogeny Based on Mitochondrial Gene Arrangements
Edited by Marshal Hedin: Associate Editor
1 Département de Biochimie, Université de Montréal Succursale Centre-Ville, Montreal, Que H3C 3J7, Canada
2 Robert Cedergren Centre, Program in Evolutionary Biology, Canadian Institute of Advanced Research Montreal, Canada
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Abstract |
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Phylogenetic relationships among the metazoan phyla are the subject of an ongoing controversy. Analysis of mitochondrial gene arrangements is a powerful tool to investigate these relationships; however, its previous application outside of individual animal phyla has been hampered by the lack of informative out-group data. To address this shortcoming, we determined complete mitochondrial DNA sequences for the demosponges Geodia neptuni and Tethya actinia, two representatives of the most basal animal phylum, the Porifera. With sponges as an outgroup, we investigated phylogenetic relationships of nine bilaterian phyla using both breakpoint analysis of global mitochondrial gene arrangements and maximum parsimony analysis of mitochondrial gene adjacencies. Our results provide strong support for a group that includes protostome (but not deuterostome) coelomate, pseudocoelomate, and acoelomate animals, thus clearly rejecting the Coelomata hypothesis. Two other groups of bilaterian animals, Lophotrochozoa and Ambulacraria, are also supported by our analyses. However, due to the remarkable stability of mitochondrial gene arrangements in Deuterostomia and the Ecdysozoa, conclusions on their evolutionary history cannot be drawn.
Keywords: Coelomata hypothesis; metazoan phylogeny; mitochondrial DNA; phylogenetic inference; Porifera
Received May 6, 2004; Revised August 9, 2004; Accepted April 15, 2005
Metazoan phyla can be defined as "the largest groupings of taxa that can readily be seen to be more closely related to each other than to any other groups" (Budd and Jensen, 2000), and thus essentially representing the upper limit in the resolving power of traditional morphological systematics. The interrelationships among different phyla have been the subject of a century-long controversy, and no consensus on the global animal phylogeny has been reached based on morphological and/or embryological data (Jenner and Schram, 1999). Despite this lack of consensus, metazoan relationships have been traditionally depicted as a gradual progression in morphological complexity from simple to complex forms, with a special emphasis on the type of body cavity and the presence or absence of segmentation (Barnes, 1987; Brusca and Brusca, 1990; Hyman, 1940). Accordingly, "acoelomate" platyhelminthes were placed at the base of the bilaterian tree, followed first by "pseudocoelomate" worms, such as nematodes and priapulids, and then by the assemblage of "coelomate" animals (the Coelomata), consisting of the Protostomia (e.g., annelids, mollusks, and arthropods) and the Deuterostomia (e.g., echinoderms, hemichordates, chordates, and often lophophorates) (Fig. 1A).
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The advent of molecular studies, primarily based on nuclear small subunit (SSU or 18S) ribosomal RNA sequences, has challenged this traditional view on animal phylogeny. Unexpectedly, these studies have placed the acoelomate and pseudocoelomate taxa within the Protostomia, thus refuting the Coelomata hypothesis and shifting the split between the protostome and deuterostome animals to the base of bilaterian evolution (Fig. 1B). Several other changes were proposed, including the relocation of the lophophorate taxa from deuterostome to protostome lineage (Halanych et al., 1995; Mackey et al., 1996); the recognition of two large protostome clades, the Lophotrochozoa (e.g., platyhelminthes, annelids, mollusks, and lophophorates) and Ecdysozoa (e.g., arthropods, priapulids, and nematodes) (Aguinaldo et al., 1997; Carranza et al., 1997; Halanych et al., 1995); and the grouping of echinoderms and hemichordates in the Ambulacraria, to the exclusion of chordates (Halanych, 1995; Turbeville et al., 1994; Wada and Satoh, 1994). For a more detailed review of molecular studies related to animal phylogenetics, see Halanych (2004).
Although often referred to as the "new animal phylogeny," the metazoan tree based on 18S sequences has found rather limited support by the analyses of independent molecular datasets (Copley et al., 2004; Telford, 2004; Wagele and Misof, 2001). Some corroboratory evidence comes from the analysis of Hox genes (de Rosa et al., 1999; but see Telford, 2000), Na/K ATPase gene (Anderson et al., 2004), LSU rRNA (Mallatt and Winchell, 2002), and more recently, multiple protein-coding genes (Philippe et al., 2005). By contrast, several other studies based on multiple protein genes reject the rRNA-based phylogeny and advocate the return to the traditional Coelomata hypothesis (Blair et al., 2002; Mushegian et al., 1998; Philip et al., 2005; Wolf et al., 2004). Additional independent data sets are clearly needed to resolve this controversy.
Comparisons of mitochondrial gene arrangements is a powerful tool for phylogenetic inference (Boore, 1999; Boore and Brown, 1998). The large number of possible gene arrangements makes convergence in the gene order unlikely, while the usually slow rate of gene rearrangements in animal mtDNA preserves the phylogenetic signal from mutational oversaturation. Analyses of mitochondrial gene orders in animals have provided convincing results in several cases where all other data were equivocal, including the relationships among major groups of echinoderms (Smith et al., 1993), arthropods (Boore et al., 1995, Boore, Lavrov, and Brown, 1998), and crustaceans (Lavrov et al., 2004; Morrison et al., 2002). However, application of this data set to the study of metazoan phylogeny outside of individual phyla has been hampered by the lack of informative data from accepted outgroups. The nonmetazoan mitochondrial gene arrangements, even of the closest relatives of animals, are too derived to be used in outgroup comparisons (Burger et al., 2003), whereas studied diploblastic animals (cnidarians) lack most mitochondrial tRNA genes (Beagley et al., 1998). In search for an appropriate outgroup for bilaterian animals, we determined complete mtDNA sequences from the demosponges Geodia neptuni and Tethyaactinia (Lavrov et al., 2005), two representatives of arguably the most basal animal phylum, the Porifera. Here we compare poriferan mitochondrial gene arrangements to those of other animals and use them as an outgroup for the analysis of bilaterian phylogeny based on mitochondrial gene order.
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Materials and Methods |
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Specimen Collection, DNA Extraction, Amplification, Cloning, and Sequencing
A specimen of Geodia neptuni (Sollas, 1886) (Class Demospongiae: Order Astrophorida: Family Geodiidae) was collected from Tennessee Reef, Florida Keys, at a depth of 15 m. A specimen of Tethya actinia (de Laubenfels, 1950) (Class Demospongiae: Order Hadromerida: Family Tethyidae) was collected from mangrove roots in Zane Grey Creek, Long Key, Florida. Portions of each sponge were stored frozen after addition of an 8M guanidinium chloride solution (pH 8). Total DNA was prepared from
1-cm3 piece of each specimen by phenol-chloroform extraction following proteinase K digestion. Portions of cox1 and rnl were amplified using primers HCO, LCO, 16S-ARL, and 16S-BRH (Folmer et al., 1994; Hillis et al., 1996) and used to design specific primers for these regions. Complete mtDNA from both species was amplified in two overlapping fragments using the TaKaRa LA-PCR kit under recommended conditions. Random clone libraries were constructed from the purified PCR products by shearing them into fragments 1–3 kbp in size (Okpodu et al., 1994) and by cloning them into a modified pBluescript II KS+ vector with a shortened multi-cloning site (pBFL). Clones were sequenced on a Li-Cor automated sequencer (Lincoln, NE) and assembled using the STADEN software suite (Staden, 1996). Problematic and underrepresented regions were sequenced directly from PCR products by primer-walking. tRNA genes were identified by the tRNAscan-SE program (Lowe and Eddy, 1997); other genes were identified by similarity searches in local databases using the FASTA program (Pearson, 1994), and in GenBank at the NCBI using BLAST network service (Benson et al., 2003). The sequence data from this study have been deposited in GenBank (AY320032
[GenBank]
and AY320033
[GenBank]
).
Phylogenetic Analysis
Two different approaches to the encoding and analysis of gene arrangement data are possible. In the first approach, the ordering of the genes along the chromosome is encoded as a single multistate character, and a distance measure is used to determine the transformational cost among different character states. Since the true evolutionary distance between any two genomes is usually unknown, it is approximated either by the edit distance (the minimum number of permitted evolutionary events that can transform one gene order into another), or by the breakpoint distance (the number of adjacencies present in one genome but not the other) (Watterson et al., 1982). Although such pairwise distances can be used in distance matrix methods (e.g., Sankoff et al., 1992), a better alternative is to use them in direct optimization analyses that reconstruct genomes for internal nodes and minimize the total length of the tree (Blanchette et al., 1999; Tang and Moret, 2003). Direct optimization methods have been developed for breakpoint (Sankoff et al., 1996) and inversion (Bader et al., 2001) distances and have been named minimum breakpoint analysis (Sankoff and Blanchette, 1998) and inversion phylogeny (Moret et al., 2002), respectively. Given that inversions constitute only a small fraction of all rearrangements in animal mtDNA (Boore, 1999; Blanchette, 1999), we used the minimum breakpoint analysis as implemented in the GRAPPA 1.7 program (Moret et al., 2001) for our study. Furthermore, due to the limit on the number of taxa that can be simultaneously analyzed in GRAPPA (< 15; Moret et al., 2004), we constrained the evaluated trees to those that preserve the monophyly of the 10 individual phyla used (see below). These constrains reduce the number of evaluated trees from 1.9x 1017 to just over 2 million and allow us to complete the minimum breakpoint analysis within 1 week on a 2.5-GHz G5 computer.
In the second approach to the analysis of gene order data, the ordering of genes along the chromosome is encoded as a set of characters, corresponding either to observed gene adjacencies or to relative positions of individual genes. If gene adjacencies are used, the presence/absence status for every possible pair of signed genes is recorded as a binary character (Cosner et al., 2000), where a gene's "sign" indicates its transcriptional polarity. If relative gene positions are used, the signed identities of upstream and downstream neighbors for every gene are usually recorded as two multistate characters (Boore et al., 1995; Bryant, 2004; but see Gallut and Barriel, 2002; Wang et al., 2002). In both cases resulting matrices are used directly in the maximum parsimony analysis, and the two methods have been named maximum parsimony on binary encoding (MPMB) and maximum parsimony on multistate encoding (MPME), respectively (Wang et al., 2002). We used only the MPME method for our analysis because it is known to outperform both the MPBE and distance-based methods (Wang et al., 2002). To automate the encoding procedure, we wrote a set of Perl scripts that convert a Genbank flatfile to a matrix of 74 characters corresponding to upstream and downstream position of 37 genes typical for bilaterian mtDNA, as suggested by Boore et al. (1995). This matrix was subsequently used in PAUP* 4.0 Beta10 (Swofford, 2002) for maximum parsimony and bootstrap (1,000 replicates) analyses, and for Kishino-Hasegawa and Templeton tests. Bremer support values were determined using the AutoDecay program by Torsten Eriksson; MacClade 3.04 (Maddison and Maddison, 1992) was used for reconstruction of ancestral states. Both the Perl scripts and the MPME matrix are available upon request.
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Mitochondrial Gene Arrangements of Demosponges
The mitochondrial genomes of G. neptuni and T. actinia (Fig. 2A) contain all 37 genes typical for animals, plus genes for subunit 9 of ATP synthase (atp9), and for two (G. neptuni) or three (T. actinia) additional tRNAs. All genes are transcribed from the same DNA strand of the molecule in both mtDNAs. The relative arrangement of protein and RNA genes is conserved between the two genomes, except for the position of nad6, whereas the locations of 13 tRNA genes differ between them (Fig. 2B). Analysis of gene adjacencies in mtDNAs reveals that 18 identical gene boundaries are present in the two demosponges, and up to 12 between demosponges and bilaterian animals (Fig. 3). Our simulation studies show that two randomly reshuffled genomes with all genes transcribed from the same strand would share on average only one gene boundary. The probability for sharing more than three boundaries is less than 0.05, and even smaller when two transcriptional polarities are allowed. Accordingly, poriferan mitochondrial gene arrangements contain strong, genuine phylogenetic signal that can be used to root a bilaterian tree.
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Phylogenetic Analysis of Animal Relationships Based on Mitochondrial Gene Order Data
The mitochondrial gene orders from two demosponges and selected representatives of nine bilaterian phyla were used for phylogenetic analyses (Table 1). Within each phylum, we chose the phylogenetically most distant species with the best-conserved gene arrangements (as estimated by the number of shared gene boundaries with other phyla): two each from Annelida, Arthropoda, Brachiopoda, Chordata, Echinodermata, Mollusca, and Platyhelminthes, plus the only available hemichordate, Balanoglossus carnosus, and the nematode Trichinella spiralis (Table 1). Although complete mtDNA sequences are available from several nematode species, all but T. spiralis have highly derived gene arrangements statistically indistinguishable from randomly shuffled genomes with the same gene content (data not shown). Furthermore, two other animal phyla for which complete mtDNA sequences are available, the Cnidaria (Beagley et al., 1995) and the Chaetognatha (Helfenbein et al., 2004), have been excluded from this analysis because their mtDNA lacks more than half of the genes found in other animal phyla.
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Minimum breakpoint analysis using GRAPPA 1.7 produced a single best tree with a score of 302 (Fig. 4A). The maximum parsimony analysis of the gene adjacency matrix from the same dataset produced five most parsimonious trees each 578 steps long, consistency index, CI = 0.92 and retention index, RI = 0.86 (Fig. 4A). Both analyses support a monophyletic group including protostome coelomate, pseudocoelomate and acoelomate animals (= protostomia sensuAguinaldo et al. [1997]). Within this group, the lophotrochozoan clade (annelids, mollusks, brachiopods, and platyhelminths) is supported, whereas the relationship among Lophotrochozoa, Nematoda and Arthropoda remains unresolved. The second large group of bilaterian animals, the Deuterostomia (Chordata, Hemichordata, and Echinodermata), is supported only by the MP analysis (Fig. 4B). However, the only character that supports the monophyly of the Deuterostomia in all five MP trees (the presence of -trnS(uga) upstream of trnD) does not appear to be synapomorphic. Rather, the inferred ancestral state for the gene upstream of trnD (+cox1 + trnD) found in one of the sponges and the mollusk Katharina tunicata likely results from an isolated case of convergent evolution. In contrast, Ambulacraria (Hemichordata plus Echinodermata) is recovered as a monophyletic group both in minimum breakpoint and maximum parsimony analyses.
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Bremer support values and bootstrap percentages are moderate for most internal nodes on the MPME tree, an expected result given the small size of the dataset and the relative stability of gene order. Interestingly, bootstrap values appear to be more homogeneous than Bremer support values, with both the Protostomia (Bremer support = 3) and the Deuterostomia (Bremer support = 1) recovered in
75% of bootstrap replicates. To test whether there is a statistically significant signal in the gene order data, we conducted Kishino-Hasegawa and Templeton tests on the MPME matrix for the two a priori hypotheses of animal relationships shown in Figure 1. Both tests showed strong preference for the new animal phylogeny, rejecting the traditional tree with high statistical support (p < 0.002). As corroborative evidence, the best tree that preserves the monophyly of Coelomata in the minimum breakpoint analysis is 313 steps long, 11 steps (3.6%) longer than the best tree without such constraint.
Mitochondrial Gene Arrangement of Ancestral Bilaterian and Gene Order Evolution
One of the open questions in animal evolution is the nature of the last common ancestor of bilaterian animals (Erwin and Davidson, 2002). Both minimum breakpoint and maximum parsimony analyses reconstruct character states for internal (ancestral) nodes, providing an opportunity to address a part of this issue related to mitochondrial gene order. Figure 5A presents the minimum breakpoint reconstruction for the mitochondrial gene order of the common ancestor of bilaterian animals and the MP support for individual gene boundaries in this arrangement, shown by two dots above each of them. As shown in Figure 5A, both analyses agree well on the inferred ancestral bilaterian gene arrangement; only the position of three tRNA genes remains uncertain (shown in gray).
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Figure 5B compares the inferred ancestral bilaterian gene order with those for present-day deuterostome (H. sapiens) and protostome (L. polyphemus) animals. This comparison indicates that the differences previously observed between vertebrate and arthropod genomes (Fig. 4C, D; Clary and Wolstenholme, 1985) are due predominantly to gene rearrangements that occurred in the protostome lineage. By contrast, the gene arrangement typical for present-day vertebrates is almost identical to that of the common ancestor of bilaterian animals. An important implication of this finding is that mitochondrial gene arrangement cannot be used to support either deuterostome monophyly or the affinity of other animals with deuterostomes (despite some recent claims to the contrary; Bourlat et al., 2003). Interestingly, a similar pattern in occurrence of gene rearrangements is repeated in Protostomia. The reconstructed gene arrangement of the protostome ancestor is identical to that of Limulus polyphemus (not shown). Accordingly, the monophyly of the Ecdysozoa or Arthropoda cannot be tested by mitochondrial gene rearrangements.
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Discussion |
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Conservation of Mitochondrial Gene Arrangement Across the Metazoa
One peculiar feature of animal mtDNA is the stability of gene arrangements, which often remain unchanged over long evolutionary periods. Identical or nearly identical mitochondrial gene orders have been found in animal taxa that diverged more than 500 MYA, and some gene clusters are conserved across most animal phyla (Boore, 1999). The present study suggests that the factors underlying this genome stability evolved in the common ancestors of multicellular animals because identical gene clusters are present in mtDNAs of demosponges and bilaterian animals, but not between animals and those of other eukaryotes, including the closest studied outgroup, the choanoflagellate Monosiga brevicollis (Burger et al., 2003). The prevalence of tRNA translocations among gene rearrangements found in two demosponges is also typical of animal mtDNA and suggests a common mechanism of mitochondrial gene rearrangements throughout the Metazoa.
Mitochondrial Gene Rearrangements and Animal Phylogeny
Adoutte et al. (2000) have aptly compared phylogenetics to cosmology, where experimental testing of hypotheses is impossible, and where confidence in the inference depends on the congruence between results obtained from independent data sets. The present analysis of mitochondrial gene arrangements provides strong, independent support for two previously proposed groups of bilaterian animals, Protostomia (sensuAguinaldo et al. (1997)) and Lophotrochozoa (Halanych et al., 1995). The placement of protostome coelomate, pseudocoelomate and acoelomate animals in Protostomia clearly rejects the Coelomata hypothesis in its traditional form (e.g., Barnes, 1987) and also its recent reincarnation (Philip et al., 2005; Wolf et al., 2004). Furthermore, we recover the grouping of hemichordates and echinoderms (Ambulacraria) within Deuterostomia, although in maximum parsimony analysis the support for this group is based on a single shared derived boundary trnE+trnT. Finally, the monophyly of either Deuterostomia or Ecdysozoa is not supported in our analysis, due to the apparent lack of synapomorphic rearrangements in these groups.
For comparison, maximum likelihood, maximum parsimony, and neighbor-joining analyses based on the amino acid sequences of mitochondrial genes for the same set of species produce a phylogeny, with nematodes and platyhelminthes forming a monophyletic group at the base of Bilateria (Fig. 6). This result is likely due to the long branch attraction, a phylogenetic artifact that for these two taxa persists even when many more genes and many more species are included in the analysis (Philippe et al., 2005).
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+I). Identical positions of Nematodes and Platyhelminthes were obtained in maximum parsimony (MP) and neighbor joining (NJ) analyses. Bootstrap support values for "Coelomata" and Nematoda + Platyhelminthes are based on NJ with gamma, MP, ML without gamma, and ML with gamma analyses of 100 bootstrap replicates.Gene Arrangements and Phylogenetics
Although sometimes considered to be a novel character (Dowton et al., 2002), gene order (pattern of chromosomal banding), have been used for phylogenetic inference, even before the role of DNA in inheritance was known (Sturtevant and Dobzhansky, 1936). Later, the gene order–based differences in organellar DNA restriction patterns have been used to study evolutionary relationships among plant species (Knox et al., 1993; Palmer and Zamir, 1982; Timothy et al., 1979). The influx of complete genome sequences, both nuclear and organellar, opens new possibilities for the use of gene order data in phylogenetics. Although not all phylogenetic questions can be studied based on the gene order data, we hope that the present study will inspire further use of this data set in animal phylogenetics, and the development of algorithms that use gene rearrangements for phylogenetic inference.
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Acknowledgements |
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We thank Michelle Kelly for help with specimen collection, Lise Forget and Zhang Wang for assistance in cloning and sequencing, and Bernard Moret for help with GRAPPA. We are grateful to the Editor Roderic Page, Associate Editor Marshal Hedin, two referees, Jon Mallatt and Susan Masta, and to Henner Brinkmann, Wesley Brown, Tim Collins, Karri Haen, Amy Hauth, Nicolas Lartillot, and Herve Philippe for many valuable comments and suggestions. Salary and interaction support from the Canadian Institutes of Health Research (DVL, BFL), the Canadian Institute for Advanced Research (BFL), and supply of laboratory equipment and informatics infrastructure by Genome Quebec/Canada are also gratefully acknowledged.
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3 Current Address: Department of Ecology, Evolution and Organismal Biology, Iowa State University, 343A Bessey Hall, Ames, IA, 50011, USA; E-mail: dlavrov{at}iastate.edu
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References |
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-
Adoutte A., Balavoine G., Lartillot N., Lespinet O., Prud'homme B., de Rosa R. The new animal phylogeny: Reliability and implications. Proc. Natl. Acad. Sci. USA (2000) 97:4453–4456.
Aguinaldo A. M. A., Turbeville J. M., Linford L. S., Rivera M. C., Garey J. R., Raff R. A., Lake J. A. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature (1997) 387:489–493.[CrossRef][Medline]
Anderson F. E., Cordoba A. J., Thollesson M. Bilaterian phylogeny based on analyses of a region of the sodium-potassium ATPase beta-subunit gene. J. Mol. Evol. (2004) 58:252–268.[CrossRef][Web of Science][Medline]
Bader D. A., Moret B. M., Yan M. A linear-time algorithm for computing inversion distance between signed permutations with an experimental study. J Comput Biol. (2001) 8:483–491.[CrossRef][Web of Science][Medline]
Barnes R. D. Invertebrate Zoology (1987) Sinauer Associates.
Beagley C. T., Macfarlane J. L., Pont-Kingdon G. A., Okimoto R., Okada N., Wolstenholme D. R. Mitochondrial genomes of Anthozoa (Cnidaria). Prog. Cell Res. (1995) 5:149–153.
Beagley C. T., Okimoto R., Wolstenholme D. R. The mitochondrial genome of the sea anemone Metridium senile (Cnidaria): Introns, a paucity of tRNA genes, and a near-standard genetic code. Genetics (1998) 148:1091–1108.
Benson D. A., Karsch-Mizrachi I., Lipman D. J., Ostell J., Wheeler D. L. GenBank. Nucleic Acids Res. (2003) 31:23–27.
Blair J. E., Ikeo K., Gojobori T., Hedges S. B. The evolutionary position of nematodes. BMC Evol. Biol. (2002) 2:7.[CrossRef][Medline]
Blanchette M., Kunisawa T., Sankoff D. Gene order breakpoint evidence in animal mitochondrial phylogeny. J. Mol. Evol. (1999) 49:193–203.[CrossRef][Web of Science][Medline]
Boore J. L. Animal mitochondrial genomes. Nucleic Acids Res. (1999) 27:1767–1780.
Boore J. L., Brown W. M. Big trees from little genomes: Mitochondrial gene order as a phylogenetic tool. Curr. Opin. Genet. Dev. (1998) 8:668–674.[CrossRef][Web of Science][Medline]
Boore J. L., Collins T. M., Stanton D., Daehler L. L., Brown W. M. Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature (1995) 376:163–165.[CrossRef][Medline]
Bourlat S. J., Nielsen C., Lockyer A. E., Littlewood D. T., Telford M. J. Xenoturbella is a deuterostome that eats molluscs. Nature (2003) 424:925–928.[CrossRef][Medline]
Bremer K. Branch support and tree stability. Cladistics (1994) 10:295–304.[CrossRef][Web of Science]
Brusca R. C., Brusca G. J. Invertebrates (1990) Sunderland, Massachusetts: Sinauer Associates.
Bryant D. A lower bound for the breakpoint phylogeny problem. J. Discrete Algorithms (2004) 2:229–255.[CrossRef]
Budd G. E., Jensen S. A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. Camb. Philos. Soc. (2000) 75:253–295.
Burger G., Forget L., Zhu Y., Gray M. W., Lang B. F. Unique mitochondrial genome architecture in unicellular relatives of animals. Proc. Natl. Acad. Sci. U.S.A. (2003) 100:892–897.
Carranza S., Baguna J., Riutort M. Are the Platyhelminthes a monophyletic primitive group? An assessment using 18S rDNA sequences. Mol. Biol. Evol. (1997) 14:485–497.[Abstract]
Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecule of Drosophila yakuba: Nucleotide sequence, gene organization, and genetic code. J. Mol. Evol. (1985) 22:252–271.[CrossRef][Web of Science][Medline]
Copley R. R., Aloy P., Russell R. B., Telford M. J. Systematic searches for molecular synapomorphies in model metazoan genomes give some support for Ecdysozoa after accounting for the idiosyncrasies of Caenorhabditis elegans. Evol. Dev. (2004) 6:164–169.[CrossRef][Web of Science][Medline]
Cosner M. E., Jansen R. K., Moret B. M., Raubeson L. A., Wang L. S., Warnow T., Wyman S. A new fast heuristic for computing the breakpoint phylogeny and experimental phylogenetic analyses of real and synthetic data. Proc. Int. Conf. Intell. Syst. Mol. Biol. (2000) 8:104–115.[Medline]
de Rosa R., Grenier J. K., Andreeva T., Cook C. E., Adoutte A., Akam M., Carroll S. B., Balavoine G. Hox genes in brachiopods and priapulids and protostome evolution. Nature (1999) 399:772–776.[CrossRef][Medline]
Dowton M., Castro L. R., Austin A. D. Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: The examination of genome ‘morphology.’ Invertebrate Systematics (2002) 16:345–356.[CrossRef][Web of Science]
Erwin D. H., Davidson E. H. The last common bilaterian ancestor. Development (2002) 129:3021–3032.
Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. (1994) 3:294–299.[Medline]
Gallut C., Barriel V. Cladisic coding of genomic maps. Cladistics (2002) 18:526–536.[Web of Science]
Halanych K. M. The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data. Mol. Phylogenet. Evol. (1995) 4:72–76.[CrossRef][Medline]
Halanych K. M. The new view of animal phylogeny. Annu. Rev. Ecol. Evol. Syst. (2004) 35:229–256.[CrossRef]
Halanych K. M., Bacheller J. D., Aguinaldo A. M., Liva S. M., Hillis D. M., Lake J. A. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science (1995) 267:1641–1643.
Helfenbein K. G., Fourcade H. M., Vanjani R. G., Boore J. L. The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes. Proc. Natl. Acad. Sci. USA (2004) 101:10639–10643.
Hillis D. M., Moritz C., Mable B. K., eds. Molecular systematics (1996) Sunderland, Massachusetts: Sinauer Associates.
Hyman L. H. The invertebrates (1940) New York: McGraw-Hill.
Jenner R. A., Schram F. R. The grand game of metazoan phylogeny: Rules and strategies. Biol. Rev. Camb. Philos. Soc. (1999) 74:121–142.
Knox E. B., Downie S. R., Palmer J. D. Chloroplast genome rearrangements and the evolution of giant Lobelias from Herbaceous Ancestors. Mol. Biol. Evol. (1993) 10:414–430.[Web of Science]
Lavrov D. V., Brown W. M., Boore J. L. Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proc. R. Soc. Lond. B Biol. Sci. (2004) 271:537–544.[Medline]
Lavrov D. V., Forget L., Kelly M., Lang B. F. Mitochondrial genomes of two Demosponges provide insights into an early stage of animal evolution. Mol. Biol. Evol. (2005) 22:1231–1239.
Lowe T. M., Eddy S. R. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. (1997) 25:955–964.
Mackey L. Y., Winnepenninckx B., De Wachter R., Backeljau T., Emschermann P., Garey J. R. 18S rRNA suggests that Entoprocta are protostomes, unrelated to Ectoprocta. J. Mol. Evol. (1996) 42:552–559.[CrossRef][Web of Science][Medline]
Maddison D., Maddison W. MacClade: Analysis of Phylogeny and Character Evolution (1992) Sunderland, Massachusetts: Sinauer Associates Inc.
Mallatt J., Winchell C. J. Testing the new animal phylogeny: First use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol. Biol. Evol. (2002) 19:289–301.
Moret B. M. E., Siepel A. C., Tang J., Liu T. Inversion Medians Outperform Breakpoint Medians in Phylogeny Reconstruction from Gene-Order Data. Lecture Notes in Computer Science (2002) 2452:521–536.[CrossRef]
Moret B. M., Tang J., Warnow T. Reconstructing phylogenies from gene-content and gene-order data. In: Mathematics of Evolution and Phylogeny—Gascuel O., ed. (2004) Oxford: Clarendon Press. Pages 1–32.
Moret B. M., Wyman S., Bader D. A., Warnow T., Yan M. A new implementation and detailed study of breakpoint analysis. Proc. 6th Pacific Symp. on Biocomputing (PSB'01). World Scientific Pub. 583–594.
Morrison C. L., Harvey A. W., Lavery S., Tieu K., Huang Y., Cunningham C. W. Mitochondrial gene rearrangements confirm the parallel evolution of the crab-like form. Proc. R Soc. Lond. B Biol. Sci. (2002) 269:345–350.[Medline]
Mushegian A. R., Garey J. R., Martin J., Liu L. X. Large-scale taxonomic profiling of eukaryotic model organisms: A comparison of orthologous proteins encoded by the human, fly, nematode, and yeast genomes. Genome Res. (1998) 8:590–598.
Okpodu C. M., Robertson D., Boss W. F., Togasaki R. K., Surzycki S. J. Rapid isolation of nuclei from carrot suspension culture cells using a BioNebulizer. Biotechniques (1994) 16:154–159.[Web of Science][Medline]
Palmer J. D., Zamir D. Chloroplast DNA evolution and phylogenetic relationships in Lycopersicon. Proc. Natl. Acad. Sci. USA (1982) 79:5006–50010.
Pearson W. R. Using the FASTA program to search protein and DNA sequence databases. Methods Mol. Biol. (1994) 25:365–389.[Medline]
Philip G. K., Creevey C. J., McInerney J. O. The Opisthokonta and the Ecdysozoa may not be clades: Stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the Coelomata than Ecdysozoa. Mol. Biol. Evol. (2005) 22:1175–1184.
Philippe H., Lartillot N., Brinkmann H. Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa and Protostomia. Mol. Biol. Evol. (2005) 22:1246–1253.
Sankoff D., Blanchette M. Multiple genome rearrangement and breakpoint phylogeny. J. Comput. Biol. (1998) 5:555–570.[Web of Science][Medline]
Sankoff D., Leduc G., Antoine N., Paquin B., Lang B. F., Cedergren R. Gene order comparisons for phylogenetic inference: Evolution of the mitochondrial genome. Proc. Natl. Acad. Sci. USA (1992) 89:6575–6579.
Sankoff D., Sundaram G., Kececioglu J. Steiner points in the space of genome rearrangements. Int. J. Found. Comput. Sci. (1996) 7:1–9.[CrossRef]
Staden R. The Staden sequence analysis package. Mol. Biotechnol. (1996) 5:233–241.[Web of Science][Medline]
Sturtevant A. H., Dobzhansky T. Inversions in the third chromosome of wild races of Drosophila pseudoobscura, and their use in the study of the history of the species. Proc. Natl. Acad. Sci. (1936) 22:448–450.
Swofford D. L. PAUP*: Phylogenetic analysis using parsimony (*and other methods) (2002) Sunderland, MA: Sinauer Associates. Version 4.
Tang J., Moret B. M. Scaling up accurate phylogenetic reconstruction from gene-order data. Bioinformatics (2003) 19(Suppl. 1):i305–i312.[Abstract]
Telford M. J. Turning Hox "signatures" into synapomorphies. Evol. Dev. (2000) 2:360–364.[CrossRef][Web of Science][Medline]
Telford M. J. Animal phylogeny: Back to the coelomata? Curr. Biol. (2004) 14:R274–R276.[CrossRef][Web of Science][Medline]
Timothy D. H., Levings C. S. I., Pring D. R., Conde M. F., Kermicle J. L. Organelle DNA variation and systematic relationships in the genus Zea: Teosinte. Proc. Natl. Acad. Sci. USA (1979) 76:4220–4224.
Turbeville J. M., Schulz J. R., Raff R. A. Deuterostome phylogeny and the sister group of the chordates: Evidence from molecules and morphology. Mol. Biol. Evol. (1994) 11:648–655.[Abstract]
Wada H., Satoh N. Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc. Natl. Acad. Sci. USA (1994) 91:1801–1804.
Wagele J.-W., Misof B. On quality of evidence in phylogeny reconstruction: A reply to Zrzavy's defense of the ‘Ecdysozoa’ hypothesis. J. Zoolog. Syst. Evol. Res. (2001) 39:165–176.[CrossRef]
Wang L. S., Jansen R. K., Moret B. M., Raubeson L. A., Warnow T. Fast phylogenetic methods for the analysis of genome rearrangement data: An empirical study. Proc. 7th Pacific Symp. on Biocomputing (PSB'02). World Scientific Pub. 524–535.
Watterson G. A., Ewens W. J., Hall T. E., Morgan A. The chromosome inversion problem. Journal of Theoretical Biology (1982) 99:1–7.[CrossRef][Web of Science]
Winchell C. J., Sullivan J., Cameron C. B., Swalla B. J., Mallatt J. Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol. Biol. Evol. (2002) 19:762–776.
Wolf Y. I., Rogozin I. B., Koonin E. V. Coelomata and not ecdysozoa: Evidence from genome-wide phylogenetic analysis. Genome Res. (2004) 14:29–36.
Hillis D. M., Moritz C., Mable B. K., eds. Molecular systematics (1996) Sunderland, Massachusetts: Sinauer Associates.
Hyman L. H. The invertebrates (1940) New York: McGraw-Hill.
Jenner R. A., Schram F. R. The grand game of metazoan phylogeny: Rules and strategies. Biol. Rev. Camb. Philos. Soc. (1999) 74:121–142.
Knox E. B., Downie S. R., Palmer J. D. Chloroplast genome rearrangements and the evolution of giant Lobelias from Herbaceous Ancestors. Mol. Biol. Evol. (1993) 10:414–430.[Web of Science]
Lavrov D. V., Brown W. M., Boore J. L. Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proc. R. Soc. Lond. B Biol. Sci. (2004) 271:537–544.[Medline]
Lavrov D. V., Forget L., Kelly M., Lang B. F. Mitochondrial genomes of two Demosponges provide insights into an early stage of animal evolution. Mol. Biol. Evol. (2005) 22:1231–1239.
Lowe T. M., Eddy S. R. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. (1997) 25:955–964.
Mackey L. Y., Winnepenninckx B., De Wachter R., Backeljau T., Emschermann P., Garey J. R. 18S rRNA suggests that Entoprocta are protostomes, unrelated to Ectoprocta. J. Mol. Evol. (1996) 42:552–559.[CrossRef][Web of Science][Medline]
Maddison D., Maddison W. MacClade: Analysis of Phylogeny and Character Evolution (1992) Sunderland, Massachusetts: Sinauer Associates Inc.
Mallatt J., Winchell C. J. Testing the new animal phylogeny: First use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol. Biol. Evol. (2002) 19:289–301.
Moret B. M. E., Siepel A. C., Tang J., Liu T. Inversion Medians Outperform Breakpoint Medians in Phylogeny Reconstruction from Gene-Order Data. Lecture Notes in Computer Science (2002) 2452:521–536.[CrossRef]
Moret B. M., Tang J., Warnow T. Reconstructing phylogenies from gene-content and gene-order data. In: Mathematics of Evolution and Phylogeny—Gascuel O., ed. (2004) Oxford: Clarendon Press. Pages 1–32.
Moret B. M., Wyman S., Bader D. A., Warnow T., Yan M. A new implementation and detailed study of breakpoint analysis. Proc. 6th Pacific Symp. on Biocomputing (PSB'01). World Scientific Pub. 583–594.
Morrison C. L., Harvey A. W., Lavery S., Tieu K., Huang Y., Cunningham C. W. Mitochondrial gene rearrangements confirm the parallel evolution of the crab-like form. Proc. R Soc. Lond. B Biol. Sci. (2002) 269:345–350.[Medline]
Mushegian A. R., Garey J. R., Martin J., Liu L. X. Large-scale taxonomic profiling of eukaryotic model organisms: A comparison of orthologous proteins encoded by the human, fly, nematode, and yeast genomes. Genome Res. (1998) 8:590–598.
Okpodu C. M., Robertson D., Boss W. F., Togasaki R. K., Surzycki S. J. Rapid isolation of nuclei from carrot suspension culture cells using a BioNebulizer. Biotechniques (1994) 16:154–159.[Web of Science][Medline]
Palmer J. D., Zamir D. Chloroplast DNA evolution and phylogenetic relationships in Lycopersicon. Proc. Natl. Acad. Sci. USA (1982) 79:5006–50010.
Pearson W. R. Using the FASTA program to search protein and DNA sequence databases. Methods Mol. Biol. (1994) 25:365–389.[Medline]
Philip G. K., Creevey C. J., McInerney J. O. The Opisthokonta and the Ecdysozoa may not be clades: Stronger support for the grouping of plant and animal than for animal and fungi and stronger support for the Coelomata than Ecdysozoa. Mol. Biol. Evol. (2005) 22:1175–1184.
Philippe H., Lartillot N., Brinkmann H. Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa and Protostomia. Mol. Biol. Evol. (2005) 22:1246–1253.
Sankoff D., Blanchette M. Multiple genome rearrangement and breakpoint phylogeny. J. Comput. Biol. (1998) 5:555–570.[Web of Science][Medline]
Sankoff D., Leduc G., Antoine N., Paquin B., Lang B. F., Cedergren R. Gene order comparisons for phylogenetic inference: Evolution of the mitochondrial genome. Proc. Natl. Acad. Sci. USA (1992) 89:6575–6579.
Sankoff D., Sundaram G., Kececioglu J. Steiner points in the space of genome rearrangements. Int. J. Found. Comput. Sci. (1996) 7:1–9.[CrossRef]
Staden R. The Staden sequence analysis package. Mol. Biotechnol. (1996) 5:233–241.[Web of Science][Medline]
Sturtevant A. H., Dobzhansky T. Inversions in the third chromosome of wild races of Drosophila pseudoobscura, and their use in the study of the history of the species. Proc. Natl. Acad. Sci. (1936) 22:448–450.
Swofford D. L. PAUP*: Phylogenetic analysis using parsimony (*and other methods) (2002) Sunderland, MA: Sinauer Associates. Version 4.
Tang J., Moret B. M. Scaling up accurate phylogenetic reconstruction from gene-order data. Bioinformatics (2003) 19(Suppl. 1):i305–i312.[Abstract]
Telford M. J. Turning Hox "signatures" into synapomorphies. Evol. Dev. (2000) 2:360–364.[CrossRef][Web of Science][Medline]
Telford M. J. Animal phylogeny: Back to the coelomata. Curr. Biol. (2004) 14:R274–R276.[CrossRef][Web of Science][Medline]
Timothy D. H., Levings C. S. I., Pring D. R., Conde M. F., Kermicle J. L. Organelle DNA variation and systematic relationships in the genus Zea: Teosinte. Proc. Natl. Acad. Sci. USA (1979) 76:4220–4224.
Turbeville J. M., Schulz J. R., Raff R. A. Deuterostome phylogeny and the sister group of the chordates: Evidence from molecules and morphology. Mol. Biol. Evol. (1994) 11:648–655.[Abstract]
Wada H., Satoh N. Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc. Natl. Acad. Sci. USA (1994) 91:1801–1804.
Wagele J.-W., Misof B. On quality of evidence in phylogeny reconstruction: A reply to Zrzavy's defense of the ‘Ecdysozoa’ hypothesis. J. Zoolog. Syst. Evol. Res. (2001) 39:165–176.[CrossRef]
Wang L. S., Jansen R. K., Moret B. M., Raubeson L. A., Warnow T. Fast phylogenetic methods for the analysis of genome rearrangement data: An empirical study. Proc. 7th Pacific Symp. on Biocomputing (PSB'02). World Scientific Pub. 524–535.
Watterson G. A., Ewens W. J., Hall T. E., Morgan A. The chromosome inversion problem. Journal of Theoretical Biology (1982) 99:1–7.[CrossRef][Web of Science]
Winchell C. J., Sullivan J., Cameron C. B., Swalla B. J., Mallatt J. Evaluating hypotheses of deuterostome phylogeny and chordate evolution with new LSU and SSU ribosomal DNA data. Mol. Biol. Evol. (2002) 19:762–776.
Wolf Y. I., Rogozin I. B., Koonin E. V. Coelomata and not ecdysozoa: Evidence from genome-wide phylogenetic analysis. Genome Res. (2004) 14:29–36.
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