A phylogenetic analysis of the 18S ribosomal RNA sequence of the coelacanth Latimeria chalumnae

Stock, David W.; Moberg, K D; Maxson, Linda R.; Whitt, Gregory S.

doi:10.1007/bf00007447

Cited by 30 publications

(17 citation statements)

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“…17 and 18). Fragments of both 18S and 28S ribosomal RNA genes were assayed in the past to address the question on the origin of tetrapods (16,19,20). These studies supported the sister group relationship of lobe-finned fishes to tetrapods, but they were typically unable to distinguish which sarcopterygian fishes were more akin to tetrapods because they often did not include either the lungfishes or the coelacanth (for review, see ref.…”

mentioning

confidence: 99%

Evolutionary relationships of the coelacanth, lungfishes, and tetrapods based on the 28S ribosomal RNA gene.

Zardoya

Meyer

1996

Proc. Natl. Acad. Sci. U.S.A.

109

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The origin of land vertebrates was one of the major transitions in the history of vertebrates. Yet, despite many studies that are based on either morphology or molecules, the phylogenetic relationships among tetrapods and the other two living groups of lobe-finned fishes, the coelacanth and the lungfishes, are still unresolved and debated. Knowledge of the relationships among these lineages, which originated back in the Devonian, has profound implications for the reconstruction of the evolutionary scenario of the conquest of land. We collected the largest molecular data set on this issue so far, about 3,500 base pairs from seven species of the large 28S nuclear ribosomal gene. All phylogenetic analyses (maximum parsimony, neighbor-joining, and maximum likelihood) point toward the hypothesis that lungfishes and coelacanths form a monophyletic group and are equally closely related to land vertebrates. This evolutionary hypothesis complicates the identification of morphological or physiological preadaptations that might have permitted the common ancestor of tetrapods to colonize land. This is because the reconstruction of its ancestral conditions would be hindered by the difficulty to separate uniquely derived characters from shared derived characters in the coelacanth/lungfish and tetrapod lineages. This molecular phylogeny aids in the reconstruction of morphological evolutionary steps by providing a framework; however, only paleontological evidence can determine the sequence of morphological acquisitions that allowed lobefinned fishes to colonize land.The origin of land vertebrates is a question that has fascinated paleontologists and comparative morphologists for several decades. However, this issue is still debated because of the complexity of the series of morphological and physiological modifications that were involved in the transition of life in water to life on land, the difficulty in identifying homologous characters in fragmentary fossils, a general paucity of fossils, and the rapidity with which land was conquered (for reviews, see refs. 1-4). Nonetheless, it is generally accepted that lobe-finned fishes (Sarcopterygii), which also include the tetrapod lineage (5), form a monophyletic group. Ray-finned fishes (Actinopterygii) are only distantly related to tetrapods (6, 7). To better understand the origin of tetrapods, their phylogenetic relationships to other lineages of lobe-finned fishes need to be agreed upon. It is likely that an extinct lineage of rhipidistians (a major group of Sarcopterygian fishes) might have been the direct ancestor of tetrapods rather than any living lineage of lobe-finned fishes (refs. 3 and 8; for review, see ref. 4). Coelacanths (Actinistia) were traditionally classified with rhipidistians in the Crossopterygii (e.g., ref. 8) and, therefore, many believed that they are the closest living relatives of tetrapods (e.g., ref. 9). However, other researchers (e.g., refs. 7 and 10), based on morphological evidence, also proposed that lungfishes are the closest living relat...

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confidence: 99%

Evolutionary relationships of the coelacanth, lungfishes, and tetrapods based on the 28S ribosomal RNA gene.

Zardoya

Meyer

1996

Proc. Natl. Acad. Sci. U.S.A.

109

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“…It is not clear whether these genes will be able to resolve the pattern of relations, however. The 18S gene evolves too slowly and sporadically (see also Stock et al 1991), and the 16S rRNA gene evolves too rapidly and shows much length variation that hinders optimal alignments. Longer portions of the mitochondrial 12S rRNA gene and sequences of nuclear and mitochondrial proteincoding genes seem to hold the greatest promise for providing data that might resolve this question with statistical confidence.…”

Section: Resultsmentioning

confidence: 99%

“…Previous molecular analyses did not settle the issue because they did not include a lungfish (Maeda et al 1984;Hillis and Dixon 1989). Since our initial study (Meyer and Wilson 1990), additional molecular data have been published (Gorr et al 1991;Stock et al 1991) but could not resolve the branching order because of the inadequacy of the molecule or the methods of phylogenetic reconstruction chosen (Meyer and Wilson 1991;Sharp et al 1991;Stock and Swofford 1991 Meyer and Wilson (1990) are several. Normark et al (1991) sequenced a smaller piece of cytochrome b; they did not sequence the 12S gene and did not include it into their analysis; they hence had fewer phylogenetically informative sites than Meyer and Wilson (1990) to investigate the coelacanthlungfish-tetrapod question.…”

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confidence: 99%

Molecules, fossils, and the origin of tetrapods

Meyer

Dolven

1992

J Mol Evol

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Summary. Since the discovery of the coelacanth, L a t i m e r i a c h a l u m n a e , more than 50 years ago, paleontologists and comparative morphologists have debated whether coelacanths or lungfishes, two groups of lobe-finned fishes, are the closest living relatives of land vertebrates (Tetrapoda). Previously, Meyer and Wilson (1990) determined partial DNA sequences from two conservative mitochondrial genes and found support for a close relationship of lungfishes to tetrapods. We present additional D N A sequences from the 12S r R N A mitochondrial gene for three species of the two lineages of lungfishes that were not represented in the first study: Protopterus a n n e c t e n s a n d Protopterus aethiopicus from Africa and N e o c e r a t o d u s forsteri (kindly provided by B. Hedges and L. Maxson) from Australia. This extended data set tends to group the two lepidosirenid lungfish lineages (Lepidosiren and Protopterus) with N e o c e r a t o d u s as their sister group. All lungfishes seem to be more closely related to tetrapods than the coelacanth is. This result appears to rule out the possibility that the coelacanth lineage gave rise to land vertebrates. The common ancestor of lungfishes and tetrapods might have possessed multiple morphological traits that are shared by lungfishes and tetrapods [Meyer and Wilson (1990) listed 14 such traits]. Those traits that seem to link L a t i m e r i a and tetrapods are arguably due to convergent evolution or reversals and not to common descent. In this way, the molecular tree facilitates an evolutionary interpretation of the morphological differences among the living forms. We recommended that the extinct groups of lobe-finned fishes be placed onto the molecular tree that has lungfishes and not the coelacanth more closely related to tetrapods. The placement of fossils would help to furOffprint requests to: Axel Meyer ther interpret the sequence of morphological events and innovations associated with the origin of tetrapods but appears to be problematic because the quality of fossils is not always high enough, and differences among paleontologists in the interpretation of the fossils have stood in the way of a consensus opinion for the branching order among lobefinned fishes. Marshall and Schultze (1992) criticized the morphological analysis presented by Meyer and Wilson (1990) and suggest that 13 of the 14 morphological traits that support the sister group relationship of lungfishes and tetrapods are not shared derived characters. Here we present further alternative viewpoints to the ones of Marshall and Schultze (1992) from the paleontological literature. We argue that all available information (paleontological, neontological, and molecular data) and rigorous cladistic methodology should be used when relating fossils and extant taxa in a phylogenetic framework. K e y w o r d s : Polymerase chain reaction --12S rRNA --Coelacanth --L a t i m e r i a c h a l u m n a e -- Ray-finned fishes --Lungfishes --L e p i d o s i r e n --Protopterus --N e o c e r a t o d u s ...

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“…Tree-2 is based on the model [ray-finned fish (lungfish (coelacanth, tetrapod))] (Miles 1975;Hennig 1983;Fritsch 1987;Schultze 1987;Gorr et al 1991; see text). Tree-3 is based on the model [ray-finned fish ((lungfish, coelacanth) tetrapod)] (Northcutt 1987;Chang 1991). cleotide and amino acid sequences of various genes were analyzed in an attempt to clarify the origin of tetrapods; mitochondrial 12S rRNA (Meyer and Wilson 1990;Meyer and Dolven 1992), mitochondrial apocytochrome b (cyt b) (Meyer and Wilson 1990;Nomark et al 1991), hemoglobins (Gorr et al 1991;and see also Forey 1991;Stock and Swofford 1991;Sharp et al 1991;Meyer and Wilson 1991), and 18S rRNA (Stock et al 1991) have been analyzed. However, the relationship among coelacanths, lungfishes, and tetrapods has remained obscure.…”

Section: Tree-2~mentioning

confidence: 99%

“…Moreover, the o~ hemoglobin data also support the coelacanth/lungfish clade only slightly (Tree-3). The serious problem with hemoglobin data is that the distinction between orthologous and paralogous relations is not clear (Forey 1991); 18S rRNA data (Stock et al 1991) could not clarify this relationship.…”

Section: Phylogenetic Analysis Of Mitochondrial Genesmentioning

confidence: 99%

Relationship among coelacanths, lungfishes, and tetrapods: A phylogenetic analysis based on mitochondrial cytochrome oxidase I gene sequences

et al. 1994

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To clarify the relationship among coelacanths, lungfishes, and tetrapods, the amino acid sequences deduced from the nucleotide sequences of mitochondrial cytochrome oxidase subunit I (COI) genes were compared. The phylogenetic tree of these animals, including the coelacanth Latimeria chalumnae and the lungfish Lepidosiren paradoxa, was inferred by several methods. These analyses consistently indicate a coelacanth/lungfish clade, to which little attention has been paid by previous authors with the exception of some morphologists. Overall evidence of other mitochondrial genes reported previously and the results of this study equally support the coelacanth/lungfish and lungfish/tetrapod clades, ruling out the coelacanth/tetrapod clade.

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A phylogenetic analysis of the 18S ribosomal RNA sequence of the coelacanth Latimeria chalumnae

Cited by 30 publications

References 70 publications

Evolutionary relationships of the coelacanth, lungfishes, and tetrapods based on the 28S ribosomal RNA gene.

Evolutionary relationships of the coelacanth, lungfishes, and tetrapods based on the 28S ribosomal RNA gene.

Molecules, fossils, and the origin of tetrapods

Relationship among coelacanths, lungfishes, and tetrapods: A phylogenetic analysis based on mitochondrial cytochrome oxidase I gene sequences

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