Lecture #27

Eye evolution5/7/13

With acknowledgements to Dr Richard Payne

The end is in sight

• Wiki’s due Thursday at midnight• Final exam on Thurs 5/16 1:30-3:30 pm

3 questions - pick 3 of 5 10 Q are posted on web1 question - pick one of 4 student QYour question is due tonight and study Q will be posted by tomorrow1 question - last two lectures (today and Thurs)

Charles Darwin 1809-1882• 5th youngest of 6 children

Father Robert Waring Darwin was a physicianMother, Susannah Wedgewood, died when Charles was 8

• Father sent him to Edinburgh to study medicineCouldn’t bear sight of blood - gave up on medicineDeveloped naturalist interests

• Enrolled in Christ’s College, Cambridge to study biology, geology

Voyage of HMS Beagle: Dec 1831 - Oct 1836

• Professor Henslow got him position as naturalist and companion to captainFather objected but uncle interceded

• Collected many specimens• Interpreted what he saw in

terms of Charles Lyell Small gradual changes over long times could make immense changes

Beagle voyage around the world

Down house

Darwin’s sand walk

The Origin of Species by Charles Darwin

Darwin wrote a treatise to explain his theory of natural selection and how that could lead to new species.

Mystery of mysteries - where do new species come from?

Cichlid fishes ofLake Malawi

Selective breeding causes change

Pigeon breeders increase diversity over just few generations

Natural variation exists in all organisms

Variation in shell morphology

Competition occurs between individuals

Geometric increase in individuals+ limited resources = conflict

Natural selection results from variation and competition in nature

Selection leads to evolution of different way to feed to fill different niches

Mechanisms of evolution

• Natural selectionChanges that result because of increased fitness, survivability

• Sexual selectionChanges that result because of increased mating success

• Genetic driftRandom effects because genes sampled at random from small population

Difficulties of the Theory

Tried to address arguments against his theory

Acknowledge them

Come up with counter arguments

Darwin’s theory of natural selection

• Why is the eye a problem?• What is Darwin’s solution?• What is his evidence?

“Organs of extreme perfection” – the problem

“To suppose that the eye with all its inimitable contrivances - for adjusting the focus to different distances,- for admitting different amounts of light, and- for the correction of spherical and chromatic aberration,

could have been formed by natural selection, seems, I freely confess, absurd in the highest degree”

• Reason tells me, that - if numerous gradations from a simple and imperfect eye to one complex and perfect can be shown to exist, each grade being useful to its possessor, as is certainly the case; - if further, the eye ever varies and the variations be inherited, as is likewise certainly the case; and - if such variations should be useful to any animal under changing conditions of life,

then the difficulty of believing that a perfect and complex eye could be formed by natural selection … should not be considered as subversive of the theory.

The solution

In searching for the gradations through which an organ in any species has been perfected, we ought to look exclusively to its lineal progenitors;

but this is scarcely ever possible, and we are forced to look to other species and genera of the same group, that is to the collateral descendants from the same parent-form, in order to see what gradations are possible, and for the chance of some gradations having been transmitted in an unaltered or little altered condition.

But the state of the same organ in distinct classes may incidentally throw light on the steps by which it has been perfected.

How to gather evidence

To understand how something evolves, would like to follow ancestral path

• ..aggregates of pigment-cells, apparently serving as organs of vision, without any nerves..Eyes of the above simple nature are not capable of distinct vision, and serve only to distinguish light from darkness.

• The simplest organ which can be called an eye consists of an optic nerve, surrounded by pigment-cells and covered by translucent skin.

• In starfishes, small depressions in the layer of pigment which surround the nerve are filled with transparent gelatinous matter..to concentrate luminous rays

• With insects it is now known that numerous facets on the cornea of their great compound eyes form true lenses

Some of data

When we reflect on these facts, here given much too briefly, with respect to the wide, diversified, and graduated range of structure in the eyes of the lower animals; and

when we bear in mind how small the number of all living forms must be in comparison with those which have become extinct,

the difficulty ceases to be very great in believing that natural selection may have converted the simple apparatus of an optic nerve, coated with pigment and invested by transparent membrane, into an optical instrument as perfect as is possessed by any member of the Articulate class.

Conclusion

• He who will go thus far, ought not to hesitate to go one step further, if he finds on finishing this volume that large bodies of facts, otherwise inexplicable, can be explained by the theory of modification through natural selection; he ought to admit that a structure even as perfect as an eagle's eye might thus be formed, although in this case he does not know the transitional states.

What are some key questions regarding eye evolution?

• What order to parts evolve?• Which kinds of eyes evolved first• How did parts start and then change with time• Molecular basis of these changes causative mutations• Number and complexity of layers• What was environment? Water or land?• How many times did it happen? More than once?• How long it took between changes• How many steps does it take to make part more efficient• Were parts ever lost• When color vision• Predicting future eye evolution• Trial and error of gains and losses

Questions in eye evolution

• What was the proto-eye?• How many times have eyes evolved?• How did sub-components evolve?

PhotoreceptorsNeural cellsLenses

• What is the evolutionary history of the vertebrate eye?

Diversity of eyes

• 33 animal phyla1/3 have no specialized light detector1/3 have light sensitive organs1/3 have eyes

6 phyla have image forming eyes

Cnidaria - coral, sea anemone, jelly fish

Mollusca - snails, muscles, squid

Annelida - worms, leeches

Onychophora - velvet wormsArthropoda

Chordates

Figure 32.11

ANCESTRALCOLONIALFLAGELLATE

Deuterostomia Lophotrochozoa

Bilateria

Eumetazoa

Metazoa

Ecdysozoa

Porifera

Ctenophora

Cnidaria

Acoela

Echinodermata

Chordata

Platyhelminthes

Rotifera

Ectoprocta

Brachiopoda

Mollusca

Annelida

Nematoda

Arthropoda

Evolution of eyes

Progression of eye forms in molluscs

Fig 4.1

Most sophisticated mollusc eye

Visual system constraints• Energy to make and operate an eye• Make space for eye• Neural system to interpret• Sensitive conditions of night and day• Environmental – amt light, wavelengths• Life history traits – visual tasks• Pressure / temperature• Shape / ability to focus• Form transparent cells• Maintain eye (eyelids / tears)

What unique parts are needed to make an eye?

• Photoreceptor cells• Optic nerves – get message to brain• “retina” = neural processing• Pupil – control light levels• Lens• Cornea• Vasculature to support it

Gradual eye evolution

How easy is it to make an eye?

• How long does it take to evolve an eye?

• Start with light sensitive patch on the skin - photoreception already exists

• Assume can change 1% in some dimension each generationSmall change

1% changes make rapid improvements in eye resolution over short time

Eye resolution increases linearly along this path

How easy is it to make an eye?

Takes 1829 steps: if a step is only 1 yr = 1829 years

However, 1% change / year is actually pretty big

If only 0.005% per step then it would take <400,000 generations

Fig 1.6

Protective layer

Receptors

Pigment cells

Are there any flaws to this argument?

• Selection acts on lots of things• Selection may not be constant (stagnant)• May be some trade offs• Are you really stuck on these peaks• Deux ex machina - photoreceptors and lens

appear

How many times have eyes evolved?

• What kind of data can we use to decide this?Rods and cones evolved at diff timesConservation of genesOrganization of retinaLoss of eyes – mechanisms shared?Compare

Have eyes evolved once or many times?

• Ciliary and microvillar photoreceptorsSalmander

Human

Drosophila

Have eyes evolved once or many times?

• Source of eye tissue during development Epidermal epitheliumvsNeural epithelium (brain)

Have eyes evolved once or many times?

• Photoreceptor orientation

Have eyes evolved once or many times? Phototransduction

OpsinFamily members

(+)GC (+)cGMP (+)cng (K+)

(+)PDE (-)cGMP (-)cng (cations)

ciliary

microvillar

DAG/PIP2 (+)trp (Ca2+, cations)

InsP3/Ca2+ (+) ?? (Na+, cations)

GT

(-)PDE (+)cGMP (+)cng (cations)

G0

G0

Gq

PLC

hyperpolarizedepolarize

Other variations of the phototransduction cascade exist

Dr. Payne

How many times have eyes evolved?Lens crystallins

Different organisms use different proteins to make the transparent lens crystallin proteins

How many times have eyes evolved?

Fig 1.9

a pitb compoundc lensd corneae appositionf superpositiong single chamber mirrorh compound mirror

The 6 phyla contribute 96% of known species and use 8 different eye designs

Fernald 2006

Are microvillar photoreceptors confined to compound eyes?

No…, squid and spider eyes use them

What is the relationship between these photoreceptor types and Eye designs or phyla?

Dr. Payne

Are microvillar photoreceptors confined to invertebrates?

Well, they are present in chordates

And a class of retinal ganglion cells in our eyes may respond directly to light via an invertebrate-like rhodopsin and the IP3 pathway.

Are ciliate photoreceptors confined to vertebrates?

No – simple scallop eyes contain ciliate photoreceptors(which hyperpolarize due to activation of K+ channels!)

And, in the same eyes, microvillar photoreceptors existwhich depolarize due to activationNa+ channels

How many times have eyes evolved?

Fig 1.7

This tree suggests eyes may have evolved many (40-50?) times

In spite of different origins

• Many molecules are in common across all animal phyla which contain eyesOpsinsPax6

Mammals and worms both use ciliary and rhabdomeric opsins

Mammals Ciliary - photoreceptors Rhabdomeric - retinal ganglion cells

Annelids Rhabdomeric - photoreceptors Ciliary - brain

Lamb et al 2007

Opsins common to all photoreceptors

Where did the photoreceptive molecule come from?

• Rhodopsins occur in single celled organismsBacteriorhodopsin in Archea (Halobacteria)Uses photons to pump H+ outside cellH+ gradient used to generate ATP

Mouse, Drosophila and Xenopus have interchangeable Pax6 gene

Gehring thinks Pax6 evolved once which

led to an eye which then

diversified into multiple types

Does this mean there is a single origin of the eye?

• What do you think?

• Convergence vs single unique origin?

Intelligent design

Michael Behe

Irreducible complexity

Accepts age of the earthAccepts common descent

Does not believe natural selection explains molecular life.

Darwin’s Black Box pg 15

• “Biochemistry has pushed Darwin’s theory to the limit. It has done so by opening the ultimate black box, the cell, thereby making possible our understanding of how life works. It is the astonishing complexity of subcellular organic structures that has forced the question, How could all this have evolved?”

Irreducible complexity

• Darwin : “If it could be demonstrated that any complex organ existed which could not possibly have been formed by numerous, successive, slight modifications, my theory would absolutely break down”

Behe

• Current organs are irreducibly complex - if remove any of the parts, the rest would not function

• It is not possible to produce an irreducibly complex system by small modifications

• Eye is an irreducibly complex organCan’t see with half of an eye

Michael Behe - intermediate structures must be functional

Are you convinced?

Intelligent design vs evolution disclaimer

• ID claims there is an intelligent designer that created the universe

• It is not possible to prove or disprove this claim

• This is a philosophical discussion that is beyond the purview of our scientific method

• Important to be aware that this debate continues