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Table 2 Examples of some of the direct and indirect evolutionary processes that may be involved in the evolution of eyes

From: The Evolution of Complex Organs

Process

Examples from eye evolution

Direct adaptive evolution

Gradual evolution of lens crystallin concentrations resulting in evolution of graded refractive index lenses in aquatic animals

Exaptation

  One structure has one function and takes on or switches to a new function in a new environment

The cornea, which has no refractive capacity in water, became the primary focusing structure after tetrapods moved onto land

The lens became far less important in image formation in terrestrial vertebrates and became specialized for accommodation instead

  One structure has one function but becomes modified enough to allow a shift in function

Circadian organ in early chordates became modified sufficiently that it became capable of visual functions

An early protective, transparent layer of cells became sufficiently thickened and invaginated that it could begin serving as an early lens

  Two structures perform the same function but become differently specialized

Though both cell types were probably found in the distant bilaterian ancestor, ciliary photoreceptors became the dominant type in vertebrates whereas rhabdomeric photoreceptors came to predominate in most other animals (see also duplication and divergence)

  A vestigial structure takes on new function

In vertebrates, rhabdomeric photoreceptors lost their microvilli and became retinal ganglion cells that function in circadian entrainment rather than in vision

Duplication and maintenance of repetition

The compound eyes of arthropods are composed hundreds or thousands of repeated lens eyes called ommatidia

Duplication and divergence

Opsin genes duplicated and diverged to become r-opsins and c-opsins, along with specialization of rhabdomeric cells with r-opsins and ciliary cells with c-opsins

In certain taxa, duplications and diversification of opsins to respond to different wavelengths of light allowed the evolution of color vision

The rod cells of vertebrates are derived from cone cells, both of which are derived from a single ancestral ciliary photoreceptor

Gene sharing

Some lens crystallin proteins function both in the eye in light refraction and elsewhere in the body for other functions (e.g., cellular stress response)

Collage

The first photopigment was formed by the combination of a preexisting light sensitive molecule derived from vitamin A (which became retinal) with a preexisting G protein-coupled receptor protein (which became the ancestral opsin)

The first “eye” arose by the combination of a photoreceptor cell with a pigment cell

During the evolution of complex camera-type eyes, various types of tissue that already existed (e.g., blood vessels, nerves, muscles) were incorporated

Scaffolding

May apply to the evolution of phototransduction pathways or other relevant biochemical systems, but more data are required

Constraints, trade-offs, and historical contingency

Trade-off between resolution versus brightness in pinhole camera eyes

Trade-off between visual acuity versus size of compound eyes

Inverted retina in vertebrates

A narrow range of available wavelengths of sunlight is perceived in most animals, probably because eyes first evolved in water which filters most wavelengths

Convergence

Lenses, irises, and various other components of camera-type eyes emerged independently in vertebrates and cephalopods

Parallel evolution

The same developmental or other genes may have been independently co-opted in different lineages (though homology is also a possibility)