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

Abstract

The colonization of land by tetrapod ancestors is one of the major questions in the evolution of vertebrates. Despite intense molecular phylogenetic research on this problem during the last 15 years, there is, until now, no statistically supported answer to the question of whether coelacanths or lungfish are the closest living relatives of tetrapods. We determined DNA sequences of the nuclear-encoded recombination activating genes (Rag1 and Rag2) from all three major lungfish groups, the Australian Neoceratodis forsteri, the South American Lepidosiren paradoxa and the African lungfish Protopterus dolloi, and the Indonesian coelacanth Latimeria menadoensis. Phylogenetic analyses of both the single gene and the concatenated data sets of RAG1 and RAG2 found that the lungfishes are the closest living relatives of the land vertebrates. These results are supported by high bootstrap values, Bayesian posterior probabilities, and likelihood ratio tests.S ince the discovery in 1938 of the ''living fossil,'' the coelacanth Latimeria chalumnae, a representative of a group of lobe-finned fish thought to have gone extinct Ϸ80 million years ago (1, 2), there has been remarkable interest in this legendary fish by the public and scientists alike. However, the evolutionary relationships of the coelacanths to the other two living groups of lobe-finned fish (Sarcopterygii), the lungfish (Dipnoi), and the land vertebrates (Tetrapoda) remain debated until today. Since its discovery, many comparative morphologists and paleontologists considered the coelacanth to be the closest living relative of the land vertebrates (1-4), although the lungfish were historically thought, and continued to be thought by some researchers, to hold that claim. More recently, however, several analyses began to challenge the sistergroup relationship between the coelacanth and the tetrapods, first on morphological and paleontological grounds (5-7) and later based on molecular phylogenetic analyses (8,9). Palaeontological studies are limited to studying morphological features, and strong phylogenetic inferences are often hindered because of missing data in incomplete fossils. 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 a...

Molecular evidence for the monophyly of East Asian groups of Cyprinidae (Teleostei: Cypriniformes) derived from the nuclear recombination activating gene 2 sequences

“…The RAG2 gene encodes components of the recombinase involved in recombination of immunoglobin and T-cell receptor genes and appears as conserved single copies in all examined vertebrates (Hansen and Kaattari, 1996;Willett et al, 1997). The RAG2 gene has been widely used to evaluate intrageneric and intraspeciWc relationships (Baker et al, 2000;Clements et al, 2004;Hardman, 2004;Lewis-Oritt et al, 2001;Lovejoy and Collette, 2001), and it is also used to reveal higher-level phylogenetic relationships (Brinkmann et al, 2004;Calcagnotto et al, 2005). Although the considerable morphological variability of East Asian cyprinids represents a challenge to phylogenetic analyses based on morphology, we included representative species from all hypothesized subfamilies (Chen, 1998) in our present molecular analysis.…”

Oldest coelacanth, from the Early Devonian of Australia

“…Morphological and molecular sequence data clearly demonstrate that the living coelacanth Latimeria (Actinistia) is the closest relative of lungfishes and tetrapods (Cloutier & Ahlberg 1997;Brinkmann et al 2004). However, the earliest known lungfishes and their relatives (Dipnomorpha) are Early Devonian in age (Lochkovian-Pragian, ca 410-415 Myr ago), as are the onychodonts, another fossil group of basal sarcopterygians (Chang 1982;Chang & Yu 1984;Zhu et al 2001;Zhu & Yu 2004).…”

Behavioral evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes

“…Lungfishes, including P. annectens, are the sister group to living tetrapods (2,4,15), and as such are important for understanding the evolution of movement patterns and limb function in this group. P. annectens is clearly specialized relative to other sarcopterygians in that its fins are longer and more slender than all other known examples (16,17).…”