10/25/2012

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Eye evolution (guest lecture )

Lars Schmitz 10/25/2012

Why don’t plants have eyes?

10/25/2012

2

Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

10/25/2012

3

… about a third have light-sensitive

cells.

… about a third have proper eyes.

… about a third have no visual

specializations whatsoever.

Of the ~30 animal phyla …

“proper” eye: an organ able to compare light

intensities in different directions [spatial vision]

Turbellarian Flatworm

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Chambered Eyes

Scallop

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Vertebrate eyes

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Amniote Eye

California Condor

cornea

lens

iris

pupil

Retina

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Chambered Eyes

everse (octopus)

vs.

inverse (cod)

Cephalopod eyes

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Compound Eyes

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schizochroal

holochroal

abathochroal

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Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

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 possible degree. (Darwin 1872)

Darwin on eye evolution

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Yet reason tells me, that if numerous gradations from a perfect and complex eye to one very imperfect and simple, each grade being useful to its possessor, can be shown to exist; if further, the eye does vary ever so slightly, and the variations be inherited, which is certainly the case; and if any variation or modification in the organ be ever useful to an 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, can hardly be considered real. (Darwin 1872, 143-144)

Darwin on eye evolution (next paragraph)

Time required to evolve an eye

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Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

Refractive

System

Receptors Neural Processing

(Retina + Brain)

Behavioral

Anatomical

Optical

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Visual

Capacity Resolution

Field of View

Sensitivity

Light PND

S

Quantifiable as

Spatial Sampling Frequency (SF)

PND: Posterior nodal

distance

S: Separation of

receptor centers

(min. ~2 µm)

SF = ____ PND

2·s

Land (1981)

Resolution

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Land and

Nilsson 2002 Spatial Sampling Frequency

Octopus

Aeschna

Nautilus

Aquila audax

Falco berigora

resolving power

behavioral: 132-143 c/deg

anatomical: 140 c/deg

resolving power

behavioral: 69-76 c/deg

anatomical: 76 c/deg

Reymond 1985,1987

(Wedge-tailed Eagle)

(Brown Falcon)

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Accommodation

Visual

Capacity Resolution

Field of View

Sensitivity

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Sensitivity to Point Light Sources

klr eer

EAN 1

16 2

2Sensitivity ~

monochromatic light

E: # of photons originating at source l: length of receptors

A: aperture k: peak absorption coefficient r: distance to light source α: combined attenuation coefficient

for given receptors, light distance and intensity

A2

Warrant (1999)

kl

klA

PND

d3.2

2

2

2

Sensitivity=

PND

A2

d: diameter of receptors

l: length of receptors

k: peak absorption coefficient

A: aperture

PND: posterior nodal distance

(for given receptor dimensions)

Land (1981)

Sensitivity to Extended Sources

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f-number

PND

A2

Sensitivity ~

f-number = PND

A

the lower the better

PND PND

A S

TRADE OFF

Resolution Sensitivity

SF = ____

2·s

PND F =

____ PND

A

for given eyeball size,

receptors, neural processing

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Visual

Capacity Resolution

Field of View

Sensitivity

Visual Fields

Martin et al. 2007

Apteryx sp.

(Kiwi)

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Steatornis caripensis

(Oilbird)

38°

Visual

Capacity Resolution

Field of View

Sensitivity

Contrast sensitivity

improved by 40% Visual threshold

improved by 40%

Trade Off

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Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

Bio-mechanics

Bio-optics

EVOLUTION

Physical constraints

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Light Levels Luminance [photons m-2 sr-1 s-1]

8 lo

g u

nit

s

water depth [m]

terrestrial marine 1

4 lo

g u

nit

s

Po

int

Lig

ht

So

urc

es

4

Starlight

Moonlight

Bright

Sunlight

6

10

8

12

14

16

18

20

1000

800

600

400

200

0

Epipelagic

Mesopelagic

Bathypelagic

Oil Bird

Scopelarchus guentheri

Martin et al. 2004

Warrant 2004

Retinal adaptations

Tapetum Lucidum IRS

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Tapetum Lucidum

Retinal adaptations

Apteryx mantelli

kiwifoundation.org.nz

inside

outside

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Retina

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Muraenidae

perco-

morphs

holo-

centrids elopo-

morphs

Holocentridae

perco-

morphs

holo-

centrids elopo-

morphs

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Apogonidae

perco-

morphs

holo-

centrids elopo-

morphs

Priacanthidae

perco-

morphs

holo-

centrids elopo-

morphs

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Sciaenidae

perco-

morphs

holo-

centrids elopo-

morphs

Pempheridae

perco-

morphs

holo-

centrids elopo-

morphs

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Haemulidae perco-

morphs

holo-

centrids elopo-

morphs

diurnal nocturnal

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Schmitz and Wainwright 2011 (BMC Evol. Biol.)

A

D x f

2

small large

A: Aperture

D: retinal area

f: focal length

aquatic

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Schmitz and Wainwright, 2011 (BMC Evol. Biol.)

Eye morphospace of reef fish

round, large

pupil;

large lens

large, elliptical

pupil;

small lens

small, elliptical

pupil

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Light sensitivity

large, elliptical

pupil;

small lens

round, large

pupil;

large lens

small, elliptical

pupil

Diurnal

IRS

IRS

IRS

Collared Lizard

Chipmunk

King Parrot

Flame Robin

Eastern Robin

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Leopard Gecko

Nocturnal

Crested Owl

ADW

IRS

Oilbird stanford.edu/~cagan/southamerica.htm

Brown Rat ADW

Cathemeral Crepuscular

Asian Elephant

BNAO

Common Nighthawk

BNAO

Giraffe giraffe.org

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A

D x f

2

small large

A: Aperture

D: retinal area

f: focal length

terrestrial

Eye morphospace

Discriminant Axis 1

Dis

cri

min

an

t Axis

2

95% confidence ellipses

mammals, n=35

birds, n=15

squamates, n=8

Variables: eyeball diameter,

axial length,

lens diameter

Schmitz and Motani 2010, Vision Res.

misclassified

proportion (pFDA):

13.4%

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Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

Weishampel et al. 2004

-mixed time periods-

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Weishampel et al. 2004

-mixed time periods-

Scleral Rings

Bubo

Osteology

and optics?

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Mammal Bird

Scleral ring

Scaphognathus

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Lens diameter

External scleral ring

Internal scleral ring

Axial length

Eyeball diameter Orbit length

Hard-tissue Soft-tissue

Orbit length External + internal

scleral ring

diameter

Schmitz 2009 (J. Morphol.)

diurnal

nocturnal

Schmitz and Motani 2011 (Science)

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Dinosauria

Archosauria

33 Mesozoic archosaur species

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Weishampel et al. 2004

-mixed time periods-

cathemeral/

crepuscular

equivocal (either

nocturnal or cathemeral/

crepuscular)

diurnal

nocturnal

8

14

9

2

Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

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Point light sources

Extended luminous sources (form illumination)

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Extended non-luminous sources

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Questions…

• How many times did eyes evolve?

• How long did it take to evolve an

eye?

• What makes a good eye?

• How does ecology influence the

evolution of eyes?

• Were some dinosaurs nocturnal?

• Why do giant squid and ichthyosaurs

have giant eyes?

• What fish have reduced eyes?

10/25/2012

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Scytalina

Forbesichthys

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Ditropichthys

Melanocetus

Oneirodes

Bufoceratias