MBE Advance Access originally published online on April 13, 2007
Molecular Biology and Evolution 2007 24(7):1518-1527; doi:10.1093/molbev/msm070
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Research Articles |
Glass Sponges and Bilaterian Animals Share Derived Mitochondrial Genomic Features: A Common Ancestry or Parallel Evolution?
* Department of Ecology, Evolution and Organismal Biology, Iowa State University
Département de Biochimie, Université de Montréal, Boulevard Edouard Montpetit, Montréal, Québec, Canada
Harbor Branch Oceanographic Institution, Fort Pierce, Florida
E-mail: dlavrov{at}iastate.edu.
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Abstract |
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Glass sponges (Hexactinellida) are a group of deep-water benthic animals that have a unique syncytial organization and possess a characteristic siliceous skeleton. Although hexactinellids are traditionally grouped with calcareous and demosponges in the phylum Porifera, the monophyly of sponges and the phylogenetic position of the Hexactinellida remain contentious. We determined and analyzed the nearly complete mitochondrial genome sequences of the hexactinellid sponges Iphiteon panicea and Sympagella nux. Unexpectedly, our analysis revealed several mitochondrial genomic features shared between glass sponges and bilaterian animals, including an Arg
Ser change in the genetic code, a characteristic secondary structure of one of the serine tRNAs, highly derived tRNA and rRNA genes, and the presence of a single large noncoding region. At the same time, glass sponge mtDNA contains atp9, a gene previously found only in the mtDNA of demosponges (among animals), and encodes a 
with an atypical A11–U24 pair that is also found in demosponges and placozoans. Most of our sequence-based phylogenetic analyses place Hexactinellida as the sister group to the Bilateria; however, these results are suspect given accelerated rates of mitochondrial sequence evolution in these groups. Thus, it remains an open question whether shared mitochondrial genomic features in glass sponges and bilaterian animals reflect their close phylogenetic affinity or provide a remarkable example of parallel evolution.
Key Words: Hexactinellida • Iphiteon panicea • Sympagella nux • mtDNA • genetic code • transfer RNA
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialsAcknowledgementsReferences |
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Glass sponges (class Hexactinellida) are an exclusively marine and predominantly deep-water group of animals that contains about 500 described extant species and plays an important role in benthic communities. The group is defined by the presence of siliceous spicules of triaxonic (cubic) symmetry or their derivatives that are often fused to form a rigid framework (Reiswig 2002
) and sometimes display remarkable optical characteristics (Sundar et al. 2003; Aizenberg et al. 2004). In addition to their characteristic spicules, hexactinellids differ from other sponges in their unique syncytial organization (reviewed in Leys [2003]) and their unusual capability of impulse conduction (Lawn, Mackie, and Silver 1981; Mackie, Lawn, and Pavans de Ceccatty 1983; Leys, Mackie, and Meech 1999).
Although glass sponges have been traditionally placed with calcareous and demosponges in the phylum Porifera (Thomson 1869; Schmidt 1870), this association is based on the overall morphological similarity of sponges rather than any specific synapomorphies (Hooper, Van Soest, and Debrenne 2002). Furthermore, most sequence-based phylogenetic studies fail to recover Porifera as a monophyletic group (Collins 1998; Kruse et al. 1998; Adams, Mclnerney, and Kelly 1999; Borchiellini et al. 2001; Medina et al. 2001; Rokas, Kruger, and Carroll 2005; Müller, Müller, and Schröder 2006). Some of these studies place the Hexactinellida as a sister group to the rest of the Metazoa (Kruse et al. 1998; Borchiellini et al. 2001; Müller, Müller, and Schröder 2006), whereas others support their affinity with the Demospongiae, but exclude Calcarea from the group (Adams, McInerney, and Kelly 1999; Medina et al. 2001). However, statistical support for these alternative hypotheses of poriferan relationships is generally low, and a recent attempt to use multiple genes to elucidate animal phylogeny found no resolution for the relationships among the 3 classes of sponges and other nonbilaterian animals (Rokas, Kruger, and Carroll 2005).
Comparisons of mitochondrial genomes have been useful for investigating ancient animal relationships (Boore, Lavrov, and Brown 1998; Reyes et al. 2004; Lavrov and Lang 2005). In addition to the large amount of sequence data, which minimizes sampling error in sequence-based phylogenetic analysis, mtDNA harbors additional rare genomic characters that are valuable for phylogenetic inference, including indels in the coding sequences, variations in the genetic code, changes in the secondary structures of encoded transfer and ribosomal RNAs, and gene rearrangements (Rokas and Holland 2000). To gain a better understanding of the phylogenetic position of the Hexactinellida and to fill a gap in our sampling of animal mitochondrial genomes, we determined the nearly complete mitochondrial genome sequences of 2 glass sponges, Iphiteon panicea and Sympagella nux. Here, we describe these genomes and analyze their features in relationship to the phylogenetic position of glass sponges and animal mitochondrial evolution.
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Materials and Methods |
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Specimen Collection, DNA Extraction, Amplification, Cloning, and Sequencing
Specimens of I. panicea (Bowerbank, 1869) (Class Hexactinellida: Order Hexactinosida: Family Dactylocalycidae) and S. nux (Schmidt 1870
) (Class Hexactinellida: Order Lyssacinosida: Family Rossellidae) were collected by the "Johnson-Sea-Link" manned submersible near Turks & Caicos and processed as described in Adams et al. (1999). Small fragments of cox1, cox2, cox3, and rnl were amplified from total DNA using sponge-specific primers, checked against the GenBank database to minimize the possibility of contamination, and used to design specific primers for these regions (table 1). Complete mtDNA of I. panicea and partial mtDNA of S. nux mtDNA were amplified in overlapping fragments using the TaKaRa LA-PCR kit. Regions of the S. nux mtDNA upstream of cox1 and downstream of cox3 were amplified using a modified step-out polymerase chain reaction (PCR) approach (Wesley UV and Wesley CS 1997).
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Random clone libraries were constructed from purified PCR products by nebulizing them into fragments 1–3 kbp in size and cloning them into the pCR 4Blunt-TOPO vector (Invitrogen, Carlsbad, CA) as described previously (Wang and Lavrov 2007
), sequenced at the Iowa State University DNA Facility on a ABI 3730 DNA Analyzer, and assembled using the STADEN software suite (Staden 1996). The region downstream of cob and upstream of cox1 was problematic for PCR amplification, cloning, and sequencing, and only partial sequence from this region has been determined.
Most tRNA genes were identified by the tRNAscan-SE program (Lowe and Eddy 1997); other genes were identified by comparisons between the 2 genomes, similarity searches in local databases using the FASTA program (Pearson 1994) and in GenBank using the Blast network service (Benson et al. 2003). The secondary structures of tRNA genes were drawn with the Macromedia FreeHand program.
Phylogenetic Analysis
The inferred amino acid sequence for Cantharellus cibarius mtDNA was downloaded from http://megasun.bch.umontreal.ca/People/lang/FMGP/proteins.html. Other sequences were derived from the GenBank files: Katharina tunicata NC_001636, Limulus polyphemus NC_003057, Asterina pectinifera NC_001627, Mustelus manazo NC_000890, Acropora tenuis NC_003522, Astrangia sp. NC_008161, Briareum asbestinum NC_008073, Metridium senile NC_000933, Montastraea annularis NC_007224, Nematostella sp. NC_008164, Ricordea florida NC_008159, Sarcophyton glaucum AF064823 and AF063191, Aurelia aurita NC_008446, Axinella corrugata NC_006894, Geodia neptuni NC_006990, Oscarella carmela EF081250, Tethya actinia NC_006991, Trichoplax adhaerens NC_008151, Amoebidium parasiticum AF538042–AF538052, Monosiga brevicollis NC_004309, Allomyces macrogynus NC_001715, Cryptococcus neoformans NC_004336, Mortierella verticillata NC_006838, Penicillium marneffei NC_005256, Podospora anserina NC_001329, Rhizopus oryzae NC_006836, and Spizellomyces punctatus NC_003052.
A concatenated alignment of protein-coding genes was prepared as described previously (Lavrov et al. 2005). Searches for the maximum likelihood (ML) topologies were performed with the TreeFinder program (Jobb, von Haeseler, and Strimmer 2004) using the mtArt + 
(Abascal, Posada, and Zardoya 2006), cpREV + (Adachi et al. 2000), mtREV + (Adachi and Hasegawa 1996), and JTT + (Jones, Taylor, and Thornton 1992) models of amino acid substitutions and with the RAxML program (Stamatakis 2006) using the cpREV + F + model. Bayesian inferences were conducted with the MrBayes 3.1.2 (Ronquist and Huelsenbeck 2003) and Phylobayes 2.1c programs. For the MrBayes analysis, we used the cpREV model of amino acid substitutions with 4 + I distributed rates and conducted 2 simultaneous runs, each with 4 Markov chain Monte Carlo chains, for 1,100,000 generations. Trees were sampled every 1,000th cycle after the 1st 100,000 burn-in cycles. The results of the 2 runs were compared with the AWTY program (Wilgenbusch, Warren, and Swofford 2004). For the PhyloBayes analysis, we used the CAT + model and ran 3 chains for 35,000 cycles. Trees were sampled every 10th cycle after the 1st 5000 burn-in cycles (the maximum difference in the frequency of bipartitions between the 2 runs was 0.03). Likelihood-based tests of alternative topologies were conducted as follows: ML branch lengths of alternative topologies were calculated with Tree-Puzzle (Schmidt et al. 2002) using the mtREV24 + F + 8 model of amino acid substitutions; log-likelihood values for individual sites in the alignment were computed with Codeml (Yang 1997) using the cpREV + F + 8 substitution model; and the probability values for different likelihood-based tests were determined with Consel (Shimodaira and Hasegawa 2001).
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Results |
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Mitochondrial Genome Organization Is Similar in Glass Sponges and Bilaterian Animals
The sequenced portions of the mitochondrial genomes of I. panicea and S. nux are 19.0 and 16.3 kb in size and contain 37 and 35 genes, including 13 and 12 protein-coding genes, 2 rRNA genes, and 22 and 20 tRNA genes, respectively (fig. 1). Identified protein-coding genes include all those typical for bilaterian animals with the exception of atp8 (and nad6 in S. nux), as well as the gene for subunit 9 of adenosine triphosphate (ATP) synthase (atp9), previously found only in the mtDNA of demosponges among animals. Identified mt-tRNA genes include only those typical for bilaterian animals; none of the additional mt-tRNAs present in demosponges and the placozoan T. adhaerens have been found in glass sponge mtDNA. In addition, 2 large (>200 bp) open reading frames (ORFs) of 582 and 909 bp in size are present in the sequenced portion of the I. panicea mitochondrial genome.
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All genes have the same transcriptional orientation in both mtDNAs. The arrangements of protein and rRNA coding genes in the 2 genomes are identical with the exception of the position of cox2 and the absence of the nad6 gene in S. nux (fig. 1). In contrast, only 6 of the tRNA genes share the same relative position in the 2 genomes. A maximum of 5 gene boundaries are shared with the demosponge G. neptuni: 3 of these gene boundaries (+nad2+nad5, +atp6+cox3, and +nad3+trnR) are well conserved in the mitochondrial DNA of demosponges and cnidarians, and, except for the +nad2+nad5 boundary, have also been reconstructed in ancestral bilaterian mtDNA (Lavrov and Lang 2005
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The A + T content of I. panicea and S. nux is 65.3% and 70.4%, respectively, which is within the range of other animals and similar to that of demosponges. The coding strand of I. panicea mtDNA has an AT skew of 0.36 and a GC skew of –0.36. In S. nux, the AT skew is 0.19 and the GC skew is –0.28. The polarity of each skew holds true regardless of the gene type analyzed: protein, tRNA, and rRNA (table 2). However, the AT-skew is reversed at the 2nd codon position in coding sequences, consistent with the fact that most codons specifying nonpolar amino acids, which are prevalent in mitochondrial (and other transmembrane) proteins, have thymidine (uridine) at the 2nd position (table 2). The compositional biases observed in the coding strands of glass sponge mtDNA are similar to those of many bilaterian animals rather than demosponges, cnidarians, and the choanoflagellate M. brevicollis, in which coding strands have an overall positive GC skew and negative AT skew (Beagley, Okimoto, and Wolstenholme 1998; Burger et al. 2003; Lavrov et al. 2005; Dellaporta et al. 2006).
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Although most genes in hexactinellid DNA are compactly arrayed, a single large noncoding region is present in both genomes downstream of nad4. This region has been only partially sequenced and contains at least 645 bp (41.3%) and 348 bp (33.3%) of the noncoding nucleotides in I. panicea and S. nux mtDNA, respectively. Like in many bilaterian animals, this large noncoding region includes multiple repeated sequences and was problematic for PCR amplification, cloning, and sequencing. Other noncoding regions are substantially smaller, and several genes in S. nux mtDNA appear to overlap. Thus, with the exception of the presence of atp9, hexactinellid mtDNA resembles the mtDNA of bilaterian animals in gene content, nucleotide composition, and general organization of mtDNA. A more detailed analysis revealed several specific mitochondrial features that are potentially informative for understanding the phylogenetic position of glass sponges.
Glass Sponges and Bilaterian Animals Share an Arg Ser Reassignment of Mitochondrial AGR Codons
The analysis of mitochondrial coding sequences in hexactinellids both manually and using genetic code prediction software (Abascal, Zardoya, and Posada 2006) showed that glass sponges use a modified genetic code for mitochondrial protein synthesis with UGA coding for tryptophan and AGR coding for serine. Specifically, nearly all tryptophan residues in encoded proteins are specified by the UGA codon (the UGG codon is extremely rare in both genomes and is potentially involved in translational frameshifting [Haen KM, Lavrov DV, unpublished data]), whereas 
42% of AGR codons in evolutionarily conserved positions in each genome code for serine, and none of them code for arginine. Furthermore, the inference that AGR codons specify serine is supported by the presence of only one tRNA for AGN codons 
in both genomes. Whereas the reassigned UGA codon is found in the mtDNA of all animals, the only other known reassignments of AGR codons occurred in the mtDNA of bilaterian animals, first in the lineage leading to this group (Arg Ser), then in the lineage leading to chordates (Ser ?), and finally in 2 chordate lineages: Urochordata (? Gly) and Vertebrata (? stop) (Knight, Freeland, and Landweber 2001).
Interestingly, although the AUA codon appears to have a standard meaning (isoleucine) in glass sponges, the sequenced portions of glass sponge mtDNA do not code for the 
that usually translates this codon in eubacteria and eubacteria-derived organelles (Muramatsu et al. 1988; Weber et al. 1990; Soma et al. 2003). This lack of a specific tRNA for the AUA codon is shared with several groups of bilaterian animals (hemichordates, echinoderms, and flat worms), where the AUA codon also specifies isoleucine, but is translated by a modified 
together with 2 other isoleucine codons, AUC and AUU (Castresana, Feldmaier-Fuchs, and Pääbo 1998; Tomita, Ueda, and Watanabe 1999). It is not clear whether these changes occurred convergently in these groups or if they represent an intermediate state in the reassignment of the AUA codon from isoleucine to methionine in animal mtDNA.
Mitochondrial Genomes of Glass Sponges Encode Highly Derived rRNA and tRNA Structures
The analysis of tRNA and rRNA genes in glass sponge mtDNA revealed that both the primary and secondary structures of encoded RNAs are highly derived and resemble those encoded by bilaterian rather than nonbilaterian animals. The changes in tRNA structures are particularly striking (fig. 2). Canonical tRNAs in nuclear, bacterial, and most organellar genomes have several highly conserved features: a 7-bp aminoacyl arm, a dihydrouridine (DHU) stem varying in size from 3–4 bp, a DHU loop of 8–10 nt, a 5-bp anticodon stem with a 7-nt anticodon loop, and a 5-bp T
C stem with a 7-nt loop (Marck and Grosjean 2002). Furthermore, several nucleotides are nearly universally conserved in standard tRNAs, including 2 guanines within the DHU-loop that bind to well-conserved nucleotides in the TC loop, stabilizing the 3-dimensional L-shaped structure of tRNAs. Conventional tRNAs are found in demosponge, cnidarian, and Trichoplax mtDNA, but in most bilaterian animals there are multiple deviations from this pattern of conservation (Wolstenholme 1992). Similar to bilaterian animals, glass sponge mt-tRNAs display a great degree of variation in both the size and nucleotide sequence of the DHU and TC arms, including a highly variable sequence of the TC loop and a typical absence of guanine residues in the DHU loops (fig. 2). The authors are not aware of any other group of organisms that encode tRNAs with similar characteristics.
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Unusual Structure of tRNA(Ser) and an Unusual R11-Y24 Base Pair in tRNA(Pro)
Two tRNAs encoded by glass sponge mtDNA have specific features shared with corresponding tRNAs in other animals and are potentially phylogenetically informative. First, hexactinellid
appears to have a very unusual secondary structure with the DHU arm replaced by a loop (fig 3). Remarkably, a similar "truncated cloverleaf" secondary structure is a characteristic feature of mitochondrial 
of bilaterian animals. Although this structure appears to be disadvantageous in translation, at least in vitro (Hanada et al. 2001), it is conserved throughout the evolution of the Bilateria (Garey and Wolstenholme 1989; Wolstenholme 1992; Ruiz-Trillo et al. 2004).
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Second, an atypical R11–Y24 pair is present in
of glass sponges as well as all demosponges and the placozoan Trichoplax but is not found in the outgroup species M. brevicollis and A. parasiticum or in bilaterian animals (Wang and Lavrov 2007). Because the R11–Y24 base pair is an important recognition element for initiator tRNA, it is usually strongly counterselected in elongator tRNAs (Marck and Grosjean 2002), and its presence in the proline tRNA of sponges and T. adhaerens may indicate the monophyly of nonbilaterian animals or at least the monophyly of the Porifera and Placozoa (this character is not available for Cnidaria because they lack this and most other tRNA genes in their mtDNA).
Phylogenetic Analyses Based on Sequence Data Give a Mixed Message about the Phylogenetic Position of the Hexactinellida
Phylogenetic analyses based on deduced amino acid sequences using traditional empirical substitution models provide strong support for the sister group relationship between glass sponges and bilaterian animals (fig. 4A). These analyses separate animals into 2 groups: the Diploblastica (excluding the Hexactinellida) and the Bilateria, with glass sponges grouping with the latter group. The inferred phylogeny is stable with respect to the substitution matrix—identical ML topologies were found by the TreeFinder program when using the JTT + , mtREV + , cpREV + , or mtART + models of sequence evolution—and with respect to the phylogenetic program used—both TreeFinder and RAxML (using the best available cpREV + F + model) found the same ML topology with similar bootstrap support values. Alternative positions of the Hexactinellida (e.g., as the sister group to other Metazoa and as the sister group to the Demospongiae) were rejected by likelihood tests (fig. 4C). In addition, the ML topology received >98% posterior probability in the MrBayes analysis.
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We have previously proposed (Lavrov et al. 2005
) that the clustering of nonbilaterian animals in phylogenetic analyses based on mtDNA data might be explained by elevated rates of mitochondrial sequence evolution in Bilateria, which would pull the latter group toward the base of metazoan tree due to a long-branch attraction (LBA) artifact (Felsenstein 1978; Hendy and Penny 1989). The unusual position of the Hexactinellida can be rationalized in the same way. In fact, the LBA artifact in the present analysis should be exacerbated by the similar nucleotide compositions of coding strands in the Hexactinellida and Bilateria, which is a feature that may reflect phylogenetic relationships but is also prone to convergence (Steel, Lockhart, and Penny 1993). Several strategies have been suggested to alleviate the effect of the LBA artifact on phylogenetic inference, which involve either better detection of multiple substitutions or minimizing their number (Baurain, Brinkmann, and Philippe 2007). To minimize the number of multiple substitutions, we redid our analyses without bilaterian animals (one of the long branches on the tree) and also conducted a Bayesian analysis on the amino acid data recoded into 6 Dayhoff groups (Hrdy et al. 2004). Neither of these modifications changed the relative phylogenetic position of the Hexactinellida on the tree (not shown). We also used a potentially better model of sequence evolution—the category (CAT) + model (Lartillot and Philippe 2004) that explicitly handles the heterogeneity of the substitution process across amino acid positions. The results of this analysis placed glass sponges as an unresolved polyphyly with the demosponges A. corrugata, G. neptuni, and T. actinia (fig 4B). Although this position of glass sponges is more reasonable from a traditional perspective, it appears to be sensitive to the choice of taxa: glass sponges are placed as a sister group to G. neptuni when bilaterian animals are excluded from the analysis, but as a sister group to the jellyfish A. aurita when additional unpublished demosponge sequences are added to the data set (not shown). |
Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialsAcknowledgementsReferences |
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Genomic analyses of hexactinellid mtDNA revealed several derived mitochondrial features shared with bilaterian animals, including changes in the genetic code, gene content, nucleotide composition, tRNA and rRNA structures, and the presence of a single large noncoding region. These unexpected results can be explained either by a sister group relationship between glass sponges and bilaterian animals or by parallel mitochondrial evolution in these two groups.
In our view, the strongest support for the sister group relationship between glass sponges and bilaterian animals comes from the reassignment of the mitochondrial AGR codons from serine to arginine and from the changes in the secondary structure of the in both of these groups (fig. 3). Changes in the genetic code are complex and rare events; therefore, they are usually regarded as reliable indicators of phylogenetic relationships (Telford et al. 2000). Similarly, changes in the secondary structure of mitochondrial tRNAs and, in particular, also appear to be rare and complex events that, so far, are known to occur only in the Bilateria and Hexactinellida. It should be noted, however, that because translates AGR codons that changed their meaning in both groups, the modifications in the genetic code and structure may be not independent. Other features shared between these 2 groups are known to be prone to convergence.
Not all mitochondrial genomic features support the affinity of glass sponges and bilaterian animals. MtDNA of glass sponges and demosponges share the presence of atp9, a gene for subunit 9 of ATP synthase that is absent in the mtDNA of all other animals. Although the presence of atp9 is clearly a plesiomorphic feature for these taxa that says nothing about sponge monophyly, the sister group relationship between hexactinellids and bilaterians would imply multiple independent mitochondria-to-nucleus transfers of atp9 within the Metazoa. It should be noted, however, that such independent transfers of organellar genes are quite common (Martin et al. 1998), and a specific example of an independent atp9 transfer to the nucleus has been reported recently in the demosponge Amphimedon queenslandica (Erpenbeck et al. 2007). The 2nd mitochondrial genomic feature that contradicts the grouping of Hexactinellida and Bilateria is the unusual R11–Y24 pair in the proline tRNA. This unusual base pair is an apomorphy for sponges and placozoans and to our knowledge has not been found in the mt-tRNAPro of either bilaterian animals or any outgroups. Because the R11–Y24 base pair is an important recognition element for initiator tRNA, it is usually strongly counterselected in elongator tRNAs, and its presence in 
may be phylogenetically informative.
Interestingly, phylogenetic analyses of deduced amino acid sequences also produced ambiguous results for the position of the Hexactinellida. The use of traditional empirical models of amino acid evolution resulted in strong support (with high bootstrap and posterior probability numbers) for the sister group relationship between glass sponges and bilaterian animals. By contrast, phylogenetic inference based on the newly developed CAT model placed glass sponges within the Demospongiae. However, the alternative positioning proposed by CAT is not stable upon taxonomic resampling, suggesting the influence of other artifacts, such as compositional biases, that are not accounted for by the CAT model (Lartillot N, personal communication).
To conclude, most of the mitochondrial genomic characters support the sister group relationship between glass sponges and bilaterian animals. If confirmed, this position of glass sponges would prompt the reassessment of mainstream ideas about early animal evolution in general and the evolution of the sponge body plan in particular. If, conversely, this relationship is refuted, then all the mitochondrial features shared between glass sponges and bilaterian animals—a change in the genetic code, changes in secondary structures of the encoded tRNAs, and the loss of the D-arm in tRNAs, among others—will serve as remarkable examples of parallel evolution in mitochondrial genomes and may provide insights into the origin of unusual features in animal mtDNA. Further studies are needed to distinguish between these 2 possibilities.
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Supplementary Materials |
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Mitochondrial genome sequences of I. panicea and S. nux have been deposited in the GenBank database under the accession numbers EF537576 [GenBank] and EF537577 [GenBank] , respectively.
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialsAcknowledgementsReferences |
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We thank Hervé Philippe, Xiujuan Wang, Jonathan Wendel, and 3 anonymous reviewers for valuable comments on an earlier version of this manuscript, Nicolas Lartillot for his help with the PhyloBayes program, and the Canadian Institutes of Health Research and the College of Liberal Arts and Sciences at Iowa State University for funding.
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Footnotes |
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Martin Embley, Associate Editor
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