Evolution I:

The origins of vision

Paul McGraw
paul.mcgraw@nottingham.ac.uk
Room C50

PSGY3021 - Lecture 3
Aim: to understand how evolution has shaped visual
function

Learning objectives:

• Discover when the first primitive eyes appeared during evolution

• Understand the essential requirements for vision
• Explore the link between the evolution of vision and the evolution of
visually-guided behaviour

• Look at the diversity of eye design

 Evolution
“Nothing in biology makes sense except in the light of evolution” -
Theodosius Dobzhansky
Evolution: The change in genetic composition (and inherited characteristics) of a
population over successive generations which may be mediated by mechanisms
such as natural selection, inbreeding, hybridization or mutation.

Natural selection - changes in genetic composition that

enhance reproduction are retained in successive generations,
i.e. traits that offer a competitive advantage are passed on. Can
act at the level of genes, cells, individuals, groups of organisms
and species.
Hybridization or gene flow

Mutation bias

Genetic drift

Genetic hitchhiking

Recombination
 The evolution of vision - when did we see the light?
Timescale of
evolution

• No evidence of eyes in the fossil remains of pre-cambrian organisms

• Oldest eyes date back to Cambrian period (530-540 million years ago)
• Abrupt appearance of a wide range of organisms - ‘The Cambrian Explosion’ - trilobites and arthropods
abundant
• The Cambrian Explosion resulted in an entire fauna, including virtually all animal phyla we know today
• Visually guided predation may have been a may have been trigger for ‘evolutionary big bang’
The evolution of vision - when did we see the light?
 The evolution of vision - when did we see the light?
Cambrian Fauna

Trilobite compound eyes

• Trilobites (extinct marine fauna) had early compound eyes
• Fossil evidence suggests a large variety of visually guided animals evolved in a short space of time (~5 million years)
• Parker’s ‘light-switch’ hypothesis: evolution of vision key driver for diversification - visually guided predation may have
been a trigger for ‘evolutionary big bang’
• Body size increased during Cambrian period and skeletons and rigid protection seem to have evolved at the same time
• Improved mobility and visually guided predation introduced selection pressure to develop protection (e.g. eyes, body
armour)
 How did early visual systems evolve?

In order to ‘see’ the species needs something to harvest

light energy and an effective signaling system.

1. All animal photoreceptors use opsin proteins, bound

to a light sensitive vitamin A derivative (chromophore),
to detect light energy.
2. Light sensitive opsins signal via a G-protein cascade
and this may evolved very early in animal evolution.

Animal opsins may have originated as a modification of a

chemoreceptor protein (generates a biological signal in
response to a chemical) early in animal evolution. At a
molecular level the two systems are almost identical.
 What factors shaped the evolution of vision?

• Selection acts on both the development of the sensory detector (eye) and visually guided behaviour
6

direction toward or away from the light in a mov

obvious behaviors guided by directional photorece
taxis based on scanning body movements (Jékely e
photoreceptor’s directionality in combination with
orientation will provide a direct feedback to ste
the animal can move toward the light or seek ou
A directional photoreceptor can also be used as an op
to orient the body posture in relation to the light (
Shadow detection, which was listed under class I,
Fig. 1. The causality of different levels in the evolution of sensory systems. formed by a directional photoreceptor. If the directi
Both factors are linked with respect
The genome,to whichevolution:
is the level directly subject to heritable variation, gen- sufficiently narrow, a photoreceptor can warn abou
erates the morphology and physiology, which in turn generates behavior objects, and this can lead to higher behaviors class
Causality: genes dictate the guided
morphology and physiology,
by sensory information, and this in turnwhich
generatesin theturn
fitnessgenerates
that behavior guided by visual
selection can act upon. In this view, sensory-guided behavior is entirely a con-
information, and this in turn generates the fitness
sequence of the morphology that selection
and physiology. actsthatupon.
From this, it follows genetic
Class III: Low-resolution vision
modifications are driven by modified requirements on the morphology and
Requirement: genetic modifications are indriven
physiology, which by modified
turn are driven requirements
by modified requirements on sensory-on the morphology
An array of directionaland physiology,
photoreceptors, such as tho
which in turn are driven by modified
guided behaviorrequirements on visually-
and finally by requirements for improvedguided behavior
fitness. This is and
eyes finally
(as well as inby
morerequirements
advanced eyes), will mak
different to the view of Endler (1992), who considers sensory organs and
for improved fitness. behavior to coevolve, but the sensory organs are then seen in isolation from the
readings of the luminance in different directions.
crude resolution such information can serve a l
rest of the morphology and physiology of the organism. The two views are not
• In this view, behaviour is the causal
in logical conflict,evolutionary link
but the view illustrated here between fitness
gives a more important roleand
to the morphology/physiology
important of
tasks. Monitoring of self-motion in
sensory systems (Nilsson,behaviors,
2009)as the causal evolutionary link between fitness and sensory systems stationary world is a task that is ideally performed
(which are part of the organisms’ morphology/physiology). tial frequencies, which are also the most econom
Knowledge about the flow field caused by self-mo
to control speed and direction of locomotion as w
Classifying
Therefore, to understand the evolutionphotoreceptor-controlled
of the eye we behavior
need to consider the toryevolution
in relation to surrounding structures (Theoba
of visually-
Object avoidance (anticollision) responses also bel
guided behaviour. Eyes are well
Apart frommatched to the
true vision, simpler typesvisual tasks
of light sensing arethey serve.of behaviors. Finding a suitable habitat and mainta
well known
for controlling a range of different behaviors. In a classification of
 Classifying visual behaviours
What are the functional requirements of vision?

Constrained by:

integration time
(e.g. long integration time required for monitoring daily light cycle, but short
integration is needed for avoiding motion blur)

detecting the angle of incoming light

(e.g. unshielded receptors in transparent animals are non-directional and are useful
for monitoring ambient radiance, but phototaxis responses require directionality)

detection accuracy
(e.g. poor detection threshold (~30% change) may be sufficient for detecting the
onset of dusk, but not for discriminating boundaries of an object in a visual scene
(~3% change)

The repertoire of visual behaviours an organism must accomplish place

different demands on spatial and temporal vision
 Classifying visual behaviours
Can classify visual behaviour into 4 distinct groups (see Nilsson, 2013)

Class 1 - Behaviours controlled by non-directional monitoring of ambient light

• Control of circadian rhythms

• Monitoring water depth
• Avoiding harmful levels levels of UV radiation
• Shadow detection to avoid predators
• Surface detection for burrowing
• Monitoring light levels for reproduction
Some species of coral manage to spawn during
a single hour of the year by synchronizing their
reproductive cycles with the diurnal variation in
light.

Class 1 tasks can be performed at very low light intensities (starlight) with
unaided and morphologically unspecialized photoreceptors (i.e. only opsin
and signaling system)
 Classifying visual behaviours
Class 2 - Behaviours based on directional light
sensitivity

• Phototaxis responses
• Control of body position
• predator detection

Phototaxis - movement towards or away from light Negative phototaxis response response in the nemotode -
moves away from light.

• a large field is sufficient (180 deg.).

• Spatial information is gathered by moving the field (scanning)
• This requires much faster responses from the photoreceptors
• Intensity differences from scanning are small - need better
ability to detect intensity change

Class 2 tasks require the addition of a screening pigment or photoreceptor

shielding - this makes them directionally selective. Eye spots, or ocelli, are
sufficient for class 2 tasks.
 Classifying visual behaviours
Class 3 - Visual tasks based on low spatial resolution Flatworms

• Detecting ego or self motion

• Anti-collision mechanisms
• Selecting a new habitat
• Orientation towards large landmarks or celestial
objects

Coarse spatial resolution is sufficient (5-25 deg.)

Stacking of photoreceptor membrane is required to increase photon
catch
Reduced angle of capture for each receptor

Class 3 tasks require multiple photoreceptors that monitor light changes in different
directions. Pigment cups or pits are sufficient for class 3 tasks.
 Classifying visual behaviours
Class 4 - Visual tasks based on high spatial resolution

• Detecting prey and pursuing them

• Evasion of predators
• Mate selection
• Orientation or navigation using fine-scale landmarks
• Recognition of objects and individuals of same/different
species
• Visual communication

Require fine spatial resolution (1 arc min or 1/60 deg.)

Needs an optical system that can focus light
Very small angle of light capture for each receptor

Class 4 tasks require the evolution of a lens (or other focussing system) and
integration times need to be short to avoid motion blur.
 • intensities
Fig. 2. Minimum Minimum intensities
from Table required
1, for the four to support
classes of sensory tasks, plottedthe four
together withclasses of visual
the daily variation of naturaltasks,
luminancesplotted with the
and daylight daily
intensities at different depths in clear water. Blue indicates calculations for a 10 µm diameter cell with no membrane stacking and no focusing optics (just
variation of natural luminance and daylight intensities at different depths in clear water.
screening to obtain the desired detection angle). Calculations for membrane stacking are indicated by green and for focusing optics (and membrane stacking)
by red. The color gradients at the lower end of the bars show the range of gradually decreasing function between the primary values from Table 1 (dotted
• bracketed
lines), and the Blue values
indicates calculations
where sensory information is for a cell
assumed with
too poor notask.
for the membrane stacking and no focusing optics
• Calculations for membrane stacking are indicated by green and for focusing by red (Nilsson, 2013).
ovations, each enabling transition to a higher class of sensory
k. This means that the sensory organs required for the different
sses of sensory tasks can be identified by their structure, and it
ossible to transfer the classification of tasks to a corresponding
lutionary classification of photoreceptor organs.
Evolution of visual behaviours
Class I tasks would then be associated with cells lacking any
d of membrane stacking and any proximity to screening pigment
ther light-shielding structures. Such light sensitive cells are indeed
wn from many corners of the animal kingdom (e.g., Provencio
photoreceptor cells typically form membrane stacks of a few 10s to
several 100 layers (Eakin, 1972; Salvini-Plawen & Mayr, 1977;
Jékely et al., 2008). Some median eyes, such as the nauplius eyes
(frontal eyes) of crustaceans are directional photoreceptors that
possibly aid in controlling body orientation (Elofsson, 2006). The
paired eyespots of Acoels are unique in having a rather unspecial-
ized membrane without microvillar or ciliary extensions (Yamasu,
1991). The sensitivity calculations also indicate that membrane
stacking is not necessary for phototaxis in well-lit habitats. But

Visual behaviours correspond to the

sequential stages of eye evolution

A. unshielded photoreceptor cells

B. pigmented ocelli with broadly

directional photoreceptors

C. pigmented pit or cup eyes with low

spatial resolution

D. focussing optics and high spatial

resolution

3. Schematic illustration of the evolution of photoreceptive behaviors on a vertical scale of task complexity, with the position of major functional inno-
ons indicated. The line for directional photoreception is dashed to indicate that class II tasks may become superfluous by the evolution of class III tasks,
reas the other classes remain relevant after a higher class has evolved. Eyes capable of class IV tasks can of course still handle class III tasks. The corre-
Each higher level of task requires faster integration times, narrower angular
nding receptor/eye morphologies are shown to the right. Note that compound and single chambered eyes are principally different solutions suggesting
pendent transitions from class II to class III.
selectivity and higher contrast sensitivity. Therefore, system must capture more
photons per unit time. This is aided by membrane stacking and focussing optics
 Phylogeny of visual behaviours
Eye evolution and its functional basis 15

• Transitions between classes of

visual behaviour are indicated by
color.

Fig. 7. The classes of photoreceptive tasks plotted on a metazoan phylogeny, using the arguments from the functional discussion in this paper together
• Four phyla have developed high resolution vision (spiders, insects/crustaceans,
with information on receptor morphology (mainly from Salvini-Plawen & Mayr, 1977), and the occurrence of opsins (Plachetzki et al., 2007; Porter
et al., 2011; Schnitzler et al., 2012). For clarity, minor bilaterian taxa were omitted, and because these only have class II photoreception, the most
cephalopods and vertebrates)
parsimonious transitions to class III are the ones indicated by color. The exact pattern of transitions should be interpreted with caution because it is
sensitive to the choice of phylogenetic tree, which is here based on Philippe et al. (2009), with the placement of the Acoela according to Philippe et al.
• This indicates that spatial vision has evolved independently in different animal groups.
(2007).
screening pigment ized membrane without microvillar or ciliary extensions (Yamasu,
ve cells are indeed 1991). The sensitivity calculations also indicate that membrane
m (e.g., Provencio Diversity of eye design
stacking is not necessary for phototaxis in well-lit habitats. But

receptive behaviors
Spatial on a vertical
vision can scale of taskin
evolve complexity,
different with ways:
the position of major functional inno-
on is dashed to indicate that class II tasks may become superfluous by the evolution of class III tasks,
class1.hasMore
evolved.photoreceptors aretasks
Eyes capable of class IV added to thestillsame
can of course handle pigment shield
class III tasks. or cup
The corre- (Left - camera eye)
ight.2.
NoteThe entire organ
that compound is chambered
and single multiplied eyes(Right - compound
are principally eye) suggesting
different solutions
 Diversity of eye design

Shadow Refraction Reflection

Different modes of image formation used in both chamber and compound eyes.
 Diversity of eye design

a. compound eye with

human-like resolution across
the visual field.

b. compound eye with a

resolution of 1 arcmin at the
fovea, but falling off with
eccentricity (as in the human
eye).

From Kirschfeld (1976)

The need to constrain eye size makes the camera or chamber eye a better solution.
 “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 confess, absurd in the highest
degree...”

Charles Darwin: On The Origin of Species, Chapter 6 - "Organs of Extreme Perfection"

So how long does it take to evolve a high resolution

eye?
 How long does it take to evolve an eye?

Assuming a continuous selection for improved spatial resolution, a patch of light-

sensitive epithelium can be transformed into a fully focussed camera-type eye in less
than 400,000 generations (or similar years in small invertebrate) (Nilsson and Pelger,
1994).
Summary
• Eyes of most species evolved rapidly during the Cambrian period, coinciding with
increases in body size, improvements in mobility and visually guided predation.

• Eye evolution and visually-guided behaviour are closely linked: animals have
acquired visual systems that detect light and can support low and high resolution
behaviours.

• Visual systems evolve through the gradual acquisition of complex visual behaviours.
• Evolution has found different eye solutions to the same problem: need for increased
spatial resolution can be achieved by camera-type eye and compound eyes

• Different types of eyes (size, design, placement etc.) can evolve from range of
different tissues types and once optimized to the visual needs or behaviours of the
animal, no further adaptations need take place.

• Eye evolution could have happened in a relatively short period of time (on a
geological time scale) - around half a million years.

• Structures responsible for spatial vision in vertebrates, cephalopods and arthropods

have evolved independently: embryonic development is different in each group.
Further reading & resources
Land, M.F. & Nilsson, D-E. (2012). Animal Eyes. Oxford: Oxford University
Press.

Nilsson, D-E. (2009). The evolution of eyes and visually guided behaviour.
Philosophical Transactions of the Royal Society of London. Series B, Biological
Sciences 364, 2833–2847.

Lecture on the evolution of vision - http://www.gresham.ac.uk/lectures-and-

events/the-evolution-of-vision

Blog on eye evolution - http://blogs.scientificamerican.com/science-

sushi/2012/01/16/evolution-the-rise-of-complexity/

Eyes on the prize: the evolution of vision http://www.nhm.ac.uk/discover/eyes-

on-the-prize-evolution-of-vision.html