Origin and Evolution of the Vertebrate Eyelids and Adnexa
In humans, the eyelids form a flexible soft-tissue structure that serves important functions of protecting the cornea from direct injury, adding elements to the precorneal tear film, and helping to distribute these layers evenly over the surface of the eye. Together with the lacrimal drainage apparatus, the eyelids collect and propel tears to the medial canthus where they drain into the nose. The eyelashes on the eyelid margins sweep air-borne particles from in front of the eye, and the constant voluntary and reflex movements of the eyelids help modulate the amount of light that enters the pupil and protect the eye from excessive glare.
When closed, the eyelids cover the cornea and close the anterior entrance to the orbit. The periorbital fascia extends into the eyelids as the orbital septum and separates the orbit from the eyelid. All structures anterior to the orbital septum are technically in the eyelid so that the orbicularis oculi muscle and palpebral skin are usually considered to be part of the eyelid. However, anatomically this distinction is difficult to completely support since the orbital septum does not extend the full length of the eyelid and does not extend over the tarsus. In the medial canthal region, the septum divides into several separate layers, so that it cannot be used as a convenient division between the orbit and eyelid in this location.1 While it may be useful to think about the septum as anatomically separating the orbit and eyelid, physiologically the eyelid, with all of its layers from the skin to the conjunctiva, forms a single functional complex. Many of its structures, such as the levator aponeurosis in the upper eyelid and Müller supratarsal sympathetic muscle, bridge the boundary between orbit and eyelid. Therefore, any topographic division between these two compartments becomes somewhat arbitrary.
Like so many anatomical structures, it is easy and rather anthropocentric to assume that common structures in the human body are the same in other familiar animals. This was a long-held belief in antiquity that led to many erroneous descriptions of the heart and its circulation, the renal system, and the eye and orbit. Since the advent of the scientific revolution, increased biological and medical inquiry, and the lifting of prohibitions against human dissection, it has become clear that many aspects of human anatomy, not least the eye and its adnexa, are rather unique among different vertebrate groups.
The explosion of anatomic studies on animals and humans during the 19th and 20th centuries has shown a vast variety of visual adaptations of the eyes and adnexal structures subserving them. With respect to the eyelids, very basic primordial structures arose in some of the earliest vertebrate classes more than 400 million years ago and evolved in many different directions influenced by spatial partitioning of genetic diversity from population migration, reproductive isolation, differential reproductive success, and natural selection.
Within the subphylum Vertebrata, there are nine classes grouped into two superclasses, vertebrates without jaws (Agnatha) and those with jaws (Gnathostomata). Five of these classes are fishes including the extant hagfish and lamprey (Agnatha), Chondrichthyes, and Osteichthyes, and the extinct Placodermi. The others are Amphibia, Reptilia, Aves, and Mammalia. It is important to remember that all of the extant members of these groups have the same long evolutionary history and do not strictly represent a straight line lineage. Rather, they represent the current anatomical and physiological stages of each group that diverged from common ancestors in the distant past and which evolved at different rates, with some groups retaining more primitive features admixed with more recent adaptive changes.
The Eyelids and Adnexa in Fishes
The Jawless Fishes
The earliest stem vertebrates and fishes arose in the late Ordovician Period about 500 million years ago. Of the five classes of fishes, the hagfish and lamprey (superclass Agnatha) are jawless, have a cartilaginous skeleton with a persistent notochord, and have a completely open orbit. They lack scales, paired fins, a swim bladder, and a stomach. In the hagfish, the eyes are undifferentiated with no cornea, lens, or iris and they are covered by translucent skin with no eyelids. In the orbit, there are no extraocular muscles or motor nerves. It is still debated whether the hagfish visual system is a primitive vertebrate stage or if it is a derived, degenerate condition.
The lamprey passes through three stages during its life cycle. In the larval stage, the visual system is very simple with a nondirectional light-detecting eye spot, no extraocular muscles, and simple pretectal central neural connections. The larva enters a metamorphic stage with the gradual stepwise development of a well-developed image-forming camera eye without intraocular muscles2 and the development of more complex central visual control.3 In the adult, the orbit is an incomplete spherical connective tissue capsule
with only cartilaginous otic capsules.4 There are six extraocular muscles arising from three cephalic mesodermal myotomes to form three functionally complementary pairs (vertical, horizontal, and oblique). It has been proposed that these metamorphic stages in the lamprey visual system mirror the sequence of evolution in the early vertebrate visual system. Even though the adult lamprey extraocular muscles may resemble the primordial pattern in vertebrates, the specific arrangement differs from those of cartilaginous and bony fishes and homologies are not entirely clear.3,5 The dorsal (superior) and anterior (medial) rectus muscles and the caudal (inferior) oblique muscles are innervated by the oculomotor nerve. The caudal (lateral) rectus and vertical (inferior) rectus muscles are innervated by the abducens nerve, and the anterior (superior) oblique muscle is innervated by the trochlear nerve.4,6 The anterior (superior) and caudal (inferior) oblique muscles originate close together in the medial anterior orbit and rotate the globe axially. The anterior (medial) rectus muscle also originates anteriorly in the orbit. There is no retractor bulbi muscle. A unique extraocular muscle in the lamprey, the cornealis muscle, inserts by a tendon onto the cornea and aids in accommodation.2 The lamprey lacks true eyelids and the cornea is covered by a translucent cutaneous spectacle. The eyeball is separated from the surrounding skin by a shallow circumferential depression between the corneal epithelium and the skin, and the slightly raised outer ridge may represent the beginning of a rudimentary proto-eyelid (Figure 1.1).
with only cartilaginous otic capsules.4 There are six extraocular muscles arising from three cephalic mesodermal myotomes to form three functionally complementary pairs (vertical, horizontal, and oblique). It has been proposed that these metamorphic stages in the lamprey visual system mirror the sequence of evolution in the early vertebrate visual system. Even though the adult lamprey extraocular muscles may resemble the primordial pattern in vertebrates, the specific arrangement differs from those of cartilaginous and bony fishes and homologies are not entirely clear.3,5 The dorsal (superior) and anterior (medial) rectus muscles and the caudal (inferior) oblique muscles are innervated by the oculomotor nerve. The caudal (lateral) rectus and vertical (inferior) rectus muscles are innervated by the abducens nerve, and the anterior (superior) oblique muscle is innervated by the trochlear nerve.4,6 The anterior (superior) and caudal (inferior) oblique muscles originate close together in the medial anterior orbit and rotate the globe axially. The anterior (medial) rectus muscle also originates anteriorly in the orbit. There is no retractor bulbi muscle. A unique extraocular muscle in the lamprey, the cornealis muscle, inserts by a tendon onto the cornea and aids in accommodation.2 The lamprey lacks true eyelids and the cornea is covered by a translucent cutaneous spectacle. The eyeball is separated from the surrounding skin by a shallow circumferential depression between the corneal epithelium and the skin, and the slightly raised outer ridge may represent the beginning of a rudimentary proto-eyelid (Figure 1.1).
 FIGURE 1.1 In the lamprey, the eye is small, without eyelids, and covered with transparent skin. (Image used under license from Shutterstock.com.) |
The Cartilaginous Fishes
The Chondrichthyes include the cartilaginous sharks, skates, and rays, and they arose about 400 million years ago. The orbit is formed in cartilage and is incomplete, and the eye is cushioned by loose connective tissue. As in the lamprey, there are six extraocular muscles: four recti and two obliques. The two oblique muscles still originate anteriorly and insert onto the globe in common with the vertical rectus muscles. But unlike the lamprey, the medial rectus now originates posteriorly in common with the other rectus muscles.4 Neural innervation to the extraocular muscles is similar to that of higher vertebrates with the inferior rectus muscle now innervated by the oculomotor nerve. A unique orbital feature is a cartilaginous optic pedicle that forms a proplike structure extending from the cranium to the eye where it forms a cup-shaped synovial articulation with the posterior sclera, providing firm support to the globe while allowing full ocular motility.7 In some sharks and rays, this cartilaginous prop is thin and flexed so that when the rectus muscles relax, it pushes the eye forward aiding in passively opening the eyelids.4 In some deep benthic species, two additional orbital muscles arise from the cranium and insert onto the pedicle cup, and they may help to guide eye movements along a specific visual axis. These muscles are absent in bony fishes and higher vertebrates.
 FIGURE 1.2 Coral shark eye with short thick fatty eyelids. (Image used under license from Shutterstock.com.) |
Most sharks have short limited mobile flaps of skin and fatty tissue that can function as eyelids (Figure 1.2).8 Several species have a conjunctival fold forming a nictitating membrane or third eyelid, which is unusual in the eyes of fishes. The upper and lower eyelids are simple structures of skin folds containing diffuse muscle fibers forming a superficial palpebral retractor muscle and a deep palpebral depressor muscle, with the fibers of both being more or less blended.9 These palpebral muscles are derived from facial muscles and are supplied by the seventh cranial nerve.
A nictitating membrane (nictitans) is a form of protective eyelid that is found almost universally in terrestrial vertebrates as a mechanism to protect the eye from desiccation. While it is not needed in aquatic vertebrates, an analogous structure evolved from the lower eyelid is found in several families of sharks. In these sharks, the nictitans closes passively as the jaw opens during feeding, presumably to protect the eye,7 and it may be anatomically equivalent to the nictitating membrane in amphibians, birds, and mammals.7
 FIGURE 1.3 Eye in a teleost bony fish with a circumocular groove but no true eyelids. (Image used under license from Shutterstock. com.) |
The Bony Fishes
The Osteichthyes include the teleost bony or ray-finned fishes that account for the vast majority of living fish species and the lobe-finned fishes. The orbit is usually closed around the anterior rim, surrounded by circumorbital thin bones including some of the bones seen in higher vertebrates as well as a variable number of accessory bones of the head that can number more than 100 separate elements. The orbit is open posteriorly with no septum between the two sides and communicates with the nasopharynx. The orbital space is filled with loose connective tissue containing venous sinuses that cushion the globe. There are six extraocular muscles with configuration and innervation similar to sharks and higher vertebrates.10 The eye is separated from the surrounding skin by a shallow circumferential depression between the corneal epithelium and the skin (Figure 1.3). The slightly elevated outer rim of this sulcus anatomically represents a small lid fold and can be considered an early analogy of a proto-eyelid.9 In some swift-swimming species, the eye is partially covered by what has been referred to as adipose lids, horizontally opposed thin folds of skin arising from the outer lip of the circumferential sulcus and containing fatty tissue.4 Rarely they are lined by epithelium and fused over the cornea forming a closed conjunctival sac and a transparent spectacle. Some bottom-dwelling species that agitate dirt and sand also have small immobile upper “eyelid” flaps of fleshy tissue or skin that allow debris to roll off to avoid injuring the eye.8
The Eyelids and Adnexa of Amphibia
Amphibians are cold-blooded, tetrapod vertebrates that inhabit a wide variety of terrestrial, arboreal, and freshwater aquatic habitats. The earliest amphibians evolved in the Devonian Period about 350 million years ago from a group of bony lobed-finned teleostean fishes with lungs (Dipnoans). Almost all species of frogs and salamanders begin as larvae with gills, confined to water. These larvae or tadpoles lack eyelids and orbital glands. They later undergo metamorphosis into adult air-breathing forms with lungs. During early amphibian evolution, intermittent terrestrial life demanded numerous adaptations to protect the skin and the eyes. As a result, the ocular adnexa in amphibians differs very significantly from those of fishes. Complicated adaptations evolved to protect and lubricate the eye that was now exposed to air. Eyelids remain absent in those adult frog and salamander species that live their adult life in the water. In most terrestrial species, however, upper and lower eyelids develop during metamorphosis. When the eye is open, the eyelids are completely retracted (Figure 1.4). During a blink, the upper eyelid is immobile, and the longer lower eyelid does most of the job in covering the cornea (Figure 1.5). The blink is largely passive, with the eyelid closing as the globe is pulled into the orbit by specialized orbital muscles.
 FIGURE 1.4 Anuran amphibian (frog) eye wide open with retraction of the eyelids. (Image used under license from Shutterstock.com.) |
Although ancestral amphibians had a relatively closed orbit with bones similar to higher vertebrates, in modern frogs and salamanders, the orbit is much simplified, mostly membranous, and widely open with no bony separation between the two orbits or between the orbits and the nasopharynx.
The normal vertebrate pattern of six extraocular muscles and their innervations are present in amphibians, except that both the superior and inferior oblique muscles still originate close to each other in the anterior medial orbit (Figure 1.6). Two new muscles appear for the first time. The retractor bulbi muscle, innervated by the abducens nerve, is possibly derived from the lateral rectus muscle.4 It arises in the posterior orbit around the optic nerve and inserts by several fascicles onto the sclera posterior to and between the rectus muscles (Figure 1.6). Contraction of this muscle pulls the globe posteriorly into the orbit, allowing the lower eyelid
to close passively. The second muscle, the levator bulbi, is a large muscle complex with many slips derived from jaw-musculature innervated by the maxillary division of the trigeminal nerve. It separates the orbital floor from the mouth and anatomically it is analogous to the smooth orbital muscle of Müller in mammals that lies between the orbital floor and the pterygopalatine fossa (Figure 1.6). It not only can elevate the globe but may also act as an accessory respiratory muscle by changing the size of the mouth cavity.12 When the eye is pulled into the head by the retractor bulbi muscle, the levator bulbi bulges downward into the roof of the mouth and helps to propel food down the throat.13 It may also help return the lower eyelid to its opened position when the retractor bulbi relaxes.
to close passively. The second muscle, the levator bulbi, is a large muscle complex with many slips derived from jaw-musculature innervated by the maxillary division of the trigeminal nerve. It separates the orbital floor from the mouth and anatomically it is analogous to the smooth orbital muscle of Müller in mammals that lies between the orbital floor and the pterygopalatine fossa (Figure 1.6). It not only can elevate the globe but may also act as an accessory respiratory muscle by changing the size of the mouth cavity.12 When the eye is pulled into the head by the retractor bulbi muscle, the levator bulbi bulges downward into the roof of the mouth and helps to propel food down the throat.13 It may also help return the lower eyelid to its opened position when the retractor bulbi relaxes.
 FIGURE 1.5 Anuran eye with elevation of the lower eyelid and closure of the nictitating membrane. (Image used under license from Shutterstock.com.) |
The third group of amphibians, Gymnophiona (Caecilians), are limbless, fossorial, snakelike animals that have small, somewhat simplified eyes, covered with transparent skin that is not fused to the cornea. The orbit contains the usual six extraocular muscles as seen in frogs and salamanders. The retractor bulbi muscle is present; however, it does not insert onto the sclera as in other vertebrates, but onto the tentacle sac, an epithelial-lined sac homologous to the conjunctival sac, and unique to caecilians.14 A lubricating organ, the harderian gland, secretes into the tentacle, which is associated with the vomeronasal organ and serves as a chemosensory organ.15
In frogs and salamanders, a translucent conjunctival fold forms a false nictitating membrane that arises in the lower eyelid and extends upward (Figure 1.5), but it is not homologous with the horizontally oriented nictitating membrane of reptiles, birds, and mammals. It is rudimentary in salamanders but better developed in frogs and toads. In the latter group, the membrane is stiffened by a cartilaginous plate. A tissue cord from this fold extends back into the orbit around the posterior part of the globe to the retractor bulbi muscle so that when this muscle contracts and the eye is pulled into the orbit, this cord passively draws the nictitating membrane upward over the cornea. At the end of the blink cycle, the levator bulbi muscle in the floor of the orbit pushes the globe upward and forward, and the nictitating membrane returns to its normal position behind the lower eyelid.
 FIGURE 1.6 Woodcut drawing showing the anterior origins of the superior and inferior oblique, and the retrobulbar retractor bulbi muscles in the frog, seen from below. I, levator bulbi muscle; I.a, levator anguli scapulae; oi, inferior oblique; os, superior oblique; p, pterygoid muscle; r, retractor bulbi; re, lateral rectus; ri, medial rectus, ri′, inferior rectus. (Image from Ecker A, Wiedersheim R. Die anatomie des frosches; ein handbuch für physiologen, ärzte und studirende. Erste Abtheilung Knocken und Muskellehre. Braunshweig, F. Vieweg und Sohn; 1864:66.)11 |
During metamorphosis, glands develop in the upper eyelid margin and provide lubrication to the eye. Some glands on the medial side develop into the large harderian glands that nearly fill the orbit, and those on the lateral side may be a precursor of the lacrimal gland,9 but a true lacrimal gland is absent in frogs.4 A lacrimal punctum is present on the marginal border of the lower eyelid, and a subcutaneous canaliculus carries lubricating fluids to a nasolacrimal duct extending into the nasal cavity.16 In frogs, studies have suggested that secretions from the harderian gland are carried through the nasolacrimal duct to the external naris where they bind chemical stimuli that are then actively transported into the auxiliary olfactory vomeronasal sensory organ of Jacobson.17
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