Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla - PubMed (original) (raw)
Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla
C B Cameron et al. Proc Natl Acad Sci U S A. 2000.
Abstract
The deuterostome phyla include Echinodermata, Hemichordata, and Chordata. Chordata is composed of three subphyla, Vertebrata, Cephalochordata (Branchiostoma), and Urochordata (Tunicata). Careful analysis of a new 18S rDNA data set indicates that deuterostomes are composed of two major clades: chordates and echinoderms + hemichordates. This analysis strongly supports the monophyly of each of the four major deuterostome taxa: Vertebrata + Cephalochordata, Urochordata, Hemichordata, and Echinodermata. Hemichordates include two distinct classes, the enteropneust worms and the colonial pterobranchs. Most previous hypotheses of deuterostome origins have assumed that the morphology of extant colonial pterobranchs resembles the ancestral deuterostome. We present a molecular phylogenetic analysis of hemichordates that challenges this long-held view. We used 18S rRNA to infer evolutionary relationships of the hemichordate classes Pterobranchia and Enteropneusta. Our data show that pterobranchs may be derived within enteropneust worms rather than being a sister clade to the enteropneusts. The nesting of the pterobranchs within the enteropneusts dramatically alters our view of the evolution of the chordate body plan and suggests that the ancestral deuterostome more closely resembled a mobile worm-like enteropneust than a sessile colonial pterobranch.
Figures
Figure 1
Photographs of the adults of the hemichordate species represented in this study. (a) Ptychodera bahamensis; (b) Harrimania species; (c) Cephalodiscus gracilus individuals; (d) Cephalodiscus gracilus colony. Our results suggest that members of the family Ptychoderidae (a) form one clade of Enteropneusta, whereas the family Harrimanidae (b) plus Pterobranchia (c and d) form another.
Figure 2
Phylogenetic tree of the deuterostomes when sequences with similar evolutionary rates (16 taxa ≤0.12 substitutions per site) were analyzed with
gambit
. Key characters are mapped to the deeper nodes. The deuterostomes form two great clades, one containing the hemichordates and echinoderms and the other made up of urochordates and chordates (cephalochordates and vertebrates). Major differences in adult body plan between Cephalochordata + Vertebrata (myotomes) and Urochordata (tunic) are marked. These results, combined with morphological data, suggest that Chordata should be restricted to Cephalochordata + Vertebrata and that Urochordata is an independent phylum and the sister group to Chordata. Note that the tripartate coelom of hemichordates is considered homologous to the three pairs of echinoderm coeloms.
Figure 3
Analyses of hemichordate phylogeny. Branches are drawn to scale (Kimura two-parameter distances) to emphasize the potential for artifacts because of unequal rate effects. The same topology was obtained from NJ with Kimura two-parameter distances (bootstrap values above each branch),
gambit
paralinear distances with correction for site-to-site variation (bootstrap values below each branch), and
gambit
MP (bootstrap values to the right of each branch). See text for details. Hemichordate classes (bold) and families are indicated (Right). S. barkleyii and H. planktophilus are undescribed species (33).
Similar articles
- Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts.
Cannon JT, Rychel AL, Eccleston H, Halanych KM, Swalla BJ. Cannon JT, et al. Mol Phylogenet Evol. 2009 Jul;52(1):17-24. doi: 10.1016/j.ympev.2009.03.027. Epub 2009 Apr 5. Mol Phylogenet Evol. 2009. PMID: 19348951 - The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data.
Halanych KM. Halanych KM. Mol Phylogenet Evol. 1995 Mar;4(1):72-6. doi: 10.1006/mpev.1995.1007. Mol Phylogenet Evol. 1995. PMID: 7620637 - Tubicolous enteropneusts from the Cambrian period.
Caron JB, Morris SC, Cameron CB. Caron JB, et al. Nature. 2013 Mar 28;495(7442):503-6. doi: 10.1038/nature12017. Epub 2013 Mar 13. Nature. 2013. PMID: 23485974 - Molecular insights into deuterostome evolution from hemichordate developmental biology.
Lowe CJ. Lowe CJ. Curr Top Dev Biol. 2021;141:75-117. doi: 10.1016/bs.ctdb.2020.12.002. Epub 2021 Jan 21. Curr Top Dev Biol. 2021. PMID: 33602496 Review. - Hemichordate models.
Tagawa K. Tagawa K. Curr Opin Genet Dev. 2016 Aug;39:71-78. doi: 10.1016/j.gde.2016.05.023. Epub 2016 Jun 18. Curr Opin Genet Dev. 2016. PMID: 27328429 Review.
Cited by
- Hemichordate cis-regulatory genomics and the gene expression dynamics of deuterostomes.
Pérez-Posada A, Lin CY, Fan TP, Lin CY, Chen YC, Gómez-Skarmeta JL, Yu JK, Su YH, Tena JJ. Pérez-Posada A, et al. Nat Ecol Evol. 2024 Oct 18. doi: 10.1038/s41559-024-02562-x. Online ahead of print. Nat Ecol Evol. 2024. PMID: 39424956 - Chromosomal-level genome assembly and annotation of the tropical sea cucumber Holothuria scabra.
Zhong S, Liu X, Ma X, Chen X, Jiang Y, Zeng M, Zhao L, Huang L, Huang G, Zhao Y, Liu H, Qiao Y. Zhong S, et al. Sci Data. 2024 May 9;11(1):474. doi: 10.1038/s41597-024-03340-x. Sci Data. 2024. PMID: 38724539 Free PMC article. - The origins of gas exchange and ion regulation in fish gills: evidence from structure and function.
Sackville MA, Gillis JA, Brauner CJ. Sackville MA, et al. J Comp Physiol B. 2024 Oct;194(5):557-568. doi: 10.1007/s00360-024-01545-5. Epub 2024 Mar 26. J Comp Physiol B. 2024. PMID: 38530435 Review. - Molecular evidence of anteroposterior patterning in adult echinoderms.
Formery L, Peluso P, Kohnle I, Malnick J, Thompson JR, Pitel M, Uhlinger KR, Rokhsar DS, Rank DR, Lowe CJ. Formery L, et al. Nature. 2023 Nov;623(7987):555-561. doi: 10.1038/s41586-023-06669-2. Epub 2023 Nov 1. Nature. 2023. PMID: 37914929 - Molecular characterization of nervous system organization in the hemichordate acorn worm Saccoglossus kowalevskii.
Andrade López JM, Pani AM, Wu M, Gerhart J, Lowe CJ. Andrade López JM, et al. PLoS Biol. 2023 Sep 19;21(9):e3002242. doi: 10.1371/journal.pbio.3002242. eCollection 2023 Sep. PLoS Biol. 2023. PMID: 37725784 Free PMC article.
References
- Holland P W H, Hacker A M, Williams N A. Philos Trans R Soc London B. 1991;332:185–189. - PubMed
- Turbeville J M, Schulz J R, Raff R A. Mol Biol Evol. 1994;11:648–655. - PubMed
- Halanych K. Mol Phylogenet Evol. 1995;4:72–76. - PubMed
- Halanych K. Syst Biol. 1996;45:223–246.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Molecular Biology Databases