Molecules, fossils, and the origin of tetrapods

Abstract

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 ...

Molecular Phylogenetic Information on the Identity of the Closest Living Relative(s) of Land Vertebrates

“…These data continued to favor a lungfish+tetrapod grouping albeit with low bootstrap support (51%). However, when the African (Protopterus aethiopicus and Protopterus annectens) and the Australian (Neoceratodus forsteri) lungfishes were included into an extended study of the mitochondrial 12S rRNA gene (Meyer and Dolven 1992), an unresolved coelacanth+lungfish+tetrapod trichotomy (the lungfish+tetrapod clade was favored in the most parsimonious tree but with low bootstrap support of only 48%) resulted (Fig. 4).…”

“…Therefore due to the incomplete sampling of species these studies could not discriminate among any of the three competing hypotheses (reviewed in Meyer 1995). During the past ten years, however, mitochondrial and nuclear sequences have been collected from both the coelacanth and the lungfishes with the explicit goal of resolving this phylogenetic issue (e.g., Gorr et al 1991;Hedges et al 1993;Meyer and Dolven 1992;Meyer and Wilson 1990;Fig. 4).…”

“…B) UPGMA analysis based on b hemoglobin sequences (Gorr et al 1991). C) Maximum parsimony analysis of a mitochondrial 12S rRNA gene fragment (Meyer and Dolven 1992). D) Neighbor-joining analysis of the complete mitochondrial 12S and 16S rRNA genes (Hedges et al 1993).…”

Increased gene expression of a facilitated diffusion urea transporter in the skin of the African lungfish (Protopterus annectens) during massively elevated post-terrestrialization urea excretion

“…In fact, recent evolutionary analyses have hypothesized that lungfish (Subclass Dipnotetrapodomorpha) are phylogenetically the closest relatives to tetrapods (Meyer and Dolven, 1992;Cao et al, 1998;Zardoya et al, 1998;Tohyama et al, 2000), though exact relationships between lungfish, coelocanths and tetrapods remain unclear (Takezaki et al, 2004;Friedman et al, 2007). Furthermore, the environmental circumstances of amphibians and lungfish (amphibious life style, frequent danger of dehydration, ability to aestivate) are similar.…”

“…Given the proposed evolutionary position of the Dipnoi as the closest living relatives to the tetrapods (Meyer and Dolven, 1992;Cao et al, 1998;Zardoya et al, 1998;Tohyama et al, 2000), we also postulated that such a carrier would show greatest similarity in sequence to the UT-As of amphibians. In higher vertebrates, transcriptional control of UT-A expression occurs only very slowly, in response to dietary N changes, for example (Bagnasco, 2005).…”