Origin of Vertebrates

by

Andrés Galera

• LAST MODIFIED: 24 July 2024
• DOI: 10.1093/obo/9780199941728-0155

Introduction

Vertebrates have inhabited the Earth for at least 400 million years, first appearing during the Cambrian period. Initially, as the name indicates, the representative anatomical characteristic of the group is an internal bony structure formed by vertebrae surrounding the spinal corp, that is, the vertebral column. It was the French naturalist Jean-Baptiste Lamarck who had the ingenious idea of using this feature as a distinctive classificatory element. The nomenclature became official in 1801. Animals were then forever to be separated into vertebrates and invertebrates—a simple, effective, and convenient formula. With this differentiation, Lamarck highlights a substantial morphological fact. The animal kingdom has two anatomical outlines adapted to life. According to Lamarckian evolutionary theory, they were typologies diversified from a common origin caused by the environment. In 1859, Charles Darwin formulated his theory of evolution by natural selection. Similar in approach but with a different mechanism to explain the origin of species through continuous and selective morphological changes. Within the new Darwinian order, embryologists such as Anton Dohrn, William Bateson, Francis Balfour, Walter Gaskell, Alexander Kowalevsky, and Ray Lankester turned morphogenesis into the stage on which to study transformation. No doubt, knowing what happened and how it happened will be key questions for the development of evolutionary theory. Proving the invertebrate–vertebrate morphological transition, unimaginable to the naked eye, was fundamental to its validation. Who is the ancestor, how does the transformation occur, what phylogenetic lines does it represent, and which groups of extant invertebrates are closest to the earliest stage are questions that have shaped the research on the origin of vertebrates that began in the 19th century. Since then, clearing up the unknowns has been a complex biological problem that has had diverse interpretations and discordant answers. This intellectual discussion was based fundamentally and firstly by data from embryonic morphology, and later also by biochemical, genetic, and palaeontological data. Hypotheses, ideas, models, and theories all contribute to an unfinished debate.

General Overview

The theory of evolution has a unique challenge: to explain how the complex anatomy of vertebrates arose from invertebrate species to generate a new body model. Although not the beginning, it was in the 1860s, at the beginning of the Darwinian era, that morphogenesis crystallized as a phylogenetic argument of reference. Advances in microscopy made this possible. During this time, the biologist Alexander Kowalevsky presented the ascidian theory, attributing the role of ancestor to the tunicates. Discoveries in embryonic morphology continued. Other phylogenies established the connection in different invertebrate lineages leading to, for example, the arthropod theory, the auricularia theory, the enteropneusta theory, and the nemertean theory. Lankester 1888 discusses the subject as a protagonist. Bowler 1989 and Bowler 1996 offer a worthy modern analysis. In the first decades of the 20th century, a new embryological approach based on heterochrony emerged: changes in ontogenetic rhythm. It was proposed by Walter Garstang who was studying the ontogeny of marine invertebrates characterized by successive larval metamorphoses. The differentiated development of the larva, acquiring reproductive capacity, would have originated the phyletic lineage of vertebrates from a tunicate larva. Holland 2011 analyzes the topic. Gould 1977 made heterochrony an evolutionary benchmark. In the 1930s, paleontology became an integral part of the debate. Fossil carpoids—the present-day subphylum Homalozoa—were a substantial element. They are an extinct group of marine invertebrates similar to echinoderms but without radial symmetry. Linking paleontology and embryology, Swedish zoologist Torsten Gislén pointed out the similarities with the chordate body plan. In the mid-1960s, paleontologist Richard Jefferies continued the approach by applying cladistics. The result was the calcichordate theory: today’s chordates evolved in independent lineages from carpoids. Jefferies 1986, cited under Textbooks, offers a complete summary. The theory continues to generate controversy despite its widespread rejection since the 1990s. Gee 1996, cited under Textbooks, provides a thorough analysis. In the 1960s, molecular biology was introduced as a solution to the problem of the vertebrate origin by comparing variations in the genetic code. In more recent times, the sequencing of the amphioxus genome in Putnam, et al. 2008 has been a significant evolutionary contribution. This cephalochordate would represent the closest extant species to the common chordate ancestor. Before that, the authors of Dehal, et al. 2002 sequenced the ascidian genome. Around the same time, Holland and Chen 2001 evaluated advances in evolutionary molecular genetics and microanatomy. Since the 1980s, evolutionary developmental biology (evo-devo) has become the guiding evolutionary formula. Synthetically, the discipline links genome and ontogeny. In other words, it analyzes the genetic changes that modify embryogenesis to produce new body plans. In this context, studies such as Holland and García-Fernández 1996 also point to amphioxus as the present-day representative of the vertebrate evolutionary past. The vertebrate origin remains a complex and thrilling question calling for novel revelations. Gee 2001 proposes that the common ancestor of the deuterostomes would have been a segmented animal with pharyngeal clefts, an approach that substantially changes vertebrate evolutionary origins.

• Bowler, P. J. 1989. Development and adaptation: Evolutionary concepts in British morphology, 1870–1914. British Journal for the History of Science 22.3: 283–297.

  DOI: 10.1017/S0007087400026169

  Analyzes the ideas of biologists such as E. Ray Lankester, Francis M. Balfour, Adam Sedgwick, Ernest W. McBride, and William Bateson, who all played leading roles in the debate on the origin of vertebrates during the second half of the 19th century. The central aim of the study is to answer a general question about the intrinsic identity of these evolutionary morphologists: Were they Darwinian and did they develop the research program for Origin of Species?

• Bowler, P. J. 1996. Life’s splendid drama. Chicago and London: The Univ. of Chicago Press.

  Analyzes the origin of vertebrates as a fundamental element in the process of reconstructing the past that evolutionary biology developed from 1860 to 1940. “Vertebrate Origins” is the title of the extensive chapter devoted not only to the subject, analyzing the different stages, theories, and studies, but also to the scientific significance that the invertebrate–vertebrate biological nexus had for the theory of evolution within the Darwinian framework. A basic book for thinking about the present by knowing the past.

• Dehal, P., Y. Satou, R. K. Campbell, et al. 2002. The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins. Science 298:2157–2167.

  DOI: 10.1126/science.1080049

  Presents the genome sequence of the ascidian Ciona intestinalis. It contains 16,000 protein-coding genes and an estimated 160 million base pairs. Analysis determines the existence of vertebrate gene families present in Ciona with a single representative, and the existence of other families with multiple genes in both groups but with little to no correspondence. This is representative of genomic diversification independent of the ancestral chordate in both lineages.

• Gee, H. 2001. Deuterostome phylogeny: The context for the origin and evolution of chordates. In Major events in early vertebrate evolution: Palaeontology, phylogeny, genetics and development. Edited by P. E. Ahlberg, 1–14. London and New York: Taylor & Francis.

  Critical revision of the origin of vertebrates based on new data indicating the existence of characters such as metameric segmentation and pharyngeal clefts in the common ancestor of all deuterostomes. The finding has a certain phylogenetic significance considering the re-emergence of the Ambulacraria clade, which reunites echinoderms with hemichordates, and a rearrangement of carpoids as direct ancestors of echinoderms. The deuterostomes would have split into two major evolutionary lines, one leading to the Ambulacraria and the other to the chordates.

• Gould, S. J. 1977. Ontogeny and phylogeny. Cambridge, MA, and London: Harvard Univ. Press.

  A seminal book. A heterodox reference text on biological evolution, it constitutes a turning point in evolutionary biology. Explores the dilemma of speciation by relating morphogenesis and evolution as a heterochronic event in its various modes of progenesis, neoteny, hypermorphosis, acceleration, proportioned dwarfism, and proportioned gigantism. Simply put, changes in the rhythm of ontogeny lead to new self-sufficient morphologies. Taken as a whole, the work is presented as a critical account of 20th-century evolutionary thought threaded with an in-depth analysis of preceding ideas.

• Holland, N. D. 2011. Walter Garstang: A retrospective. Theory in Biosciences 130:247–258.

  DOI: 10.1007/s12064-011-0130-3

  An excellent retrospective analysis about an unorthodox controversial evolutionist in the past and the present. Certainly, Garstang’s ideology comprises some positive elements, in particular the application of the concept of heterochrony and the reformulation of the biogenetic law. However, his evolutionary theory on the vertebrate origin from the tunicate tadpole larva is not supported by modern developmental embryology and molecular biology. Holland presents an extensive and rigorous analysis of the ideas of a leading figure in evolutionary biology during the first half of the 20th century.

• Holland, N. D., and J. Chen. 2001. Origin and early evolution of the vertebrates: New insights from advances in molecular biology, anatomy, and palaeontology. BioEssays 23:142–151.

  DOI: 10.1002/1521-1878(200102)23:2<142::AID-BIES1021>3.0.CO;2-5

  A review of the vertebrate origin based on new molecular and microanatomical data obtained from the study of soft-bodied fossils found from Lower Cambrian sites in southern China. Homologies detected between the bodies of vertebrates and invertebrate chordates have provided information on the vertebrate ancestor, supporting, for example, the importance of the neural crest as a driving element of vertebrate morphology.

• Holland, P. W. H., and J. García-Fernández. 1996. Hox genes and chordate evolution. Developmental Biology 173:382–395.

  DOI: 10.1006/dbio.1996.0034

  Investigates the role of the Hox genes during embryonic development. These genes belong to the homeobox family of transcription factors, which regulate morphogenesis and early cell differentiation. Analysis is aimed at defining the relationship between Hox gene diversity and the genomic structure and embryonic expression of these genes in chordates and hemichordates. Presents two main analytical lines: modification of Hox gene expression translated into evolutionary identity changes and the relationship between gene duplication processes and the origin of vertebrates.

• Lankester, E. R. 1888. Vertebrata. In Encyclopaedia Britannica. Edited by W. R. Smith, ninth edition, 24, 178–188. Edinburgh: Adam and Charles Black.

  Outlines the evolutionary implications of the advances made in the fields of invertebrate anatomy and ontogeny during the second half of the 19th century. Discoveries that were necessary for the first reconstructions of the vertebrate family tree. Presents two relevant conceptual aspects: the systematic renewal of the vertebrate phylum and the application of the concept of degeneration to explain the evolution of the species associated with the invertebrate–vertebrate connection. Forms that would represent secondary branches with their own structural modifications.

• Putnam, N., T. Butts, D. E. K. Ferrier, et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071.

  DOI: 10.1038/nature06967

  Presents the genome sequence of amphioxus, comprising 21,900 genes. Through comparisons with orthologous genes—which have equivalent functions in different organisms—the study reveals key features of the genome of the last common ancestor of all chordates that presumably lived around 550 million years ago. It would have been an ancestor that lived during the Cambrian that gave rise to the lineage leading to the cephalochordates (amphioxus), urochordates, and vertebrates. The three would have formed a monophyletic group, although the cephalochordates would have diverged into a group with their own morphology before the separation of the urochordates and the vertebrates.