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EVOLUTION OF THE EYE
Shiva Swamynathan
[email protected]
Evolution
Charles Darwin on evolution of eyes
1860- The eye to this day gives me a cold shudder, but when I think of the fine known
gradations, my reason tells me I ought to conquer the cold shudder.
1872- 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. When it was first said that the sun stood still and the
world turned round, the common sense of mankind declared the doctrine false; but the old
saying of Vox populi, vox Dei, (the voice of the people is the voice of God) as every
philosopher knows, cannot be trusted in science. 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, though
insuperable by our imagination, should not be considered as subversive of the theory.
A working definition for an eye
Eye is an organ that provides spatial vision
What is Spatial Vision?
Ability to detect an image by comparing light intensities in different directions
Eyes first appeared in early metazoans
Insects, crustaceans, annelid worms, molluscs
Chronology of animal locomotory abilities,
and visual function
Eyes and vision : Unity in diversity
An optical system that can discriminate the direction of light to within a few degrees is
present in only 6 of the 35 animal phyla. Yet, they account for 96% of all animal species
Diversity of eye types in the animal kingdom
Eyes
Simple (Non-Compound) Eyes
(Single-Chambered Eyes; One
concave photoreceptive surface)
1. Pit Eyes (Found in ~85% of phyla)
2. Spherical Lensed Eye (Gastropods and annelids)
3. Multiple Lenses in the Optical Path (Copepods)
4. Refractive Cornea (Terrestrial vertebrates and
birds)
5. Reflector Eyes (Scallops, Spookfish)
Compound Eyes
(A number of lenses above photoreceptors )
6. Apposition Eyes (Most common, seen in
arthropods, annelids & horseshoe crab)
7. Refracting Superposition (Nocturnal
insects)
8. Reflecting Superposition (Long bodied
crustaceans like shrimp)
9. Parabolic Superposition (combines
features of superposition and apposition
eyes; functions by refracting light, then
using a parabolic mirror to focus the image.
Mayflies)
Different types of eyes in multicellular organisms
Aquatic Lens Eye
Single chambered
mirror eye
Pit Eye
Corneal Lens
Apposition
Compound Eye
Compound Eye
Refracting
Superposition
Eye
Reflecting
Superposition
Eye
Eyespots in unicellular organisms:
Early predecessors of the eye
• Clusters of photoreceptor proteins. Earliest predecessors of
the eye.
• Can only sense ambient brightness, sufficient for
synchronization of circadian rhythms.
• Insufficient for vision, as they cannot distinguish shapes or
the direction of light.
• Found in nearly all animal groups, and are common among
unicellular organisms including euglena.
Euglena Eyespot
Eyespots in multicellular organisms
“Eyespots“ comprised of photoreceptor cell(s) surrounded by
pigmented cells have evolved independently about 40-65 times.
Eyespots provide a basic sense of the direction and intensity of light
Eyespots in a planarian
Eyespots in a limpet
Pinhole camera eyes
Pinhole camera eye in a Nautilus
Compound eyes in arthropods
Horseshoe Crabs: Both simple and compound eyes
Horseshoe crabs have two primary compound eyes and seven secondary
simple eyes. Two of the secondary eyes are on the underside
Median Simple Eye
Lateral
Simple Eye
Lateral
Compound Eye
The sizes of compound eyes with human like resolution
Simple corneal eyes in arachnids
Wolf spider has eight simple eyes, two main eyes at the front and six smaller secondary
eyes. The main eyes form images. The secondary eyes detect peripheral movement
Simple (single-chambered) lens eye in vertebrates
Lens eyes: Also seen in cephalopods, annelids,
jellies, copepods…
Swamynathan et al 2003. FASEB J. 17: 1996-2005
Multiple eye types in each branch of evolutionary tree
Single Chambered
Compound
Eyes
All Eyes Sense Light
Optical Quality
Landscape of eye evolution
Evolutionary Distance
“Climbing the hills is straightforward but going from one hill top to another is near impossible.”
-Mike Land
Key innovations in eye evolution
Focusing
Optics
Membrane
Stacking
Photopigment
Regeneration
Screening Pigment
First critical part of the puzzle in building an eye :
Photosensitive molecule that can be regenerated
Opsins: Key Molecules for Vision
Phylogeny of Opsins
Phylogeny of Opsins
Second part of the puzzle: Spatiotemporal
regulation of opsin gene expression
Drosophila Twin of Eyeless
misexpression in legs
Drosophila Pax6 in Xenopus
Genetic pathway that specifies eyefield is
conserved in arthropods and vertebrates
Diverse roles of Pax transcription factors during eye evolution
Evolution of eyes reflects a central idea in evolutionary
theory-the diversity and unity of life
Evolution of Pax6-related genes
Evolution of eye structures
Analogous eyes; Homologous genes
One origin or many?
• Much of the genetic machinery employed in eye development is common to all eyed
organisms, which suggest one origin from a common ancestor that utilized some form of
light-sensitive machinery – even if it lacked a dedicated optical organ. Shared traits common
to all light-sensitive organs include the opsins family of photo-receptive proteins.
• However, even photoreceptor cells may have evolved more than once from molecularly
similar chemoreceptors, and photosensitive cells probably existed long before the Cambrian
explosion. Higher-level similarities – such as the use of crystallins in the independently
derived cephalopod and vertebrate lenses – reflect the co-option of a protein from a more
fundamental role to a new function within the eye
Lens-containing eyes evolved sporadically
throughout the animal kingdom
Different proteins serve as crystallins in diverse phyla
Distribution of photoreceptor cell types and
screening pigments in different phyla
Rhabdomeric
(Microvilli-based)
Ancestral
Ciliary
Evolution of Eyes: Convergent, or Divergent?
Polyphyletic,
Convergent
• Independent evolution of similar
features in species of different lineages
• Creates analogous structures with
similar form or function, that were not
present in their last common ancestor
Monophyletic,
Divergent
• Accumulation of differences between
groups leading to new speciation.
• Similarity is due to the common origin,
such as divergence from a common
ancestral structure or function
Vertebrates, cephalopods, and cnidaria possess camera eyes, while their last common
ancestor had a simple photoreceptive spot. Progressive refinement of this structure led to
the advanced camera eye. The similarity of these structures, despite their complexity,
illustrates how some biological challenges have an optimal solution, and suggests
polyphyletic, convergent evolution of eyes. However, conservation of opsins and the
transcription factors regulating their expression suggests monophyletic evolution of eyes.
Convergent evolution of analogous structures
Different solutions for one problem suggest multiple origins
Photoreceptors
Transducing nerves
Transducing nerves
Photoreceptors
Optic nerve
Optic nerve
Vertebrate Eye
Built Upside down
Octopus Eye
Built right way out
General scheme of eye evolution
Modern eyes evolved by division of labor
• The number of cell types in an eye has gone up concomitantly
with the increasing complexity of evolving eye types
• The number of protein-coding genes representing cellular
eye-related functions has not increased at a similar pace.
Division of labor, or functional segregation of cell types resulting in
differential distribution of cellular functions between sister cell types
Pace of eye evolution
Summary
• The eye, defined as an organ of spatial vision, is present in a fraction of the animal phyla
• Most of the eyes we see today arose during Cambrian Explosion about 530 Mya
• Despite their separate evolutionary origins, even analogous eyes (like those of sharks and
squid) have basic similarities. All eyes, wherever they evolved on the tree of life, sense light
and are used by organisms to interact with their environments. Many analogous eyes share
similar cell types — and those cells contain similar light-sensing molecules
• The photopigment rhodopsin and certain genes controlling eye development appear to
have been present in a common metazoan ancestor, as they are homologous in all eyes
• Though structural evidence suggests that the eyes evolved independently many times, the
small number of photoreceptor cell types suggests that they predate the eyes themselves
• Conservation of the genetic network of transcription factors required to specify eyefield
suggests monophyletic origin of the eyes followed by a series of specializations
• It is estimated that the evolution of an advanced fish eye from a patch of photosensitive
tissue could occur in less than 400,000 generations, providing an explanation for the large
diversity of eye types in animals
• Cell-type functional segregation, the differential distribution of cellular functions between
sister cell types may have played a major role in eye evolution