AMER. ZOOI... 19:647-653(1979).
Evolutionary Significance of Photoreceptors: In Retrospect
RICHARD M. EAKIX
Department of Zoology, University of California, Berkeley, California 94720
SYNOPSIS. This essay presents an updating of the author's theory that there are two major
lines in the evolution of photoreceptors, one ciliary and the other rhabdomeric (microvillar).
Arguments are presented for rejecting a new and alternative theory of Salvini-Plawen and
Mayr (1977) that photoreceptors have arisen many times, independently of one another,
and that there are no major lines in the evolution of light-sensitive organelles. Arguments
are also advanced against the theory of Vanfleteren and Coomans (1976) and others that
microvillar photoreceptors are induced by ciliary structures.
A little over fifteen years ago I proposed
(Eakin, 1963) that there have been two
evolutionary lines of photoreceptors, one
line in taxa with light-sensitive cilia (variously modified usually) and the other in
taxa with rhabdomeres (villi or lamellae of
the cell membrane). The former line included the radiates and deuterostomes; the
latter included the flatworms, aschelminths, and protostomes (Fig. 1). This
speculation was like the prediction of the
outcome of an election by a political analyst
on the basis of early returns from a few
precincts. In the succeeding years, numerous apparent exceptions have been discovered, such as the findings of ciliary photoreceptors in some protostomes and of
rhabdomeres in some deuterostomes.
Each time an exception has been found,
the hunter has taken aim at my balloon,
now punctured many times but still airborne, I hope. But these were pot shots in
comparison with the barrage recently fired
Acknowledgments of the assistance of many persons
in the studies that provided the initial impetus and
subsequent basis of my theory of evolution of photoreceptors are given in published papers. I express
anew, however, my gratitude to four research associates: Jean L. Brandenburger, now in the fifteenth
year of our happy and fruitful association; Jane A.
Westfall, who shared in early discoveries offinestructure of photoreceptors, and Colin O. Hermans and
Robert M. Woollacott, collaborators in a few studies
and helpful critics of others. For the financial support
of the National Institutes of Health (CM 10292 and EY
02229) over many years 1 am profoundly appreciative.
by L. V. Salvini-Plawen and Ernst Myr
(1977) who postulate that photoreceptors
have arisen "in at least 40 if not 65 or even
more separate phyletic lines," (1977, p.
209), and that, therefore, major lines of
evolution of light-sensitive organelles do
not exist (Fig. 2). Their paper is a highly
scholarly, comprehensive, and carefully
reasoned work that was graciously given to
me for reading and comment before publication.
Salvini-Plawen and Mayr propose a classification of four different photoreceptors.
To my ciliary and rhabdomeric types they
added unpleated (i.e., unmodified) cilia —
found in Hydrozoa, Nematoda, Entoprocta
and Ectoprocta—and a diverticular (i.e.,
ganglionic) type—occurring in a wide variety of animals from flatworms to amphioxus.
Salvini-Plawen and Mayr treat ciliary
photoreceptors that increase membranous
surface by infolding or outfolding of the
ciliary membrane as distinct from those
that achieve surface enlargement by increasing the number of cilia. I see no advantage to this distinction. Both are ciliary
in nature, i.e., with an axoneme of microtubules and a basal body (centriole), and
both have photopigments incorporated
into their ciliary membranes.
Furthermore, I hold that Salvini-Plawen
and Mayr's diverticular type is not significantly different from the rhabdomeric
type. In both the putative light-sensitive organelles are villi or lamellae of the plasmalemma unassociated developmentally
647
648
RICHARD M. EAKIN
Cephalochordata
Arthropoda
Ciliary Line
Echmodermata
Platyhelminthes
Rhabdomeric
Protista
FIG. 1. Representation of the theory of two lines of evolution of photoreceptors based on Eakin (1968).
EVOLUTION OF PHOTORECEPTORS
ciliary
649
rhabdomeric
FIG. 2. Representation of the theory ofindependent Aurelia); I, intermediate ciliary-rhabdomeric type (e.g.,
evolution of photoreceptors, from Salvini-Plawen and Henricia); K, rhabdomeric type with lateral microvilli
Mayr (1977). A, Unmodified monociliar cell with mi- (e.g., tornaria larva of Ptychodera); L, rhabdomeric type
crovilli; B, unpleated ciliary type (e.g., Bugula); C, with peripheral microvilli (e.g., Pecten and Peripatus);
ciliary type with sacs (e.g., Pecten); D, ciliary type with M, rhabdomeric type with corona of microvilli (e.g.,
lateral paddles (e.g., Pleurotrachea); E, ciliary type withPhascolosoma); N, rhabdomeric type with distal miinternal tubules (e.g., Sagitta); F, ciliary type with disks crovilli (e.g., Helix); O, rhabdomeric type with medial
(e.g., a vertebrate); G, ciliary type with lateral lamellae microvilli (e.g., Ciona); P, rhabdomeric type with mi(e.g., Pleurobrachia); H, ciliary type with microvilli (e.g.,crovilli in an internal vesicle (e.g., Lumbricus).
(see below) or physiologically with cilia.
Further, these modified ganglionic cells are
said to be "acilious"; yet I believe that if a
careful search were made, cilia would be
found in the embryo if not in the adult,
because cilia are ubiquitous, particularly in
ectodermally derived organs. Moreover,
the photosensory cells in the cerebral ocelli
of the polychaete Nereis (Eakin and
Westfall, 1964) and in those of the archiannelid Nerilla (Eakin et al., 1978) are known
to bear cilia, although the numerous mi-
650
RICHARD M. EAKIN
crovilli are probably the photosensory organelles.
Setting aside the question, purely
academic to my thinking, of whether there
are two, three, or four distinct types of
photoreceptors, I now debate the major
question: do kinds of light-sensitive organelles have evolutionary significance? If
the answer is yes, and I so affirm, how do I
explain the presence of ciliary photoreceptors in protostomes, as for example, in the
branchial and pygidial ocelli of annelids
(Krasne and Lawrence, 1966; Kernels,
1966, 1968; Ermak and Eakin, 1976, to
name a few works) or in the pallial or tegmental eyelets of mollusks (Barber et al.,
1967; Boyle, 1969; Hughes, 1970, to cite a
fe'w references). I believe, in agreement
with Salvini-Plawen and Mayr (1977, p.
222), that these ciliary receptors are indeed
cenogenetic.z.e., secondarily evolved, structures. In the cerebral ocelli of annelids and
mollusks, however, the photoreceptors are
microvillar, and I hold that integumentary
and cerebral ocelli are nonhomologous.
The few scattered ciliated cells that have
been observed in or near the brains of annelids have not been proven to be photoreceptors. They are not associated with a
pigmented cup, or a lens-like body, or a
tapetum, structures commonly found in
eyes, and so far there is no neurophysiological evidence that they are light-sensitive.
Some recent ultrastructural studies of
cerebral ocelli in annelids and mollusks
strengthen the above thesis. Eakin et al.
(1978) examined theeyecupsof a representative each of four of the five presently recognized families of archiannelids (see
Hermans, 1969). In each instance the
photoreceptor was an array of microvilli.
With one exception, no cilia were observed
in the ocelli of these archiannelids. The exception is that in two specimens of Nerilla
we found a pair of rudimentary cilia in one
of the two sensory cells, but the cilia appeared to have no relation to the microvilli.
We drew the conclusion that the rhabdomere was proably the receptoral organelle
of cerebral ocelli in the earliest annelids,
regardless of whether the archiannelids
represent an ancestral stock or whether
they are secondarily simplified, interstitial
polychaetes.
Rosens al. (1978, 1979) have studied the
cerebral ocelli in an adult mussel (a pelecypod) and in the trochophore larva of a
chiton (a polyplacophoran). The obvious
photoreceptor is a rhabdomere, although
cilia are present, one per sensory cell. These
authors believe that cerebral ocelli are not
homologous with the pallial eyecups of
bivalves or the tegmental ocelli of chitons,
both of which may bear ciliary photoreceptors, and that the rhabdomere is "conserved
in cerebral ocelli and does aid in establishing the broad evolutionary affinities among
the protostomous phyla" (Rosenef a/., 1978,
p. 17).
I present now some comments on the
occurrence of cilia, well-developed or rudimentary, in or adjacent to a rhabdomere
in a cerebral ocellus. Is this an instance of
"guilt by association"? I regard the cilia in
those ocelli as adventitious, that is, incidental and probably not functioning as
light-sensitive organelles. Their presence
can be explained by the developmental origin of cerebral ocelli from ectoderm, which
is typically ciliated. It is not surprising to
find cilia or their accessory structures, basal
bodies and striated rootlets, as developmental vestiges associated with rhabdomeres, therefore.
Some workers (see Vanfleteren and
Coomans, 1976, for references) have speculated that the presence together of ciliary
structures and rhabdomeres is more than
incidental. The argument can be summarized by the following quotation from
Vanfleteren and Coomans (1976, p. 165).
"It is suggested that in both types [ciliary
and rhabdomeric] the elaboration of the
photoreceptoral organelle is induced by a
ciliary formation, which, after initiating
membrane proliferation, may become
more or less abortive (rhabdomeric type) or
may develop further into a ciliary organelle
(ciliary type)."
The photoreceptors of arthropods appear to be exclusively rhabdomeric. The
only possible exception known to me is the
crustacean organ of Bellonci that contains
remarkable ciliary structures. Chaigneau
(1971) concluded from his studies of this
organ in an isopod that it might be photosensory in function, but a recent work
(Renaurd-Mornant et al., 1977) on an ap-
EVOLUTION OF PHOTORECEPTORS
parently homologous structure (Chaigneau, 1977) in a primitive, cave-dwelling
crustacean (subclass Mystacocarida) "does
not point to a photoreceptive function,"
(Renaud-Momante/a/., 1977, p. 476). How
do the arthropodan rhabdomeres arise?
Are they induced by embryonic ciliary
structures that do not persist in the adult?
Wachmann and Hennig (1974) conducted
an investigation of the possible role of centrioles in the development of rhabdomeres
in a leaf-cutter bee. In an early pupal stage
these organelles of a differentiating retinula cell assume an in-tandem position
proximal to the nucleus. A striated rootlet
then develops from them and extends basally. The authors conclude: "it was not possible to demonstrate any connexion between the centrioles and the developing
microvilli of the rhabdomeres" (p. 337) that
arise from the cell membrane of the retinula cell distal to its nucleus. Finally, if cilia or
basal bodies are organizers of microvilli,
one would expect brush borders to exhibit
evidence of ciliary structures in the embryo
if not in the adult. To my knowledge, such a
case is not known.
On the other hand, cilia appear in unexpected places: pituitary, adrenal gland, and
pancreatic islets (see Eakin et al., 1978, for
references) and in fibroblasts, odontoblasts,
chondrocytes and osteocytes (see Wilsman,
1978, for references). Whenever a centriole
lies beneath a cytomembrane — not necessarily the cell membrane —there is the possibility of the induction of a cilium. The
ubiquity of ciliary structures needs to be
considered when drawing conclusions
about the significance of those found in association with rhabdomeres.
There are other taxa in my rhabdomeric
line in which putative ciliary photoreceptors have been found: some flatworms (see
Ehlersand Ehlers, 1977a,b, for references),
a gastrotrich (Teuchert, 1976) and a nematod (Burr and Burr, 1975). The best explanation for these exceptions is probably
Salvini-Plawen and Mayr's theory of independent evolution.
Now what is to be said about the echinoderm line? The exceptions —microvillar instead of ciliary photoreceptors—have been
few until the present. The eyecups of Hesse
along the neural tube of amphioxus (Eakin
651
and Westfall, 1962) and the eye of the
pelagic tunicate, Salpa (Gorman et al., 1971)
are clearly rhabdomeric. These may be
other instances of cenogenetic evolution.
The case in hemichordates is ambiguous, I
think, judging from one study (Woollacott
et al., 1972) of the ocellus of a tornarian
larva. The receptor appears to have both
ciliary and microvillar features.
I have long been dissatisfied with the evidence of ciliary photoreceptors in echinoderms. Our early study (Eakin and
Westfall, as reported in Eakin, 1963, 1968)
and those of Vaupel-von Harnack (1963)
and Emerson (1977) on the ocelli of seastars
showed the ocellar cavities to be filled with
sensory cell processes, microvilli, and cilia.
The cilia were unlike kinocilia in that they
had basal excrescences, interpreted by us as
microvilli, and atypical axonemes. The electron micrographs in all of these papers did
not give a satisfactory picture of the relationship, if any, between the cilia and the
other microvilli. We thought that the problem was poor preservation of structure, so
we tried many fixatives in the past several
years.
This year Yamamoto and Yoshida (1978)
published an account of the effects of light
and darkness on a holothurian ocellus, and
demonstrated unmistakably that the microvilli are the light-sensitive organelles. A
restudy of the asteroid ocellus was immediately undertaken by Mrs. Brandenburger and me in three seastars (Patiria,
Leptasterias and Henricia). We used a better
fixative and scanning as well as transmission
electron microscopy and, most importantly,
we compared specimens from both darkadapted and light-exposed animals (Eakin
and Brandenburger, 1979). It then appeared that we had been looking at seastars
at the wrong time of the day to obtain critical information on the nature of the microvilli. They arise from the sensory cell
processes without any morphological connection to cilia, one per process. Moreover, the microvilli are sensitive to light. In
ocelli illuminated for a day or more, the villi
become deranged and abscised from the
processes, whereas in the dark they appear
to regenerate by elongation and neoformation. Because of these recent studies the
echinoderm photoreceptor must be reas-
652
RICHARD M. EAKIN
signed to the microvillar category.
Where does my theory of two lines of
evolution of photoreceptors now stand?
Stated facetiously: without a ciliary photoreceptor in Patiria et al. I have lost the seastars; without the asteroids and holothurians the echinoderms are lost; without the
echinoderms the echinoderm line may be
lost; and without the echinoderm line my
theory may be lost. Note the italics.
Is the ciliary line really lost without the
echinoderms, though? I think not. There is
indeed a remarkable variation in ciliary
photoreceptors: outfoldings to form villi
(cnidarians) or lamellae (ascidians) or
whorls (ctenophores); infoldings to create
disks (vertebrates) or tubules (chaetognaths); a basal flagellar swelling (Euglena);
or even unpleated cilia (bryozoans). But
there is one basic feature that all have in
common, the incorporation of a photopigment in the ciliary membrane, irrespective
of the membrane's morphology. I believe
that the thread of continuity is the "know
how" to build and to use the chief structural
protein of the ciliary membrane—an opsin
conjugated with vitamin A — to capture
photons. This novel and highly portentous
evolutionary step occurred in some early
protist, and it has been passed down
through the geologic ages to the vertebrates. But somewhere above the radiates, a
mutation, or series of mutations, endowed
the sensory cell plasmalemma with photosensitivity, and by the formation of villi or
lamellae, in various configurations, surface
area was increased, as in ciliary modifications, thus enhancing the light-gathering
power of the cell membrane. Rhabdomeric
photoreceptors then appeared and were
perpetuated along the mollusk-annelidarthropod line. In some taxa of that
lineage, however, either the photosensitive
cilium was retained in the integument or a
ciliary photoreceptor was evolved anew.
And, it now appears, that photosensitive
microvilli arose independently and secondarily in the echinoderms.
There is probably no challenge to an assertion that cilia, per se, have evolutionary
significance. The "know how" to build a
cilium with its basal centriole and axoneme
of microtubules is in the DNA of all
eukaryotes from Euglena to Homo and from
Euglena to Ginkgo. Like the four purines
and pyrimidines of DNA itself the cilium is
a shining example of continuity in living
organisms during the couple of billion
years since nature first "invented" this remarkable organelle.
If you grant this premise, I take the next
step: The adaptation of the cilium as a light
detector by the incorporation of a photopigment in its membrane suggests a common ancestry of the taxa bearing lightsensitive cilia. My critics, however, say, No
—ciliary photoreceptors have arisen many
times independently of one another and
similarities are due to convergence. Until
persuaded to the contrary, I am holding to
the Darwinian principle of descent with
modification.
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