Bio 205 Comparative Vertebrate Anatomy

Lecture 3 : Vertebrate Origins

What are Vertebrates?

The vertebrata include all animals with a segmented vertebral column, which includes gnathostomes + lampreys. But this excludes hagfishes, which have traditionally been considered vertebrates! What are the synapomorphies that unite Vertebrata (gnathostomes + lampreys) with hagfishes? Basically, a head skeleton, tripartite brain, and ectodermal placodes. Notice that all of these have something to do with advances in locomotion (ectodermal placodes develop into special sensory organs such as equilibrium, hearing, taste/smell, vision which facilitate moving forward to find things and not bump into things. The development of the brain allows for increased processing of this sensory input. The head skeleton provides a protective shell for the sensory organs). The group (hagfishes + vertebrates) is called Craniata (the craniates).

So who are the craniates related to?

Hypotheses of Vertebrate origins:The question "from which invertebrate did vertebrates arise?" has boggled comparative biologists for 200 years. Much of the history is retold in a recent book, Before the Backbone : Views on the Origin of the Vertebrates, by Henry Gee.

Upside down Arthropod / Annelid hypothesis

in 1822 Etienne Geoffroy St. Hillaire argued that the body-plans of arthropods and vertebrates were fundmentally alike except that one was the dorsoventral inverse of the other. The essential theory was critized by many but elaborated with modifications by others (Nübler-Jung & Arendt, 1994).

Anton Dorn in 1875 argued that vertebrates evolved from annelid-like animals, which are segmented (as are vertebrates), and, following St. Hillaire, suggested that the dorsoventral axis reversed itself on the lineage to vertebrates.

Picture from Vertebrate Body to come.

The upside down arthropod / annelid hypothesis has been criticized because vertebrates differ from both annelids and arthropods in several important developmental features including the fate of the blastopore and the type of cleavage. These will be discussed later in the development lecture. It should suffice that developmental data suggest that vertebrates are allied with Deuterostomes, which include echinoderms (starfish, sea urchins, sea cucumbers), hemichordates (acorn worms), urochordates (sea squirts and allies), and cephalochordates (amphioxus).

The upside down arthropod / annelid hypothesis can be more rigorously tested with a phylogeny (click here to see the similar but different Tree of life phylogeny of the bilateria with great links to other WWW sites):

This cladogram, which is a composite of 18S rDNA molecular phylogenies, suggests that the ancestor of vertebrates was not an annelid, or an arthropod, which are both protostomes, but was some kind of deuterostome.

Deuterostome characters

These are the classic characters that differentiate deuterostomes from protostomes (see cladogram above)

1. radial cleavage - during the earliest stage of development in animals, a stage called "cleavage" (because the cells cleave or divide into 2 cells) there are two different ways to do this, spirally and radially. Protostomes have spiral cleavage. See below.
2. mouth develops independently of blastopore (hence name). In protostomes, the mouth develops from the blastopore. See below.
3. enterocoely (the coelom arises by an outpocketing of the archenteron). In Protostomes, the coelom arises by the splitting of the mesoderm. See below.

Radial vs. spiral cleavage

Click on image above to see a movie. In the movie use the scroll button to play at your own speed.

Gastrulation: Protostome vs. Deuterostome

The figure below illustrates gastrulation in an echnioderm. Some of these terms will make more sense after we discuss embryology. Gastrulation is the devlopment of the three principle embryonic layers: the ectoderm, the mesoderm, and the endoderm. The mesoderm and endoderm are formed when cells on the outside of the blastula (the ball of cells) move inside through an opening, the blastopore. Invaginating cells create a tube within the ball called the archenteron (primitive gut). In protostomes, the mouth is formed from the blastopore. In deuterostomes, the mouth forms on the opposite side of the embryo by the destruction of cells between the outer ectoderm and the archenteron.

Coelom formation - enterocoely vs. schizocoely

The coelom is a cavity within the body that surrounds the gut. Mesoderm lines the body wall and covers the gut, so the coelom forms is technically, a cavity within the mesoderm. In schizocoely, the mesoderm just splits to create the coelom. In enterocoely (the deuterostome character), the mesoderm is an outpocketing of the archenteron and so forms with a cavity. See figure.

Problems with this morphological concept of protostome vs. deuterostome

Many deuterostomes (including us) have schizocoelic coelom formation and neither our mouth nor our anus devops from the blastopore. Nevertheless, molecular phylogenetic evidence supports the monophyly of the deuterostomes (but not necessarily the protostomes).

Deuterostomes - cast of characters - click on link to see picture

Echinoderms - starfish, brittlestars, sea urchins, etc.

hemichordates - pterobranchs, acorn worms

Urochordates - tunicates or "sea squirts", salps, etc. Notice that the larvae of sea squirts are motile but the adults are sessile.

Cephalochordates - amphioxus

Craniates

Characters uniting the Chordata (urochordates + cephalochordates + craniates) - these are the characters that everyone in comparative vertebrate anatomy has to memorize!

1. branchial (or pharyngeal) pouches - outpocketings of the pharynx
2. endostyle - an organ in the floor of the pharynx that secretes mucus
3. notochord (hence name "chordata") - a skeletal rod that is stiff in compression but can bend. This keeps the body from "telescoping" when muscles on one side contract. Instead, the body bends, which allows the animal to swim.
4. postanal tail
5. dorsal, hollow nerve chord

Garstang's ascidian "tadpole" hypothesis

Picture to come

• Ur-chordate a sessile adult with free swimming larvae - similar to modern Ascidian "tadpole" larvae
• In a lineage leading to vertebrates, the larval stage is extendend and metamorphosis is finally lost.
• This pattern, where ancestral juvenile characters are retained by descendant adults, is called Paedomorphosis, a term coined by Garstang.

The ascidian "tadpole" hypothesis can be tested with a phylogeny:

This is a phylogeny based on 18S rDNA from Wada (1998), which suggests that the ancestor of euchordates (Branchiostoma + craniates) was pelagic and had a tadpole-like body morphology throughout its life history. That is, the 18S data are inconsistant with the ascidian "tadpole" hypothesis.

How did vertebrates arise from from a small, pelagic, tadpole-like animals?

What this cladogram suggests is that the lineage leading to vertebrates has been dominated by the evolution of characters that make an animal stronger, faster, and smarter.

Other things to note about this cladogram

1. hagfish have traditionally been classified as vertebrates but should properly be classified with vertebrates as craniates. That is, chordates with a head skeleton. Vertebrates include the lampreys and gnathostomes, or jawed-vertebrates (lampreys and hagfishes do not have jaws supporting the mouth).
2. Other important characters appear in nodes not illustrated in this cladogram, including bone, teeth, and pectoral fins. Please refer to Kardong and read the relevant tree of life pages (hypertext links above).

St. Hillaire vindicated: The upside down Arthropod / Annelid hypothesis revisited

Even though the immediate ancestor of vertebrates was not anything like an arthropod or annelid, St. Hillaire's original thesis,

that the embryos of arthropods and vertebrates are variations on a common plan, the major differences due to their inverted dorso-ventral axes,

is supported by a growing body of molecular developmental evidence. Here is the abstract from Holley et al. (1995). Remember Drosophila (fruit fly) is an arthropod while xenopus (a frog) is a vertebrate.

In other words, not only do the fruit fly and frog have homologous genes that promote dorsoventral pattening but the homologous genes have opposite effects within each animal and that, remarkably, the genes are functionally interchangeable. That is, even though the products of sog ventralizes fly embros it dorsalizes frog embryos, just like its homolog in the frog, chordin.

Summary Table

Again, this common (but inverted) organization of arthropods and vertebrates does not mean the immediate ancestor of vertebrates was an arthropod but that arthropods and vertebrates (and the other related phyla) share a common ancestor, the ur-bilateria, with a set of features common to all bilaterians. What is wonderful about this molecular developmental work is that biologists are finally solving many of the hard questions that reached an impasse long ago in comparative morphology.

 

Holley, S. A., Jackson, P. D., Sasal, Y., Lu, B., De Robertis, E. M., Hoffmann, F. M. and Ferguson, E. L. (1995). A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249-253.

Wada, H. (1998). Evolutionary history of free-swimming and sessile lifestyles in Urochordates as deduced from 18S rDNA molecular phylogeny. Mol. Biol. Evol. 15, 1189-1194.