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

Abstract

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...

Limitations of Metazoan 18S rRNA Sequence Data: Implications for Reconstructing a Phylogeny of the Animal Kingdom and Inferring the Reality of the Cambrian Explosion

“…The unpaired regions (loops, bulges, and other) are A-rich, reflecting the possible interactions of these regions with rRNA subunits and ribosomal proteins (Gutell et al 1985). These results are consistent with previous rDNA analyses performed at different phylogenetic scales (Vawter and Brown 1993;Orti et al 1996;Zardoya and Meyer 1996;Friedrich and Tautz 1997) and reveal that the functional constraints on various regions within the 18S rRNA molecule may render these regions nonindependent from one another (Wheeler and Honeycutt 1988;Orti et al 1996). This Fig.…”

Coelacanth genomes reveal signatures for evolutionary transition from water to land

“…2), in which lungfishes are also included. Indeed, molecular phylogenetic studies clearly indicate that coelacanths and lungfishes are more closely related to tetrapods than to teleost fishes (e.g., Zardoya and Meyer 1996), whereas the branching order of coelacanths, lungfishes, and tetrapods is still controversial (Takezaki et al 2004). The karyotype of L. chalumnae, which was reported to be 48 chromosomes including microchromosomes, is similar to that of frogs and other species such as turtles or birds, further supporting the phylogenetic closeness of the coelacanth with tetrapods (Bogart et al 1994).…”

Nuclear protein-coding genes support lungfish and not the coelacanth as the closest living relatives of land vertebrates

“…The most recent paleontological evidence demonstrated that the lungfish represent an ancient lineage and that several of the features defining this group remained highly conserved throughout the entire evolutionary history of land vertebrates (10). The majority of palaeontological studies published during the last decade suggest that lungfish (Dipnoi) are the closest living relatives of the tetrapods or, alternatively, that coelacanths and lungfish form a monophyletic group that is equally closely related to the land vertebrates (11,12).A wealth of molecular phylogenetic studies addressed the tetrapod origin question, first based on mitochondrial DNA data by using partial gene sequences, single genes, or a few genes, and more recently, based on complete mitochondrial genomes (9,(13)(14)(15)(16)(17)(18). Most of these mitochondria-based molecular phylogenetic studies favored the lungfish as the closest living relatives of tetrapods.…”

“…A wealth of molecular phylogenetic studies addressed the tetrapod origin question, first based on mitochondrial DNA data by using partial gene sequences, single genes, or a few genes, and more recently, based on complete mitochondrial genomes (9,(13)(14)(15)(16)(17)(18). Most of these mitochondria-based molecular phylogenetic studies favored the lungfish as the closest living relatives of tetrapods.…”