Integrative and Comparative Biology Advance Access originally published online on June 13, 2007
Integrative and Comparative Biology 2007 47(5):734-743; doi:10.1093/icb/icm045
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Key transitions in animal evolution: a mitochondrial DNA perspective
Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, Iowa 50011, USA
Correspondence: 1E-mail: dlavrov{at}iastate.edu
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Synopsis
IntroductionAnimal mitochondrial DNA (mtDNA) is usually depicted as a small and very economically organized molecule with almost invariable gene content, stable gene order, a high rate of sequence evolution, and several unorthodox genetic features. Sampling across different animal phyla reveals that such a description applies primarily to mtDNA of bilaterian animals (such as arthropods or chordates). By contrast, mitochondrial genomes of nonbilaterian animals (phyla Cnidaria, Placozoa, and Porifera) display more variation in size and gene content and, in most cases, lack the genetic novelties associated with bilaterian mtDNA. Outside the Metazoa, mtDNA of the choanoflagellate Monosiga brevicollis, the closest unicellular out-group, is a much larger molecule that contains a large proportion of noncoding DNA, 1.5 times more genes, as well as several introns. Thus, changes in animal mtDNA organization appear to correlate with two main transitions in animal evolution: the origin of multicellularity and the origin of the Bilateria. Studies of mtDNA in nonbilaterian animals provide valuable insights into these transitions in the organization of mtDNA and also supply data for phylogenetic analyses of the relationships of early animals. Here I review recent progress in the understanding of nonbilaterian mtDNA and discuss the advantages and limitations of mitochondrial data sets for inferences about the phylogeny and evolution of animals.
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Introduction |
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When the first complete mitochondrial DNA (mtDNA) sequence—that of humans—was determined (Anderson et al. 1981
), it was fittingly described by the phrase "small is beautiful" (Borst and Grivell 1981). Mitochondrial genomes of bilaterian animals are indeed small (
16 kpb), not only because of their limited coding capacity (typically 37 genes), but also due to the remarkable economy of their genomic organization (Fig. 1). Genes encoded in bilaterian mtDNA are compactly arrayed, separated by no, or only a few, nucleotides and contain neither introns nor regulatory sequences. Protein and transfer RNA genes are even often truncated and completed by posttranscriptional polyadenylation (Yokobori and Pääbo 1997). Furthermore, changes in the genetic code allowed animals to reduce the set of mitochondrial tRNA genes to 22, several tRNAs fewer than the minimum number required for translation under the standard genetic code (Marck and Grosjean 2002). Encoded ribosomal RNAs are also reduced, lacking many secondary structures present in homologous molecules in other groups. In addition to their small size, bilaterian mtDNA displays several unusual genetic and genomic features such as unorthodox translation-initiation codons, highly modified structures of encoded ribosomal and transfer RNAs, a high rate of sequence evolution, a relatively low rate of gene rearrangements, and the presence of a single large noncoding "control" region (Wolstenholme. 1992b).
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Although the organization of mtDNA is remarkably uniform across different groups of bilaterian animals [but see Armstrong et al. (2000
) and Helfenbein et al. (2004) for some exceptions], it is far from typical for other eukaryotic lineages in which mitochondrial genomes vary greatly in size, gene content, and genome architecture (Lang et al. 1999). For example, the mitochondrial genome of the choanoflagellate Monosiga brevicollis, a close relative of animals, is several-fold larger with 1.5 times as many genes. In addition, it encodes bacteria-like transfer and ribosomal RNAs, and uses a minimally derived genetic code with TGA(Trp) as the only deviation from the standard code (Burger et al. 2003; Fig. 1). Thus, most distinct characteristics of animal mtDNA have clearly evolved after the divergence of the metazoan ancestors from their unicellular ancestors (Fig. 2). Recent studies on mtDNA in nonbilaterian animals provide valuable insights into this remarkable transition in the organization of mtDNA and contribute to an understanding of the evolutionary factors that shape animal mtDNA. Here I briefly review these studies and discuss their implications for animal phylogeny and for the evolution of mtDNA.
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The mitochondrial DNA of nonbilaterian animals |
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Complete, or nearly-complete, mitochondrial DNA sequences have been determined for at least 32 species of nonbilaterian animals, including 24 species of cnidarians, five species of demosponges, two species of glass sponges, and four placozoan strains (Table 1). These mitochondrial genomes show many deviations from the typical bilaterian mtDNA described above. First, mtDNA is usually larger in size in nonbilaterian compared to bilaterian animals, averaging
18.2 kbp in Cnidaria, 20.6 in demosponges, and 37.4 in placozoans (Table 1). The larger size of these mtDNAs is primarily due to the presence of noncoding intergenic regions, as well as larger and more bacteria-like ribosomal and transfer RNA genes. Second, nonbilaterian mtDNA shows more variation in the gene content. Extra protein-coding genes are found in several lineages of nonbilaterian animals, including atp9 for ATP synthase subunit 9 in most demosponges (Lavrov et al. 2005) and two glass sponges (Haen et al. 2007), tatC for twin-arginine translocase subunit C in Oscarella carmela (Wang and Lavrov 2007), mutS for a putative mismatch repair protein in octocorals (Pont-Kingdon et al. 1995, 1998; Medina et al. 2006), and polB for the DNA-dependent DNA polymerase in the jellyfish Aurelia aurita and one strain of placozoans (Shao et al. 2006; Signorovitch et al. 2007). In addition, out of 22 tRNA genes typically present in mtDNA of bilaterian animals, at most two, trnM and trnW, are found in cnidarian mtDNA (Beagley et al. 1995), only five are found in the mtDNA of the demosponge Plakortis angulospiculatus (Fig. 3; unpublished data) and 17 are found in the mtDNA of another demosponge Amphimedon compressa (Erpenbeck et al. 2007). By contrast, additional mitochondrial tRNA genes are present in mtDNA of other demosponges and placozoans. Third, mitochondrial group I introns, with or without the homing endonucleases of the LAGLI-DADG type, are found in hexacorals (Beagley et al. 1996; van Oppen et al. 2002; Fukami and Knowlton 2005), placozoans (Signorovitch et al. 2007), and several species of demosponges (Rot et al. 2006; unpublished data). Fourth, demosponges, cnidarians, and placozoans use a minimally modified genetic code for mitochondrial translation, with TGA = tryptophan as the only deviation. The same genetic code is used for mitochondrial translation in M. brevicollis and in most (but not all) fungi, whereas most bilaterian animals have modified the specificity of at least ATA and AGR codons (Knight et al. 2001). Finally, many nonbilaterian animals display low rates of evolution of mitochondrial sequences as revealed by intraspecific (Shearer et al. 2002; Duran et al. 2004; Hellberg 2006; Wörheide 2006) as well as by interspecific (Lavrov et al. 2005; Medina et al. 2006) studies based on mtDNA sequences.
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Recently we found that one group of nonbilaterian animals—glass sponges (Hexactinellida)—share several mitochondrial genomic features with bilaterian animals, including a specific change in the genetic code, highly derived structures of encoded ribosomal and transfer RNAs, and the general organization of the mitochondrial genome (Haen et al. 2007
). It is presently unclear whether the presence of these shared mitochondrial genomic features reflects a closer phylogenetic affinity between glass sponges and bilaterian animals or provides a remarkable example of parallel evolution (Fig. 2). |
Animal mitochondrial synapomorphies |
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Given that most of the features previously thought to be characteristic of animal mtDNA now appear to have evolved within the Metazoa, one may wonder whether there are any mitochondrial synapomorphies for all animals. Our analyses reveal two such shared, derived features. First, we found a set of Metazoa-specific insertions/deletions (indels) in mitochondrial protein-coding genes (Fig. 4). These indels are well conserved across the Metazoa, but are absent in M. brevicollis and other nonanimal species (Lavrov et al. 2005
). Although the value of an individual indel for phylogenetic reconstruction is limited (Gribaldo and Philippe 2002), the presence of several such events in mitochondrial genes provides strong support for the monophyly of the Metazoa and can serve as a good indicator of metazoan affinity. Second, an atypical R11-Y24 pair is present in 
of both bilaterian (Wolstenholme. 1992a) and nonbilaterian animals, but is absent in nonmetazoan outgroups. The R11-Y24 pair is otherwise a distinctive feature of bacterial, archaeal, and organellar initiator 
that is strongly counterselected in elongator tRNAs (Marck and Grosjean 2002; but see Wang and Lavrov 2007). The lack of both of these synapomorphies in the mtDNA of M. brevicollis refutes the idea that choanoflagellates may be derived from sponges or other basal metazoans (e.g., King and Carroll 2001; Maldonado 2004).
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Phylogenetic inference using mitochondrial sequences and gene orders |
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Mitochondrial genomic data provides two primary data sets for phylogenetic inference: gene sequences and gene orders (Bruns et al. 1989
; Boore and Brown 1998; Lavrov and Lang. 2005a). Both of these data sets are well suited for phylogenetic analysis within individual lineages of nonbilaterian animals because of the relatively low rate of evolution of mitochondrial sequences and the relatively high rate of mitochondrial gene rearrangements in these groups (Medina et al. 2006; Signorovitch et al. 2007; Wang and Lavrov 2007). The inference of global animal relationships based on these data sets, however, is more complicated. Two primary problems for such an analysis are heterogeneous patterns of mitochondrial evolution among different animal lineages and the sparse sampling of mitochondrial genomes from nonbilaterian animals. The first of these problems is best illustrated by unequal rates of sequence evolution and variable nucleotide composition in bilaterian versus nonbilaterian animals. These differences can cause the well-known artifact of long-branch attraction (LBA) in phylogenetic reconstruction (Felsenstein 1978; Hendy and Penny 1989), whereby rapidly evolving bilaterian animals are "attracted" to other long branches or to distantly related outgroups. The second problem can be seen in the complete absence of mtDNA data from the phylum Ctenophora and several classes of cnidarians and sponges. In the case of the data on gene order, additional problems stem from the lack of informative data from accepted outgroups and from the variation in the mitochondrial gene content across nonbilaterian animals, especially, the loss of nearly all tRNAs in Cnidaria and some sponge lineages (Lavrov and Lang. 2005a).
Two recent developments may resolve at least some of the issues outlined above. First, the sampling of mtDNA from nonbilaterian animals has increased substantially in the last couple of years and several on-going projects in our and other labs will further rectify this problem. Second, a new category (CAT) model of sequence evolution that explicitly handles the heterogeneity of the substitution process across amino-acid positions has been recently developed (Lartillot and Philippe 2004) and shows great promise in overcoming some artifact of phylogenetic reconstruction (Lartillot et al. 2007). Nevertheless, the results of mtDNA-based analyses of global animal phylogeny should be treated cautiously because even much larger data set often produce little resolution for such ancient events (Rokas et al. 2003; Rokas et al. 2005 but see Baurain et al. 2007).
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Mitochondrial size and gene content are not reliable phylogenetic indicators |
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Can mitochondrial genome size and gene content be used for phylogenetic reconstruction? At first glance there appears to be a trend in animal mtDNA evolution, with both genome size and gene content being reduced during transitions first to the Metazoa and then to the Bilateria (Fig. 2). Indeed, the mitochondrial genome of the choanoflagellate M. brevicollis is 76.6 kbp in size and contains 55 genes, those of most demosponges are between 18 and 25 kbp and contain 40–44 genes, while bilaterian mtDNA is typically between 14 and 16 kpb and has 36–37 genes. Thus, it may be tempting to use mtDNA size and gene content as indicators of phylogenetic relationships (e.g., Dellaporta et al. 2006
). It should be noted, however, that the reduction in mitochondrial DNA size and gene content are only overall trends in animal mitochondrial evolution and that both of these features can vary substantially within different groups.
The largest animal mitochondrial genomes (up to 43 kbp) are found in the placozoan Trichoplax adhaerens (Dellaporta et al. 2006) as well as some very distantly related bilaterian animals, including three species of bark weevil Pissodes (Boyce et al. 1989), the deep-sea scallop Placopecten magellanicus (Snyder et al. 1987), and the nematode Romanomermis culicivorax (Powers et al. 1986), and have clearly evolved independently in these taxa. By contrast, relatively closely related animals often display extensive variation in mtDNA size. For example, the size of the mitochondrial genome in Drosophila melanogaster is 22% (3.5 kpb) larger than that in Drosophila yakuba, while the mtDNA length in four strains of Placozoa differs by as much as 35% (Signorovitch et al. 2007). The fact that mtDNA size can change rapidly and repeatedly within different groups makes it an unreliable character for phylogenetic reconstruction. Furthermore, it is likely that we underestimate the true range of lengths variation in bilaterian mtDNA because of the difficulties associated with PCR amplification and sequencing of the large noncoding region in this molecule (e.g., Lavrov and Brown 2001).
Mitochondrial gene content is also a poor indicator of phylogenetic relationships. In most cases when "extra" genes are present, they are inherited from a common ancestor and thus represent plesiomorphies not informative for phylogenetic reconstruction. By contrast, while the losses of genes from mtDNA are apomorphies, they are known to occur in parallel in different groups, resulting in homoplasious similarities in gene contents (Martin et al. 1998). As an example, a very similar mitochondrial gene content in animal and fungal mtDNA has likely evolved in parallel given that the mitochondrial genome of the choanoflagellate M. brevicollis, the sister group to animals, contains many more genes and probably resembles the mtDNA of the common ancestor of animals and fungi (Burger et al. 2003; Fig. 2). Another example comes from our recent study of mitochondrial genomes in demosponges. This study revealed that two sponges within the family Plakinidae have a remarkably different gene content. The plakinid O. carmela has 44 genes—the largest complement of genes in animal mtDNA—including tatC, a gene for subunit C of twin arginine translocase and genes for 27 tRNAs (Wang and Lavrov 2007). By contrast, mtDNA of P. angulospiculatus, another representative of the same family, contains only 20 genes and lacks tatC as well as 19 of 25 tRNA genes typical for demosponges (Fig. 3; unpublished data).
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Implications for mtDNA evolution |
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Although mitochondrial genome size and gene content offer little information for resolving animal phylogenetic relationships, they do provide insights into mitochondrial genome evolution. Given that the transfer of nuclear genes to mitochondria is limited (in part by differences in genetic code), most additional genes found in demosponge mitochondrial DNA [atp9, tatC, trnI(cau), trnR(ucu)] were likely inherited from their common ancestor with animals. As we explained in an earlier publication (Lavrov et al. 2005
), this is particularly the case for trnI(cau). The maturation of 
encoded by this gene involves a posttranscriptional modification of the cytosine at position 34 to lysidine (2-lysyl-cytidine) (Muramatsu et al. 1988; Weber et al. 1990). This modification is performed by tRNAIle-lysidine synthetase (Soma et al. 2003), an enzyme that is not involved in the maturation of cytoplasmic isoleucine tRNAs (Marck and Grosjean 2002). Because of the dispensable nature of this function for cytoplasmic protein synthesis, it is likely that in evolutionary terms, loss of the metazoan mitochondrial is followed by the loss of the nuclear lysidine synthetase gene, rendering a reacquisition of practically impossible. The presence of trnI(cau) in the mtDNA of both demosponges and placozoans clearly indicates that the common animal ancestor used a less modified genetic code for mitochondrial translation than do most bilaterian animals. It is also likely that this common ancestor had more genes in its mitochondrial genome than any extant metazoan taxa.
Signorovitch et al. (2007) suggest that the common ancestor of all animals possessed a large, noncompact mitochondrial genome. This inference is based on the observation that both placozoans and the choanoflagellate M. brevicollis have large mtDNA and on the assumption that Placozoa forms the sister group to all other animals. There are two potential problems with this inference. First, phylogenetic analysis of global animal relationships based on mtDNA sequence data does not support the placement of Placozoa as the sister group to other animals and instead puts the most basal split in animal phylogeny between bilaterian and nonbilaterian animals (Signorovitch et al. 2007; Wang and Lavrov 2007). Second, even if Placozoa is the sister group to the rest of the animals, the most parsimonious reconstruction of genome size in the common animal ancestor can be grossly misleading given the rapid changes in the size of mtDNA observed among closely related animals as well as the long branch leading to the Placozoa (e.g., Cunningham et al. 1998).
A more interesting question, in my view, is about evolutionary forces that maintain the compact nature of mtDNA in most modern animals. Studies of nonbilaterian animals can help to answer this question because these animals display a different combination of features in their mitochondrial organization. For example, these studies indicate that small size and gene content are not directly linked with an accelerated rate of evolution of mitochondrial sequences. As shown above, while the rate of nucleotide substitutions appears to be extremely low in some nonbilaterian animals, their genomes are still very compact and mostly intron-less (with the exception of Placozoa), challenging the idea that elevated mutation pressure is solely responsible for the evolution of these features in animal mtDNA (Lynch et al. 2006).
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Implications for animal evolution |
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It is commonly believed that the study of nonbilaterian animals can also provide insights into metazoan morphological evolution. This is not because nonbilaterian animals are phylogenetically more "basal" or "lower"—these terms are clearly misleading and should be avoided (Crisp and Cook 2005
)—but because they evolved their bodyplans earlier in metazoan evolution (as revealed by the fossil record) and so may resemble the ancestors of other groups. Following this reasoning, sponges are often considered as living representatives of an intermediate stage in animal evolution that never reached the tissue-level grade of organization. Our recent study of mtDNA from the homoscleromorph O. carmela challenges this idea.
Homoscleromorpha is a small group of sponges that share several features with "higher" animals such as the presence of type-IV collagen, acrosomes in spermatozoa and cross-striated rootlets in the flagellar basal apparatus of larval cells. More importantly, it has been shown that the epithelial cells in homoscleromorph larvae meet all the criteria of a true epithelium in higher animals: cell polarization, apical cell junctions, and a basement membrane (Boury-Esnault et al. 2003). Unless these shared cytological features evolved independently in Homoscleromorpha and Eumetazoa (an unlikely scenario), two alternative explanations are possible for these findings: either Homoscleromorpha is more closely related to other animals than to sponges or most sponges lost the aforementioned features. Our analysis of the mitochondrial genome from the homoscleromorph O. carmela (Wang and Lavrov 2007) strongly rejects the first of these possibilities and instead provides support for the placement of the Homoscleromorpha with other demosponges. This result suggests that the bodyplan of sponges might represent a secondary simplification in animal morphology, potentially due to their sedimentary and water-filtering lifestyle. It should be noted here that this conclusion is still preliminary (e.g., compared to Sperling and Peterson 2007) and needs further investigation.
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Conclusions |
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Two major transitions in animal evolution—the origin of multicellularity and the origin of the Bilateria—correlate with specific changes in animal mtDNA organization. The transition to multicellular animals is associated with the loss of multiple genes from mtDNA and a drastic reduction in the amount of noncoding DNA in the genome, resulting in its "small is beautiful" nature. The transition to bilaterian animals is correlated with multiple changes in the genetic code and associated losses of tRNA genes, the emergence of several genetic novelties, and a large increase in the rates of sequence evolution. Although we do not know whether the observed changes co-occurred with the morphological transitions or evolved independently in different lineages, the remarkable uniformity of animal mtDNA suggests an ongoing evolutionary pressure that maintains its unique organization. Studies of mtDNA in nonbilaterian animals are important because they provide insights not only into the history of mtDNA evolution, but also into the evolutionary factors that shape modern-day animal mtDNA. Although our sampling of mtDNA from nonbilaterian animals is still limited, substantial progress has been made in the last few years that revealed new information about phylogenetics, the evolution of mitrochondrial genomes, and even morphological evolution in animals.
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Acknowledgments |
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I thank Bernd Schierwater, Stephen Dellaporta, and Rob DeSalle for organizing the symposium and its complementary session, Karri Haen and Xiujuan Wang and two anonymous reviewers for valuable comments on an earlier version of this manuscript, and the College of Liberal Arts and Sciences at Iowa State University for funding.
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Footnotes |
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From the symposium "Key Transitions in Animal Evolution" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
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