The Origins and Diversity of Bilateria

Bilateria (also referred to as "Bilateralia" in older literature): Monophyletic group containing most animals. In simple terms, bilaterians are animals with a distinct front, back, top, and bottom.

Fundamental synapomorphies:

Bilaterian Development:

Cleavage from A. S. Romer. 1977. The Vertebrate Body.
Consider the basic steps by which we get a proper embryo with a top, bottom, front, and back from a zygote:

Polarity: In all ova yolky matrial tends to concentrate at one end, yeilding:

The amount of yolk greatly influences developmental dynamics. For now, we consider an ovum with relatively little yolk.

Cleavage Phase of rapid cell division with little overall growth. The zygote transforms into a hollow sphere of cells, the blastula. The space in the middle is the blastocoel

The blastula has three cell types:

Gastrulation from A. S. Romer. 1977. The Vertebrate Body.

The embryo is now a gastrula. It possesses three basic germ layers: Note: This should look slightly familiar, as it is basically a cnidarian planula larva with mesoderm added.

Eucoelomate coelom schematic from A Review of the Universe
The Coelom: A characteristic feature of bilaterians is the presence of a coelom or body cavity. This feature allows for: Developed as:

Eucoelomate coelom schematic from Fueleducation
The evolution of the coelom opened many vistas for animal evolution, including significantly expanded locomotor strategies. Cnidarians show the limits of what a hydrostatic skeleton can do for an animal with a single module. Bilaterians, however, display body segmentation in which separate modules of the hydrostatic skeleton can lengthen and shorten, facilitating much more complex movement. This makes possible activities like: Indeed, non-bilaterians are deemed incapable of burrowing.

Specialized organs: These capabilities came at a price. Animals with only endoderm and ectoderm don't need to worry about gas exchange and elimination of nitrogenous waste, because no living cell is so far from the body surface that simple diffusion can't do the trick. Bilaterians, in contrast, usually require specialized organs for functions like:

Fortunately, the presence of mesoderm and a coelom seems to bestow the developmental plasticity needed to allow these to evolve. Indeed, the gut tube, kidneys, and gonads are ancestrally suspended inside the coelom.

Bilaterian Phylogeny:

First, fully appreciating the significance of segmentation as a synapomorphy of Bilateria, and the deep relationship shared by bilaterians requires an excursion into the realm of genomics:

Protein synthesis from Wikipedia
Regulatory genes: The structure of DNA was discovered in 1953, and its role as the physical repository of genes illuminated in the following decades. A brief review of how information encoded as nucleic acid is expressed as proteins goes like this:

Link to simple animation or to a more detailed explication.

The magic of the arrangement is that DNA is only transcribed into mRNA when the protein it codes for is needed. E.G.: The bacterium Escherichia coli freely metabolizes glucose, but if glucose is lacking, and lactose is present, it can metabolize it by producing an enzyme, beta-galactosidase, that breaks lactose down in to glucose and galactose. But how does it know when to make beta-galactosidase?

The work of François Jacob and Jacques Monod established the answer (Nobel Prize in 1965): Adjacent to the gene for beta-galactosidase (and other proteins involved in lactose metabolism) is a small controlling region gene to which a protein, the lac repressor binds like a padlock. This blocks RNA polymerase from unzipping the DNA and making mRNA. But, lactose, itself, binds to the lac repressor causing it to fall off of the DNA strand and allowing RNA polymerase to do its thing. Once the lactose has been metabolized, the lac repressor reattaches and transcription ceases. Animation.

Of course, the lac repressor protein is coded for, in turn, by a repressor gene whose activity may be regulated by other repressors. Indeed, the expression of genes as proteins is the result of complex cascading interactions of regulatory and structural genes and their protein products. Why are we even discussing this?

Hox gene clusters from The Biology Corner
Hox genes: During the late 20th century it became known that segmentation in bilaterian bodies is governed by a special class of regulatory genes. The story:

Fruit flies are a favorite model for geneticists, with short generation spans and interesting mutations that often effect entire sections of the body (modifying or eliminating body segments and/or the appendages that grow from them). Investigation into these segmentation-altering mutations revealed that they can be caused by mutations to eight genes. What makes this interesting:

The homeobox codes for a protein called the homeodomain that is functionally similar to regulatory proteins that block or allow transcription of other genes. It appears that the cluster of eight genes controls the identity of body segments in fruit flies. These are called Hox genes, after the homeoboxes they contain. The homeodomain protein regulates transcription of the Hox gene, whose protein products, themselves, promote or inhibit the synthesis of other regulatory proteins that govern body segmentation.

But it gets better: The search for homologs to fruit fly Hox genes found them in almost every animal surveyed. Mammals, for example, have four clusters of Hox gene homologs, in each of which the genes occur in the same order on the chromosome as the regions for which they code.

This is huge.

The fruit flies and mammals belong to the two major clades of bilaterians, and their last common ancestor lived during (or before) the Ediacaran, and yet they share important regions of the genome.

Protostomous and deuterostomous development from Nature Volume 409 Number 6816

The Bilaterian cladogram:

Working out the bilaterian pattern in detail is a difficult problem that is slowly being illuminated by molecular methods. In its broad strokes, however, there is a clear pattern of two large strongly supported clades:

Within Protostomia are two well-supported clades:

Within Deuterostomia are also two well-supported clades:

As promised: Bilaterian Origins:


Kimberella quadrata from Wikipedia
What we do definitely know:

The identity of these and later traces remains unknown, and yet, if we have Ediacaran worm-traces and a stem mollusk, early bilaterians must be out there. Why are we missing them?

Acoelomorph from NeoFronteras6
Too small to identify: The notion that bilaterians evolved through paedomorphosis from an ancestor resembling a cnidarian planula larva has had support since the early 20th century. Indeed, acoelomorph flatworms resemble what one might expect of such a creature.

Note: "flatworms" making up the traditional phylum Platyhelminthes are Polyphyletic. The "platyhelminthine" subgroup Acoelomorpha, however, appears monophyletic and may have a basal position on the bilaterian tree (Ruiz-Trillo and Paps, 2016.) Acoelomorphs are tiny (2-4 mm.) and display features that seem transitional between non-bilaterian and bilaterian grades, and have been suggested as models for the ancestral bilaterian (Hejnol and Martindale, 2007). They possess:

They lack If bilaterians are derived from such creatures, it is not surprising that their early members don't appear as fossils. On the other hand, other "flat worms" including platyhelminths have definitely secondarily lost their coeloms and anuses. Could Acoelomorpha be similarly degenerate?

Note: Today one frequently hears of the identification of genes associated with the formation of eyes (PAX6), central nervous systems, etc. being widespread among Bilateria, the implication being that the last common ancestor of Bilateria must possess the features involved. Careful! The genes may be homologous, but we can't know how they were expressed in the context of a simpler organism. Holland, 2003, for example, found that genes associated with the central nervous systems of protostomes and deuterostomes that had them were expressed in a decentralized epidermal nerve network of a hemichordate - an animal lacking a brain.

Vernanimalcula guizhouena - Bilaterian or acritarch?
from Wikipedia
Possible body fossils: Currently, the Doushantuo (630 - 550 Ma) is known to contain acritarchs, algae, and sponges; but bilaterian fossils of similar quality increasingly appear absent, prompting some workers to propose that the top of the Doushantuo marks the maximum possible age of bilaterian diversification.

Sea pen Ptilosarcus gurneyi
Looking in the wrong place?

Is it possible that we are seeing bilaterian ancestors and not recognizing them? Dewell 2000 suggests that bilaterians derive from modular colonial forms. In living cnidarians, such as sea pens (right) we often see modular colonies of zooids assume coherent and predictable shapes. In siphonophores, we even see zooids achieve sophisticated division of labor. Dewell asks if the bilaterian body could represent a particularly well-integrated colonial form. It would resolve the enigma of the absent bilaterians by suggesting that the ancestors of proper bilaterians might lie among the diversity of known modular Ediacaran weirdos.

One complication:

Remember Hox genes? According to Ryan 2007, three hox gene homologues are present in the solitary anthozoan Nematostella vectensis and are involved in the patterning of its oral-aboral axis - I.e., the oral-aboral axis of an individual cnidarian polyp is homologous to the antero-posterior axis of the bilaterians. Not what Dewel's hypothesis would lead us to expect.

This issue awaits the discovery of key fossils. Stay tuned.

Additional reading:

To Next Lecture.
To Previous Lecture.
To Syllabus.