Limits...
The evolutionary position of nematodes.

Blair JE, Ikeo K, Gojobori T, Hedges SB - BMC Evol. Biol. (2002)

Bottom Line: Instead, we found significant support for the traditional hypothesis, Coelomata.Our result is robust to different rates of sequence change among genes and lineages, different numbers of taxa, and different species of nematodes.We conclude that insects (arthropods) are genetically and evolutionarily closer to humans than to nematode worms.

View Article: PubMed Central - HTML - PubMed

Affiliation: Astrobiology Research Center and Department of Biology, The Pennsylvania State University, University Park, PA 16802, USA. jeb322@psu.edu

ABSTRACT

Background: The complete genomes of three animals have been sequenced by global research efforts: a nematode worm (Caenorhabditis elegans), an insect (Drosophila melanogaster), and a vertebrate (Homo sapiens). Remarkably, their relationships have yet to be clarified. The confusion concerns the enigmatic position of nematodes. Traditionally, nematodes have occupied a basal position, in part because they lack a true body cavity. However, the leading hypothesis now joins nematodes with arthropods in a molting clade, Ecdysozoa, based on data from several genes.

Results: We tested the Ecdysozoa hypothesis with analyses of more than 100 nuclear protein alignments, under conditions that would expose biases, and found that it was not supported. Instead, we found significant support for the traditional hypothesis, Coelomata. Our result is robust to different rates of sequence change among genes and lineages, different numbers of taxa, and different species of nematodes.

Conclusion: We conclude that insects (arthropods) are genetically and evolutionarily closer to humans than to nematode worms.

Show MeSH

Related in: MedlinePlus

Phylogenetic analyses of individual and combined (concatenated) sequence alignments bearing on the position of nematodes. V = vertebrate, A = arthropod, N = nematode, P = platyhelminth. Bootstrap values (>95%) are shown for neighbor-joining, maximum parsimony, and maximum likelihood, respectively; all are indicated for the node joining Homo and Drosophila (=Coelomata). Posterior probabilities are not shown (all highlighted nodes = 1.0). (A) Four-taxon analysis of 100 combined protein alignments (44,214 amino acids), using nematode Caenorhabditis elegans (Chromadorea, Rhabditida, Rhabditoidea, Rhabditidae); the nematode branch is approximately 16% longer than the vertebrate and arthropod branches. (B) Five-taxon analysis of 100 combined proteins includes planarian EST sequences (14,041 amino acids); the nematode branch is approximately 23% longer. Other trees show different representative nematodes. (C) Brugia (Chromadorea, Spirurida, Filarioidea, Onchocercidae), based on 18 combined proteins (4598 amino acids); nematode branch= 15% longer. (D) Trichinella (Enoplea, Trichocephalida, Trichinellidae), based on 6 combined proteins (2261 amino acids); nematode branch = 24% longer than the vertebrate branch and 5% shorter than the arthropod branch. (E) Proportion of individual protein analyses supporting each of the three possible topologies with differing numbers of phyla included (4 taxa = 124 proteins, 5 taxa= 107 proteins, 6 taxa= 66 proteins, >6 taxa = 12 proteins).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC102755&req=5

Figure 2: Phylogenetic analyses of individual and combined (concatenated) sequence alignments bearing on the position of nematodes. V = vertebrate, A = arthropod, N = nematode, P = platyhelminth. Bootstrap values (>95%) are shown for neighbor-joining, maximum parsimony, and maximum likelihood, respectively; all are indicated for the node joining Homo and Drosophila (=Coelomata). Posterior probabilities are not shown (all highlighted nodes = 1.0). (A) Four-taxon analysis of 100 combined protein alignments (44,214 amino acids), using nematode Caenorhabditis elegans (Chromadorea, Rhabditida, Rhabditoidea, Rhabditidae); the nematode branch is approximately 16% longer than the vertebrate and arthropod branches. (B) Five-taxon analysis of 100 combined proteins includes planarian EST sequences (14,041 amino acids); the nematode branch is approximately 23% longer. Other trees show different representative nematodes. (C) Brugia (Chromadorea, Spirurida, Filarioidea, Onchocercidae), based on 18 combined proteins (4598 amino acids); nematode branch= 15% longer. (D) Trichinella (Enoplea, Trichocephalida, Trichinellidae), based on 6 combined proteins (2261 amino acids); nematode branch = 24% longer than the vertebrate branch and 5% shorter than the arthropod branch. (E) Proportion of individual protein analyses supporting each of the three possible topologies with differing numbers of phyla included (4 taxa = 124 proteins, 5 taxa= 107 proteins, 6 taxa= 66 proteins, >6 taxa = 12 proteins).

Mentions: Analyses of the individual protein datasets using neighbor-joining [16] show that most (62%) support Coelomata while 25% support Ecdysozoa and 13% support hypothesis III (Supplemental Table 1, four-taxon analysis). Of the 25 proteins in which support for one of the three hypotheses is significant (≥ 95%), the results are 84% (21 proteins), 16% (4), and 0%, respectively; for those ten proteins with a highly significant (≥ 99%) topology, the results are 90% (9 proteins), 10% (1), and 0%, respectively. The four proteins showing significant support (>95%) for a hypothesis other than Coelomata were reanalyzed using maximum parsimony and maximum likelihood; bootstrap values were not significant using other methods. Such divided results are typical of single-gene analyses because of limited information (~400 amino acids), necessitating combined analysis. Coelomata was supported significantly (100% bootstrap confidence, posterior probability = 1.0) when the 100 four-taxon protein alignments were concatenated and analyzed using neighbor-joining, maximum parsimony, maximum likelihood, and Bayesian inference (Fig. 2A). Using the Shimodaira-Hasegawa (SH) test [17], this maximum likelihood topology was significantly different from the alternative hypotheses of Ecdysozoa (P < 0.001) and Hypothesis III (P < 0.001). These results agree with earlier studies involving 10–36 nuclear proteins [8,9,11].


The evolutionary position of nematodes.

Blair JE, Ikeo K, Gojobori T, Hedges SB - BMC Evol. Biol. (2002)

Phylogenetic analyses of individual and combined (concatenated) sequence alignments bearing on the position of nematodes. V = vertebrate, A = arthropod, N = nematode, P = platyhelminth. Bootstrap values (>95%) are shown for neighbor-joining, maximum parsimony, and maximum likelihood, respectively; all are indicated for the node joining Homo and Drosophila (=Coelomata). Posterior probabilities are not shown (all highlighted nodes = 1.0). (A) Four-taxon analysis of 100 combined protein alignments (44,214 amino acids), using nematode Caenorhabditis elegans (Chromadorea, Rhabditida, Rhabditoidea, Rhabditidae); the nematode branch is approximately 16% longer than the vertebrate and arthropod branches. (B) Five-taxon analysis of 100 combined proteins includes planarian EST sequences (14,041 amino acids); the nematode branch is approximately 23% longer. Other trees show different representative nematodes. (C) Brugia (Chromadorea, Spirurida, Filarioidea, Onchocercidae), based on 18 combined proteins (4598 amino acids); nematode branch= 15% longer. (D) Trichinella (Enoplea, Trichocephalida, Trichinellidae), based on 6 combined proteins (2261 amino acids); nematode branch = 24% longer than the vertebrate branch and 5% shorter than the arthropod branch. (E) Proportion of individual protein analyses supporting each of the three possible topologies with differing numbers of phyla included (4 taxa = 124 proteins, 5 taxa= 107 proteins, 6 taxa= 66 proteins, >6 taxa = 12 proteins).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC102755&req=5

Figure 2: Phylogenetic analyses of individual and combined (concatenated) sequence alignments bearing on the position of nematodes. V = vertebrate, A = arthropod, N = nematode, P = platyhelminth. Bootstrap values (>95%) are shown for neighbor-joining, maximum parsimony, and maximum likelihood, respectively; all are indicated for the node joining Homo and Drosophila (=Coelomata). Posterior probabilities are not shown (all highlighted nodes = 1.0). (A) Four-taxon analysis of 100 combined protein alignments (44,214 amino acids), using nematode Caenorhabditis elegans (Chromadorea, Rhabditida, Rhabditoidea, Rhabditidae); the nematode branch is approximately 16% longer than the vertebrate and arthropod branches. (B) Five-taxon analysis of 100 combined proteins includes planarian EST sequences (14,041 amino acids); the nematode branch is approximately 23% longer. Other trees show different representative nematodes. (C) Brugia (Chromadorea, Spirurida, Filarioidea, Onchocercidae), based on 18 combined proteins (4598 amino acids); nematode branch= 15% longer. (D) Trichinella (Enoplea, Trichocephalida, Trichinellidae), based on 6 combined proteins (2261 amino acids); nematode branch = 24% longer than the vertebrate branch and 5% shorter than the arthropod branch. (E) Proportion of individual protein analyses supporting each of the three possible topologies with differing numbers of phyla included (4 taxa = 124 proteins, 5 taxa= 107 proteins, 6 taxa= 66 proteins, >6 taxa = 12 proteins).
Mentions: Analyses of the individual protein datasets using neighbor-joining [16] show that most (62%) support Coelomata while 25% support Ecdysozoa and 13% support hypothesis III (Supplemental Table 1, four-taxon analysis). Of the 25 proteins in which support for one of the three hypotheses is significant (≥ 95%), the results are 84% (21 proteins), 16% (4), and 0%, respectively; for those ten proteins with a highly significant (≥ 99%) topology, the results are 90% (9 proteins), 10% (1), and 0%, respectively. The four proteins showing significant support (>95%) for a hypothesis other than Coelomata were reanalyzed using maximum parsimony and maximum likelihood; bootstrap values were not significant using other methods. Such divided results are typical of single-gene analyses because of limited information (~400 amino acids), necessitating combined analysis. Coelomata was supported significantly (100% bootstrap confidence, posterior probability = 1.0) when the 100 four-taxon protein alignments were concatenated and analyzed using neighbor-joining, maximum parsimony, maximum likelihood, and Bayesian inference (Fig. 2A). Using the Shimodaira-Hasegawa (SH) test [17], this maximum likelihood topology was significantly different from the alternative hypotheses of Ecdysozoa (P < 0.001) and Hypothesis III (P < 0.001). These results agree with earlier studies involving 10–36 nuclear proteins [8,9,11].

Bottom Line: Instead, we found significant support for the traditional hypothesis, Coelomata.Our result is robust to different rates of sequence change among genes and lineages, different numbers of taxa, and different species of nematodes.We conclude that insects (arthropods) are genetically and evolutionarily closer to humans than to nematode worms.

View Article: PubMed Central - HTML - PubMed

Affiliation: Astrobiology Research Center and Department of Biology, The Pennsylvania State University, University Park, PA 16802, USA. jeb322@psu.edu

ABSTRACT

Background: The complete genomes of three animals have been sequenced by global research efforts: a nematode worm (Caenorhabditis elegans), an insect (Drosophila melanogaster), and a vertebrate (Homo sapiens). Remarkably, their relationships have yet to be clarified. The confusion concerns the enigmatic position of nematodes. Traditionally, nematodes have occupied a basal position, in part because they lack a true body cavity. However, the leading hypothesis now joins nematodes with arthropods in a molting clade, Ecdysozoa, based on data from several genes.

Results: We tested the Ecdysozoa hypothesis with analyses of more than 100 nuclear protein alignments, under conditions that would expose biases, and found that it was not supported. Instead, we found significant support for the traditional hypothesis, Coelomata. Our result is robust to different rates of sequence change among genes and lineages, different numbers of taxa, and different species of nematodes.

Conclusion: We conclude that insects (arthropods) are genetically and evolutionarily closer to humans than to nematode worms.

Show MeSH
Related in: MedlinePlus