Origin of the metazoan phyla: molecular clocks confirm paleontological estimates

Abstract

The time of origin of the animal phyla is controversial. Abundant fossils from the major animal phyla are found in the Cambrian, starting 544 million years ago. Many paleontologists hold that these phyla originated in the late Neoproterozoic, during the 160 million years preceding the Cambrian fossil explosion. We have analyzed 18 protein-coding gene loci and estimated that protostomes (arthropods, annelids, and mollusks) diverged from deuterostomes (echinoderms and chordates) about 670 million years ago, and chordates from echinoderms about 600 million years ago. Both estimates are consistent with paleontological estimates. A published analysis of seven gene loci that concludes that the corresponding divergence times are 1,200 and 1,000 million years ago is shown to be flawed because it extrapolates from slow-evolving vertebrate rates to faster-evolving invertebrate rates, as well as in other ways.

Figure 1

Estimated divergence times for selected animal phyla. Mean divergence times are the averages based on 18 gene loci: 673 million years for the protostome–deuterostome divergence and 595 million years for the echinoderm–chordate divergence. Shading extends to the estimates obtained with two different methods of correcting for multiple substitutions. The boundary between Vendian and Cambrian is at 544 My (8).

Figure 2

Rates of molecular evolution (genetic distance versus time) obtained with the data points of Wray et al. (17), but separately for those 0–150 and 300–450 My old. The regression slopes for each of the four loci follow (given in parentheses are F value for the test of equal regression slopes, degrees of freedom, and P; see ref. , p. 499). ATPase 6, 0.00279 and −0.00053 (F = 8.79; df = 1, 101; P < 0.005); NADH 1 = 0.00224 and 0.00019 (F = 33.04; df = 1, 101; P < 0.001); cytochrome oxidase I, 0.00052 and −0.00006 (F = 14.31; df = 1, 116; P < 0.001); and cytochrome oxidase II, 0.00070 and −0.00026 (F = 19.85; df = 1, 322; P < 0.001).

Figure 3

Phylogeny of eubacteria and multicellular kingdoms, with branch lengths arbitrary. The averages for the genetic distances given in table 3 of ref. are 1.50 ± 0.50 between bacteria and animals, which is not greater than 1.40 ± 0.62 between plant and animals or 1.68 ± 0.81 between yeast/mold (protist for one gene) and animals. Assuming that the lineage change is half the genetic distance between taxa, the value of b is about 0, even though it encompasses the evolution from prokaryote to eukaryote and from protist to multicellularity.