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Spam and the evolution ofthe fly’s eyeDaniel Osorio
SummaryThe open rhabdoms of the fly’s eye enhance absolutesensitivity but to avoid compromising spatial acuity theyrequire precise optical geometry and neural connec-tions.(1) This neural superposition system evolved fromthe ancestral insect eye, which has fused rhabdoms. Arecent paper by Zelhof and co-workers(2) shows that theDrosophila gene spacemaker (spam) is necessary for de-velopment of open rhabdoms, and suggests thatmutantsrevert to an ancestral state. Here I outline how openrhabdoms and neural superposition may have evolvedvia nocturnal intermediates, and discuss the implicationsfor the role of spam in insect phylogeny. BioEssays29:111–115, 2007. � 2007 Wiley Periodicals, Inc.
Introduction
The ommatidium, which is the basic modular unit of insect
compound eyes (Fig. 1), normally contains a set of eight
photoreceptor cells. Themembrane on one side of the cell is a
specialised microvillar structure known as a rhabdomere. A
high density of photopigment protein (rhodopsin) gives the
rhabdomere a higher refractive index than that of normal
cytosol. Optical waveguide effectsmean that light focussed on
the rhabdomere tends to be trapped within it. Most insect
lineages have a fused rhabdom, where the rhabdomeres of all
photoreceptors form a single waveguide but, on at least five
occasions in evolutionary history, the rhabdomeres have
separated to form what is is usually called a open rhabdom
(Figs. 1–3).
The best-known open rhabdom eyes are those the higher
flies (Brachycera), which include Drosophila. Here the seven
separate rhabdomeres form an open rhabdom, with a
distinctive trapezoidal form. Spam is a secreted protein that
acts with two additional genes chaoptin and prominin to
prevent the rhabdomeres from adhering to one another.2 In
Spammutants, the rhabdomeresmakedirect contact, as is the
case in many other insects (Figs. 1 and 2). When the study2
was extended to other insect lineages, it was found that the
diurnal mosquito Toxorhynchites, which has open rhabdoms,
expresses spam, whereas the mosquito Anopheles gambiae,
which is described as a ‘closed system’, does not. Neither do
unrelated insects where rhabdomeres touch, namely the
beetle Tribolium and the honeybee Apis. Finally, expressing
spam in the Drosophila ocellus causes rhabdomeres there
to separate. The study by Zelhof and co-workers (Ref. 2)
illustrates nicely how expression of a single structural protein
can determine morphology of a complex organ. A possible
implication is that it may be relatively straightforward for the
rhabdom morphology to evolve adaptively according to
functional requirements of the visual system. If spam acts a
switch, one might expect two main types of rhabdom
morphology (Fig. 1) according to whether or not it is expressed
in the compound eye. How then do these observations fit into
the larger picture of compound eye evolution?
Spatial acuity versus absolute sensitivity
The requirement that photoreceptors should operate as
optical waveguides limits the minimum diameter of photo-
receptive structures to about 1.5 mm.(3) In compound eyes,
larger diameter rhabdoms increase absolute sensitivity
(i.e. photon catch) at the expense of spatial acuity. Thus the
grasshoppers Locusta and Valanga vary the diameter of their
fused rhabdom with a pronounced circadian rhythm, from
about 1.5mm in daytime to 5 mm at night.(4,5)
Controlling rhabdom diameter is not the only means of
modifying optics according to the light level. Four insect groups
have annular rhabdoms, where the rhabdomeres of the six
short visual fibres (R1-6) forma ring around the two long visual
fibres (R7,8; Figs. 1, 2). The isopod Ligia (Crustacea,
Malacostraca) has a similar arrangement, but without the
central rhabdomeres.(6) In the primitive insect open rhabdoms,
light is focussed on all receptors in dim conditions whereas, in
bright light, the outer ring of receptors is covered by pupil
pigment (Fig. 3).(7–10) This arrangement gives a high spatial
acuity photopic system based on the long visual fibres, and a
low acuity scotopic system based on R1-6. In higher flies
(Brachycera), the division of labour between receptors is
different, in that the short visual fibres are used at all light
levels.(11)
A possible advantageof an annular over a fused rhabdom is
thatmakesefficient useof a givenvolumeof photopigment and
photoreceptive membrane. Waveguide effects mean that light
does not travel in the central lumen, but is concentrated in the
rhabdomeres. This concentration could be beneficial because
photoreceptive membrane is metabolically costly,(12) and also
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK.
E-mail: d.osorio@sussex.ac.uk
DOI 10.1002/bies.20533
Published online in Wiley InterScience (www.interscience.wiley.com).
BioEssays 29:111–115, � 2007 Wiley Periodicals, Inc. BioEssays 29.2 111
What the papers say
Figure 1. Diagramofommatidiawith fusedandopen rhabdoms,showing radial views (left)andcrosssections through theommatidia.Terms that
are used in the text can be defined as follows: the ommatidium is the modular unit from which the compound eye is constructed. The cellular
organization of the ommatidium is highly conserved amongst the insects andmany crustaceans (Malacostraca).(26,27) Normally each ommatidium
containseightphotoreceptors.Short visual fibres (R1,6)arephotoreceptor cellswhoseaxonsproject to the first optic ganglion.Typically theycontain
a photopigment that ismost sensitive to green light (max sensitivity at about 500nm). Long visual fibres (R7,8) are photoreceptor cellswhose axons
project through the firstopticganglion.Often theycontainaphotopigment that ismost sensitive toUV light (maxsensitivityatabout360nm),but there
isconsiderablevariation. Inarthropodphotoreceptorsvisualphotopigment (rhodopsin) resides inmicrovilli,which liealongonesideof thecell to form
a rhabdomere. Thehighdensityof rhodopsin in the rhabdomeregives thisstructureahigher refractive index thansurroundingcytoplasm,andallows
it toactasanopticalwaveguide.The rhabdom is thecollectivenamefor the rhabdomereswithinanommatidium.The fused rhabdom is theancestral
form, and found inmost insect lineages.Here the rhabdomeres are fused to forma singlewaveguide, so that light focussed on the rhabdom travels
through all eight photoreceptors. In open rhabdoms the rhabdomeres do not form a single waveguide. There are many variants (Figs 2,3), but
typically R1–6 surround R7,8. The version illustrated with R1–6 having fully optically isolated rhabdomeres occurs many Diptera. Note that the
conventional nomenclature differs from that in the recent Nature paper.(2) Conventionally ‘open’ rhabdoms are contrasted with ‘fused’, whereas
the term ‘closed’ isnotused.Given that in flies there isnocleardistinctionbetween fullyopenrhabdoms,where rhabdomeresdonot touch,and those
where they do (Figs 2,3) the conventional distinction seemed logical — at least until the discovery of Spam.
Figure 2.
What the papers say
112 BioEssays 29.2
because noise due to spontaneous isomerization of the
photopigment is proportional to the quantity of pigment.(13)
An open rhabdom, associated with pooling of receptor
signals, almost inevitably sacrifices spatial acuity compared to
the narrowest possible fused rhabdom, but the extent of the
blurring depends on two factors: firstly, the degree of optical
coupling between receptors (Fig. 2), and secondly, the angular
divergence between optical axes of photoreceptors whose
outputs are combined in the optic lobe (Fig. 4). The precise
structure of the fly eye virtually eliminates these acuity losses,
and gains a six-fold increase in quantum catch.(14–17)
The performance of open rhabdom eyes is dependent on
the connectivity of the photoreceptor axons (Fig. 4). In fused
rhabdomcompound eyes, it is usual for all receptor axons from
the ommatidium to project to a single cartridge (i.e. column) of
neurons in the lamina, where they can be pooled. Some eyes
enhance sensitivity at the expense of acuity by pooling signals
via receptor axon collaterals that connect neighbouring
ommatidia, as in the scorpionfly, Panorpa (Mecoptera).(9,18,19)
This type of pooling may have been associated with the initial
appearance of open rhabdoms. Such an eye has poor
angular resolution. From this nocturnal system, acuity can be
improved by optical isolation of rhabdomeres, and by refine-
ment of their projections to the lamina, first by so-called
asymmetric pooling, and then by true neural superposition
(Figs. 1 and 3).(9,18,20,21)
Evolution of Dipteran neural
superposition eyes
Although one can readily envisage how the fly’s eye evolved,
this does not mean that the intermediate stages were
necessarily inferior. These stages probably represented
solutions to the problem of optimising the compromise
between absolute sensitivity and spatial acuity, which vary
according to lifestyle. It is therefore no surprise that open
rhabdoms have evolved repeatedly (Fig. 2), and that, within
this basic scheme, there are many variants.(7,8,21) All known
Diptera have open (as opposed to fused) rhabdoms, and all
higher flies (Brachycera) have neural superposition essentially
similar to that of Drosophila.(21,22) Thus the ‘lower’ Diptera
(Nematocera) are of most potential interest in relating the
expression of spam to morphological diversity.
Nematocerans are often relatively sluggish and/or
noctural, and rhabdoms of such flies have been described
from several families including: mosquitoes (Culicidae:
Anopheles), midges (Simulidae; Wilhelmia), fungus midges
Figure 2. A: Rhabdoms from compound eyes of various insects. In most orders, photoreceptor rhabdomeres fuse to form a single light
guide, typically 2—5mm across. Scorpionflies (Mecoptera), which are a sister taxon to the Diptera, have fused rhabdoms. Open rhabdoms
evolved independently in at least four insect groups: earwigs (Dermaptera), Heteropteran bugs (Heteroptera), a major group of beetles
(Coleoptra: Cucujiformes), which includes Tribolium, and Diptera. The extent of contact between rhabdomeres differs according to the
species, the light adaptation state, and, amongst some flies (Diptera: Culicidae, Tipulidae) and other groups location along the rhabdom
(Fig. 3).(6,7,20,21,25) A trapezoidal open rhabdom isa commoncharacter sharedby, andunique to, higher flies (Brachycera).Otherwise thesix
short visual fibres photoreceptors (R1–6) are arranged in a roughly hexagonal pattern around the long visual fibres (R7,8). In some cases
(Heteroptera, Tipula), light adaptation causes pupil pigment to block light from the outer rhabdomeres, which suggests that R1–6 are high
sensitivity low resolution system,with the long visual fibres giving high spatial acuity in bright conditions.(9) The figure is redrawn fromRef. 9,
incorporating data from other sources.(20,21)B:Convergent evolution of open (as opposed to fused) rhabdoms illustrated by a phylogeny of
insects andmalacostracan crustaceans showing the five orders that have open rhabdomsafter. A sister taxon is shown for each that has
retained the fused rhabdom. Whilst there is much variation in the morphology of open rhabdoms, I am unaware of any instance where an
open rhabdom has reverted to the fused form. The phylogeny is based on various sources.
Figure 3. Illustrations open rhabdoms from Grenacher’s
masterpiece on compound eyes.(7) Both show how rhabdo-
meres tend to converge or fuse distally, an arrangement that
benefits the trade-off between absolute and angular sensitivity
in theabsenceof neural superposition.(20)A:Anommatidiumof
a bug, the backswimmer (Notonecta, Heteroptera), in the light
adapted state, showing pigment covering the rhabdomeres of
R1–6.(9,10) B: Three ommatidia of a tipuld fly (Tipula sp;
Diptera, Nematocera).(9,12,25)
What the papers say
BioEssays 29.2 113
(Mycetophilidae: Arachnocampa), ghost midges (Chao-
boridae: Chaoborus) and craneflies (Tipulidae: Tipula;
Ptilogyna).(18,20–22) Faster flying and diurnal nematoceran
flies include the large mosquito Toxorhynchites, and the
bibionid fly, Bibio marci, whose males have a specialised high
acuity dorsal eye for finding females.(2,20,23) The underlying
connection pattern of receptor axons reflects this diversity, and
neural superpositionappears to haveevolved independently in
Brachycera, in Bibionidae and in Culicidae (Fig. 4).(16,23–25)
As we have said, it is no surprise that the nocturnal forms
have more spatial pooling, and diurnal forms have fully
developed neural superposition (Figs. 1 and 3). With respect
to the role of spam, the subtleties of rhabdom structure in
nematocerans are of interest. In particular, there is no clear
distinction between eyes where rhabdomeres do not touch
(and are termed open by Zelhof and co-workers(2)), and those
where they do (and are termed closed by Zelhof and co-
workers(2)). For example, when its eye is dark-adapted, the
rhabdomeres of the tipulid Ptilogyna fuse in the distal (outer)
part of the rhabdom, where the image is focussed, but theyare
separated proximally. Ptilogyna’s rhabdomeres become fully
separate on light adaptation (Fig. 2).(21,22) The isopod
crustacean Ligia has a similar arrangement to Ptilogyna
(Fig. 2)(6) whereas, in Anopheles (Culicidae), rhabdomeres
never separate on light adaptation.20 In the absence of
neural superposition, a fused distal rhabdom that opens
proximally allows high sensitivity with relatively high acuity
(Fig. 3).(20)
Conclusion
To conclude, several insect and crustacean lineages have
open rhabdoms, probably to enhance vision in dim light. Open
rhabdom eyes with neural superposition are derived by
refinement of rhabdom structure and of neural connections
in three dipteran lineages that moved from nocturnal to
daytime activity (Fig. 4).(9,18,21) The range of rhabdom
structures reflects the specific demands of visual acuity and
sensitivity, aswell as the insect’s phylogenetic history. The role
of Spacemaker in preventing rhabdomeres from touching one
another(2) shows how a relatively simple genetic mechanism
could underlie this adaptive radiation. However, the evidence
fromnematoceran flies suggests that continuous variation is to
Figure 4. A rangeof neural connectionpatterns beneath open rhabdoms that could account for the evolution of neural superposition from
nocturnal eyes.(9,18) Normally in fused rhabdom apposition eyes axons of all eight photoreceptors project to a single coaxial lamina
cartridge. Short visual fibre (SVF; R1–6) axons terminate in the first optic ganglion the lamina. Long visual fibre axons (LVF; R7,8, not
illustrated) project through the lamina to the second optic ganglion. LVFs may however synapse in the lamina. A: Symmetrical pooling
probably occurs in some fused rhabdom eyes such as that of the scorpionfly, Panorpa where SVF axons connect to outputs from
neighbouring ommatidia.(9,18) This pooling reduces spatial resolution, and may favour evolution of open rhabdoms. Resolution can be
improved by screening the SVFs, as in Heteroptera (Fig. 2).B:Asymmetric pooling occurs in certain nematoceran flies such asChaoborus
and Tipula. Here spatial acuity is improved because axons from the outer rhabdomeres (typically R1–6) divide to project asymmetrically to
connect to lamina cartridges that share inputs with overlapping receptive fields.(18) C: Neural superposition. A set of six SVF axons with
coincident receptive fields project to a single laminacartridge. InBrachyceran flies, the projection is to aneighbouringcartridge,(16) but it is to
the second nearest in the bibionid Bibio.(23)
What the papers say
114 BioEssays 29.2
beexpectedandnot simplyaswitch fromopen toclosed forms.
It will be interesting to see how its patterns of expression of
spam match the diversity of rhabdom forms, and diurnal
changes that occur in the nematoceran flies, and perhaps
other insect lineages.
Acknowledgments
I thank M.F. Land, R Melzer and D.-E. Nilsson for comments
and advice.
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