Evolution of Development

Fundamental problems of Development:

1. explaining the origin of a finite number of Baupläne with no real new ones since the Precambrian (see Origin of Life and Cambrian Explosion Lecture)
2. How to get large changes in shape in relatively short periods of evolutionary time (Macroevolution is the answer isn't it)
3. Accounting for the origin of complex structures and functions in terms of evolutionary fitness (Of course!)

Key concepts:

Constraint (Yin) -- viewed as internal selective environment. Evolutionary biologists have held these notions for a long time but consider them -ve genetic correlations.

Degerancy (Yang) -- "developmental paths can nevertheless be highly degenerate -- often the same kind structure can be produced from a variety of different epigenetic sequences" (gastrulation in verts). Degeneracy relaxes the stringency of developmental constraints and, together with the regulative aspects of development, provides the necessary "leeway" for evolutionary changes that would otherwise lead to blind ends or lethality. We did not discuss this in lecture, but there are indeed many ways to skin and evo-devo cat.

Atavisms -- "the recurrance of ancient structures, not normally seen in a group which harken to a "throw-back of bygone days" -- these are readily explained in terms of development and evolution and I will treat this in great detail.

History of the field

Coming to the realization that there is history embedded in the development of an embryo was a profound achievement in biology.

This revelation is on par with that experienced with the advent of modern molecular biology. There is history embedded in DNA and protein structure.

A brief, and truncated historical account concerning the 1800's debate over the priniciples governing the evolution of morphology.

Haeckel (c. 1870):

Ontogeny recapitulates phylogeny -- evolutionary change occurs by the successive addition of stages to the end of unaltered ancestral ontogeny.

"Both ontogeny and phylogeny deal with the knowledge of a sequence of changes that the organism <e.g., species or type> passes through during its developmental motions."

"Phylogeny and ontogeny are, therefore, the coordinated branches of morphology. Phylogeny is the developmental hisotry of the abstract, genealogical individual; ontogeny, on the other hand is the developmental history of the concrete, morphological individual."

Graded series of types arises by terminal addition of structures in ontogeny, and Vertebrate embryongenesis is the classic example.

von Baer (c. 1840)

His objections to recapitulation (from Gould, p. 53-54):

1. Many features of embryos are not present in adult animals (gills).
2. The mode of life of an embryo often precludes any complete repetition of lower forms (mammalian embryos in the placenta are not birds or fish) ** -- there is perhaps selection during embryogenesis not just on the terminal features of adult life (implicit statement which we will return to).
3. There is never a complete correspondence between an embryo of a "higher type" and any lower adult (e.g, chick vs fish)
4. recapitulation is often reversed transitory structures in othogeny of lower forms aften appear in adult stages of higher forms.

The final point is well illustrated by the theory of Neotenic origins of insects:

Hexapod (six-legged) Insects are thought to have evolved from a millepede ancestor, and the millipede ancestor passes through an insect like stage during embryogenesis. Thus it is thought that insects evolved from a precociously maturing millepede "embryo", classic neoteny.

Back to von Baer -- Summary:

"The embryonic vertebrate, at every stage, is an undeveloped and imperfect vertebrate, it can represent no adult animal whatever."

"Embryology is differentiation, not a climb up the ladder of perfection."

"Development proceeds from the general features, to the specific."

von Baer's Laws

1. The general features of a large group of animals appear earlier in the embryo than the special features.
2. Less general characters are developed from the most general.. until finally the most specialized appear (limb buds).
3. Each embryo of a given species, instead of passing through the stages of other animals, departs more and more from them.
4. Fundamentally, therefore, the embryo of a higher animal is never like [the adult of] a lower animal, but only like its embryo.

von Baer meets bithorax and modern molecular biology:

The evolution of arthropods

The development of Arthropods is governed by several large complexes of genes that are linearly arranged in the genome.

For example, in the fruit fly,

1. The antennapedia complex controls major segments in the head (cephalic tagmata) and
2. The bithorax complex controls major segments in the thorax (e.g., wing and leg development)
3. as well as it appears to suppress development of leg-like structures in the abdomen (intra-abdominal a, b).

If you knock out genes that suppress leg formation in the abdomen (e.g., the primitive state) you can recoup leg like structures in the abdomen. E.g., reverting to the millepede like ancestral condition.

Thus many genes have been added much in the way layers of an onion cover the embryonic onion plant. The function of such genes is to suppress the formation of "atavistic features". Occaisional such atavisms pop up in normal development and in some cases are due to a natural mutation.

One can imagine the evolution of arthropods to occur as follows (also see Origin of Life and Cambrian Explosion Lecture):

1. One small block of genes began evolving by encorporating the control of more posterior segments to the mouth to more efficiently process food at the mouth. This leads to greater cephalization. This gene complex gets larger and larger as more genes evolve to regulate the development of more and more trunk segments to be encorporated in the head.
2. Perhaps, this block of genes is tandemly duplicated, and the subsequent 2nd block acquires a new function, control of thoracic and abdomenal regions of the body. Genes evolve to suppress atavistic traits, and form new and novel leg/appendage structures. Alternatively, this block of head genes evolves to be so large that higher control genes evolve to more efficiently control the development of such structures. Whatever the case, these gene complexes tend to modify the existing atavistic structures into new kinds of appendages.
3. In this way Tagmata of the body evolve and become distinct and the control over tagamata becomes distinct.

Let us look at an up-close example of such a process, The haltere of the fly

Dipterans are quite unique in insects in that they possess a single pair of wings. The ancestral condition is the possession of two pairs of wings.

However, insects do have a club-shaped object, the haltere, in the same position the second pair of wings on a more ancestral-style insect. A simple genetic mutation in the bithorax gene complex (the bithorax gene per se) transform the flies haltere into an beautifully formed, if not just a little atavistic, 2nd pair of wings.

Thus, the evolution of dipterans, involved the evolution of a key innovation from an existing supernumary wing. The haltere is the mechanical equivalent of a gyroscope and this structure is responsible for why flies fly so well. The mutated wing in the ancestral fly may have been intially club-shaped and somewhat useless, however, it may have been readily refined by natural selection for a new function, a gyroscope in flight.

The neotenic theories concerning the origin of insects, and the evolution of flight within the insects illustrate how the evolution of major changes in evolution, Macroevolutionary style change, may arise from readily understandable mechanisms of development.

How about another example of neotony:

Thyroxine and the control of amphibian metamorphosis

Neotony is a specific form of the pattern of Heterochrony.

In neotony the timing of adult maturation is "precociously" found in a more larval stage.

In Heterochrony: Changes in the relative time of appearance and the rate of development of characters can occur at many points of the life history. I won't give you any other examples, but suffice it to say that development of structures can be slowed down or speeded up in juveniles and adults (see lectures on life history from the first part of the semester).

Hormonal feedback (negative and positive) occurs between prolactin (control of larval growth) and thyroxine (the trigger of metamorphosis).

Some salamandes remain in the larval form and this is due to an inactivation of the thyroxine cascade. Different species of salamaders have thyroxine mediated metamorphosis interrupted at various points in the cascade.

Again, the evolution of neoteny, a remarkable life history shift from breeding as a terrestrial adult that returns to water, to breeding in the water and foregoing the terrestrial stage, is due to a simple genetic lesion in many amphibian neotenic transitions (not just axolotls).

Atavisms and the Evolution of the Vertebrate Limb

Now how about turkeys, wishbones, and legbones.

Let's talk turkey concerning the origin of birds.

1. A reptile has a good tibia and fibula, and lots of tarsals
2. Archaeopteryx has a good tibia and fibula, and lots of tarsals
3. Modern birds (e.g., turkeys) have a rudimentary fibula, and fused tarsals.
4. One can, however take a developing chick and insert a piece of mica between the developing tibia and fibula. Such chicks develop a fully formed fibula, and separate tarsals!

Presumably the modern bird tibia puts out a substance that suppresses the formation of the fibula, which has cascading effects on the formation and fusion of tarsals. Separating those two tissue fields with mica causes the fibula to act as a "free-agent" which elongates and it can then induce tarsals without the hinderance or suppression by the tibia.

How about Hen's teeth

1. Modern birds have no teeth, Archaeopteryx did.
2. To get teeth you need to mix epithelium in the mouth with jaw mesoderm. The epithelium tells the mesoderm to make teeth.
3. Experiments by Kollar and Fisher indicate that chick epithelium is capable of inducing mesoderm to form teeth, but you have to supply it with mammal mesoderm. Persumably birds mesoderm has lost the capacity to "listen to the signal" that the epithelium is singing. The epithelium still sings a good song, which suggests that it must have a function in other places in development to be maintained for 60+ million years!

I also talked about the evolution of the wishbone and the ancestor to birds,

Birds evolved from dinosaurs but from which group?

No dinosuars have a good wishbone, and the wishbone is essential for bird flight.

More ancient reptiles (pre-dinosaur) have a good wishbone, thus wishbonedness is an ancestral conditon.

Deinonychus -- had a solid coracoid (shoulder) and perhaps the wishbone arose as an atavism in the descendants of this group (more ancient reptiles have a good wishbone). The wishbone is closely apposed to the coracoid and may be responsible for the induction of the wishbone.

Finally, I talked about the origin of Tetrapods

From fins to hand

The digital arch represents a very simple development program that can easily be modified to produce really cool and elaborate structures like: fins, wings, paddles, hooves, feet and hands.

Two developmental rules for chondragenic condensations that are the developmental precursors to cartilige and bone:

1. spawn of a new element at the terminus
2. or bifurcate to form two new elements

This simple set of rules can yield a phenomenal array of vertebrate limbs.