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SENSES

GENERAL SENSES

   All living things need to obtain information about their environment.  In multicellular organisms, specialized cells called receptors can function to detect a specific type of stimulus. Although multicellular organisms such as humans possess specialized receptor cells, virtually all cells respond to signals and can, in a sense, be classified as receptors.

     Chemoreception is known in bacteria, protists, and simple animals such as cnidarians (Prosser, 1973).  The anterior end of hemichordates is sensory and may include chemical-sense receptors (Beklemishev, vol. 3, p. 136).  Mechanoreceptors, pressure receptors, thermoreceptors, and chemoreceptors are known in lancelets (Ruppert, from Harrison, 1997, p. 483; Hoar, Vol V).

Because of the essential role of water for living things, cells typically possess the ability to measure osmotic pressure. Bacterial channels for measuring osmotic pressure such as MscL and MscS are homologous to mechanosensation proteins in eukaryotes (Kung, 2005). A number of TRP channels function in animal mechanosensation (including the function of hair cells) (Kung, 2005).

Fish have many free nerve endings which function as sensory receptors (Hoar, Vol V).  Pacinian corpuscles exist in tetrapods (Ariens, p. 186).  Not only can sensory cells utilize modified cilia in vertebrates, modified cilia function in sensory perception in the scolopale of locusts and the antennae of bees (Barrington). 

     Enkalphin and opiate receptors are known in actinopterygian and sarcopterygian fish.  While fish possess both types of nociceptors found in tetrapods (the small myelinated type A fibers and the larger type C fibers), fish possess a far greater percentage of type A fibers while type C fibers are more abundant in tetrapods.  Cartilaginous fish appear to lack type C fibers (Sneldon, 2004).

Meissner corpuscles are only known in marsupials and primates. Primates increased the density of Meissner corpuscles (Dominy, 2004).

SMELL

     Humans perceive smells in an area of the nasal cavity referred to as the olfactory epithelium.  Many small olfactory nerves containing olfactory receptors from the olfactory bulb innervate this area.  These receptors are specialized neurons which possess receptor proteins in the cell membrane of their single cilium.  

     Olfactory receptors (OR) are the largest gene family in multicellular organisms and thus the largest gene family of the G-protein coupled receptors superfamily.  It is estimated that there are hundreds of these genes in the human genome (some estimate from 500 to 1000) and that olfactory receptors are capable of detecting millions of different compounds (Fuchs, 2001).  There are a number of subfamilies of OR genes, many of which have clearly arisen through interchromosomal and intrachromosomal duplications. 

     C.elegans possess about 900 chemosensory receptors which are members of families unrelated to those in vertebrates and  two additional receptor families are known in Drosophila.  As a result it seems that families of olfactory receptors have arisen independently several times (Lane, 2001).  The flagellated pit in Amphioxus may be involved in olfaction.  Although jawless fish have a single olfactory sac, this structure is bilobed in lamprey larvae and probably in the ancestral condition as well.  In jawless fish, olfactory nerves pass through the cartilaginous capsule which surrounds the olfactory sac (Weichert, 1970).  The number of olfactory receptors in tetrapods is about 10 times that found in fish (Lane, 2001). 

     Olfactory receptor genes compose about 1% of the mammalian genome with as many as 1,000 receptors.    Each olfactory neuron expresses only one allele of one gene, although maternal and paternal alleles are both expressed throughout neuron populations (Lane, 2001).  Mammals can vary considerably in the number of olfactory receptors they possess: dogs possess about 230 million olfactory receptors while humans possess only 10 million (Hohl, 2001).  In the lineage which led to higher primates and humans, a large number of these genes became nonfunctional pseudogenes.  While 70% of the olfactory receptor genes are pseudogenes in humans, only about 27% of those in Old World monkeys and virtually none of those in New World monkeys are pseudogenes.    Zebrafish and mice also possess essentially no pseudogenes (Rouquier, 2000).

 

 

THE VOMERONASAL ORGAN

     Humans possess two anatomically distinct senses of smell, although one of these (the vomeronasal system) seems to be nonfunctional.  The vomeronasal organs are located at the base of the vomer.  It receives input from the terminal (0), olfactory (I), and trigeminal nerves (V).  This olfactory organ evolved in amphibians, although some salamanders lack it (Weichert, 1970).  One gene family of receptors in goldfish olfactory epithelium is homologous to mammalian VNO genes.  It seems that VNO arose by separating different populations of receptors that previously existed in the olfactory epithelium of fish (Cao, 1998).    Although goldfish do not have an anatomically distinct vomeronasal system as in tetrapods, it appears that the medial olfactory nerve, medial olfactory bulb, and the medial olfactory tract function in pheromone detection and are homologous to the VNS of tetrapods while the lateral portions of these areas are homologous to the main olfactory system of tetrapods (Halpern, 2003).

     The VNO is well developed in reptiles and monotremes.  It is smaller but well developed in marsupials, insectivores, and rodents (Weichert, 1970).  The vomeronasal organ in rodents is involved in mating, sexual development, and male-specific aggression (Ryba, 1997).  The VNO connects to a number of parts of the limbic system which influence reproductive and aggressive behaviors.  Ablation of the VNO interferes with the ability of mammals to identify gender, species, and individuals.  Expression of VNO receptors often occurs in a sexually dimorphic pattern (Matsunami, 1997; Herrada, 1997).  Higher primates have a highly developed ability to see in color and the vomeronasal organ is reduced to the point of being potentially nonfunctional.  Birds also possess great visual acuity (and tetrachromatic vision) and also lack VNOs (Zhang, 2003).

     Instead of involving cyclic nucleotides (like G proteins), the vomeronasal system seems to involve an ion channel of the transient receptor potential family (TRP) whose members are known in fruit flies and nematodes.  (Liman, 1999).  The TRPC2 (TRP2) gene is only expressed in the VNO and is essential for function.  The only genes known to function only in the VNS are the TRP2 and VNO receptor genes (V1R and V2R families).  TRP2 and a large number of receptor genes are pseudogenes in humans and related primates.  The TRP2 gene in humans possesses both frameshift mutations and premature stop codons.  It also possesses premature stop codons in all other apes and Old World monkeys whose sequences are known.  One stop codon, in exon 13 of TRP2 seems to have been the original gene mutation which deactivated the gene and is shared by virtually all catarrhines (except orangutans where a subsequent mutation has converted TGA to CGA).  Once TRP2 became a pseudogene, the entire vomeronasal system seems to have been inactivated and there would no longer have been a selective pressure to maintain functional VNO receptors.  Statistically, the small number of VNO receptor genes which still have open reading frames in humans falls into the expected range of the number which would remain after about 35 million years of mutation.  Of the 5 remaining V1R genes in humans, V1RL5 and V1RL3 seem to be in the process of pseudogenization, given the high frequency of mutations which exist in current human populaitons.  No V2R genes exist as open reading frames in humans (Zhang, 2003; Giorgi, 2000; Rodriguez; Kouros-Mehr, 2001).

 

 

TASTE

     Humans detect taste through taste buds (which contain gustatory receptor cells) on the tongue and other regions of the oral cavity.  Worms may possess chemoreceptors in cephalic grooves.  Lancelets are not known to possess taste buds although possible gustatory hair cells exist in the head of Amphioxus.   Jawless fish possess taste buds on the surface of the head and in the pharynx (Weichert, 1970, p.716; Ariens, p. 344).  Jawless fish can perceive the salty, sour, and bitter compounds but not sweet tastes (Ariens, p. 157).  The four primary tastes of tetrapods are known in bony fish. (Hoar,VOl. IV, 1970, p. 58 ). Taste buds in some fish are located all over body, such as in carp, suckers, and catfish.  Catfish may have as many as 100,000 taste buds distributed over their body (Weichert, 1970, p.716).  Some fish have prominent vagal lobes for taste in the medulla  (Weichert, 1970, p.617).   Sarcopterygians possess taste buds only in mouth, on tongue, and in pharynx. (Weichert, 1970, p. 717)  Tetrapods possess true tongues and taste buds are found here. (Ariens, p. 345).    Mammals chew their food and possess many more taste buds on their tongue than do non-mammals (Ariens, p. 345).  Human infants possess taste buds on the fungiform papillae but they later disappear.

     Taste receptors are also G-protein coupled receptors and families of these receptors which resulted from the duplications of ancestral genes are present in the human genome.  The T1R family of taste receptors is involved in the perception of sweet tastes.  Many amino acids are perceived as sweet and stimulate receptors R1 and R3.  The T2R family of 80-120 T2 receptor genes (including pseudogenes which may represent 1/3 of these sequences) which are clustered in the genome and are responsible for human perception of bitter tastes (Adler, 2000).  Gustatory cells can express multiple receptors and, as a result, a variety of toxic compounds with different chemical structures all produce the same bitter taste.  Anthropoid primates share similar responses to taste stimuli (Hladik, 2003).

 

 

THE EAR

Hair cells of the vertebrate ear and lateral line systems are cells containing actin-filled microvilli (called sterocila) which vary in size and are organized in a row of decreasing height from a non-motile cilium, the kinocilium. Hair cell function depends on a variety of proteins which evolved prior to vertebrates such as actin, myosin, unconventional myosins, tubulin, and Wnt. Hair cells are thought to be derived from ancestral mechanoreceptors in which a cilium was surrounded by microvilli. Such mechanoreceptors are known in the simplest animals and even in the unicellular choanoflagellates, the group of protists considered the sister group of animals. The cytoskeletal organization of the vertebrate kinocilium and stereocilia is homologous to that found in invertebrate mechanoreceptors (Fritzsch, 2006).

     The mammalian inner ear is not only the site for the perception of sound, but also for balance and acceleration.  The senses of the mammalian inner ear are not unique to mammals.  The inner ear detects direction as can many organisms, even unicellulrar ones.  Geotaxis is known in protozoans, plants, a diversity of invertebrates (including higher coelomates such as mollusks and arthropods), and vertebrates (in young rats, as an example of the latter).  Different types of receptors can function in the perception of  sound: crustaceans use statocysts while insects use tympanal organs (Prosser, 1973, p. 541). 

     Invertebrates lack hair cells, although they possess homologs of the ion channels which hair cells utilize and even possess ciliate epithelial cells surrounded by a potassium rich environment (as are hair cells).  Drosophila chordotonal organs share a number of characteristics with the vertebrate inner ear including importance of TGF, FGF, Hox, zinc finger, and Pax (and possibly Iroquois Hox) genes in its development.  Hair cells and their sensory neuron connections are present in all craniates.  The horizontal semicircular canal and the importance of the gene Otx in its formation is found in all gnathostomes (Fritzch, 2001).

Although the hearing structures of invertebrates and vertebrates are not directly homologous, they utilize the same ancestral receptors and thus mutations in proteins such as Myo VII can cause deafness in both humans and flies. The development of mechanosensory cells in eumetazoan animals seems to be regulated by homologous transcription factors which evolved in ancestral diploblasts such as bHLH proteins such as Atonal, Pou factors, zinc finger proteins such as Gfi1, and homeodomain proteins such as Barhl1 (Fritzsch, 2006). Flies use genes of the TRP family (possessing ankyrin repeats) for mechanoreception. In vertebrates, lateral line organs and the kinocilia of the ear express TRP receptors (Shin, 2005). Vertebrate and tunicate hair cells are homologous; these cells function as mechanoreceptors in tunicates (Burighel, 2007; Caicci, 2007).

     Tunicate brains contain 2 sensory organs: a gravity sense organ (otolith) and an eyespot.  Genetic evidence suggests that the origins of the vertebrate ear date to the early chordates.  The Pax gene expressed in the tunicate brain (HrPax-258) is homolog of Pax 2, 5, and 8 in vertebrates.  Although sensory placodes are considered to be a characteristic of the vertebrates, tunicates do form a sensory organ from an epidermal thickening which expressed HrPax-258 and appears to be homologous to the vertebrate ear (Wada, 1998).  Lancelets lack a vestibular system, a lateral line system, and a fourth ventricle.  In jawless fish, the fourth ventricle was formed by a bulging of the sensory medulla in the area of the ear (Ariens).

     Gnathostome fish frequently possess a lateral line system in which canals in the head are lined with hair cells (neuromasts) which can possess many small stereocilia and a smaller number of large kinocilia (ranging from one to several).  Lateral line nerves, the vestibular nerve, and the cochlear nerve are all related.  They all process information from receptors which detect vibration, although the cochlear and vestibular systems are no longer exposed to the external environment (Ariens, p. 500).   In fish, the stereocilia and kinocilia of the cells in lateral line organs (neuromasts) have proven to be versatile receptors since they have been modified to sense touch, water current direction (rheoreceptors), gravity, acceleration, and sound. The rheoreceptors of the lateral line system were modified to form the receptors of the inner ear and some fish use their lateral line system to hear.  Hair cells in both vertebrates and invertebrates function in the same way to detect direction.  (Hoar, 1983, p. 236).

The inner ears of jawless are the most primitive (Weichert, 1970, p.697).  In fish, sound can be perceived in all parts of inner ear (Hoar,Vol. IV, 1970, p. 65).  All fish examined to date possess a spiracular sense organ as a component of the lateral line system.  Homologs to this structure exist in the pretympanic organ of birds, young alligators, and perhaps some mammals as well (Neeser, 2002).

      In the macula, the hair cells which detect gravity do not differ from those found in lateral line organs.  The inorganic calcium salt used to detect gravity varies from the unstable vaterite of hagfish to the aragonite of reptiles and amphibians to the calcium carbonate of mammals and birds.  Mammalian otoliths are composed of proteins (otoconins) and calcium carbonate.  The major mouse otoconin is similar to secretory phospholipase A2.  The major otoconin in Xenopus is also homologous to secretory lipase A2 (Wang, 1998).

The vestibule of the vertebrate ear functions as a gravity-sensing structure and mechanoreceptors forming gravity-sensing statocysts are known in invertebrates. It is possible that the ear began its evolution as a statocyst and additional canals were added once ancestral vertebrates became capable of rapid swimming. Hagfish possess the simplest ear in which there are three regions of sensory epithelia (one of which possesses otoconia and detects gravity) and one semicircular canal. Lampreys possess four regions of sensory epithelia, one of which may have led to the development of horizontal semicircular canals in gnathostomes. The anatomy of the horizontal canal (such as its innervation and hair cell polarity) is distinct from that of the vertical canal and evolved in ancestral gnathostomes whose mobility and lateral fins allowed enhanced swimming ability. Sarcopterygian fish developed an additional sensory area in which hair cells associated with a perilymphatic duct responded to underwater sound. This region was elaborated in amphibians and developed into the cochlea of higher vertebrates (Fritzsch, 2006).

     A vestibular apparatus is known in jawless fish; hagfish possess an otolith membrane and otoliths (Hoar, Vol V; Ariens).  In lampreys, but not hagfish, there is a distinction between the saccule and utricle  (Weichert, 1970, p.698).  The hagfish labyrinth lacks a distinct saccule.  While it doesn’t respond to vibrations, it does respond to body position and acceleration  (Prosser, 1973, p. 545).  In cartilaginous fish, sound is perceived in the saccule and utricle, which only detect acceleration in higher vertebrates (Prosser, 1973, p. 519-50).  In sharks, seawater fills the membranous labyrinth rather than endolymph and introduced sand grains perform the same function as otoliths (Weichert, 1970, p.698). 

    Bony fish can perceive sound in several parts of the inner ear: the saccule, utricle, and lagena (cochlea). Many fish use the swim bladder to amplify sound produced (Prosser, 1973; Weichert, 1970, p.701).  In fish and tetrapods, the labyrinth no longer opens to the environment (Ariens, p. 452).  In bony fish and tetrapods, vestibular stimuli are processed in the tangential nucleus and Deiters (ventrolateral vestibuluar) nucleus (Ariens, p. 455).  Vestibular fibers project to the deep cerebellar nuclei and to the nodule, uvula, lingual, and flocculus of the cerebellar cortex (Ariens, p. 487).  Bony fish possess otoliths. (Weichert, 1970, p.698).  Teleosts possess a gelatinous otolithic membrane in the saccule which supports a single otolith.  This membrane possesses a unique collage called saccular collagen (Davis, 1997).

    Tetrapods possess a distinct cochlear system and the acoustico-lateralis area becomes specialized to detect hearing and balance since the lateral line system was lost (Weichert, 1970, p.617).  Lateral line cells are present in some amphibian embryos and express the same receptors as cochlear hair cells (Shin, 2005). The membranous labyrinth is completely enclosed in bony otic capsule.  A sensory region known as the macula lagena develops in amphibians, and exists in reptiles, birds, and monotremes, although it is lost in higher mammals (Weichert, 1970, p. 699-700).  Amphibians evolved a tympanic cavity (although in many lineages it was subsequently reduced) and some evolved pharyngotympanic (Eustachian) tubes. (Weichert, 1970, p.706).  One frog possesses a tympanum at the end of a tube, similar to the situation in mammals.   In tetrapods, the middle ear can conduct sound to the inner ear through the perilymphatic duct (Weichert, 1970, p.701).  In amphibians, auditory information is processed in the nucleus magnocellularis dorsalis, an area which received lateral line fibers in fish (medial nucleus).   Amphibians lack the posterior lateral line fibers which once innervated this region (Ariens, p. 466).

     In amniotes, the cells of Mauther which functioned in ancestral vestibular reflexes are absent (Ariens, p. 501).  In most amniotes (crocodilians, birds, and mammals) the lagena and perilymphatic duct form a lengthened cochlea and organ of Corti (although the mammalian structure is distinct from those of crocodilians and birds)(Weichert, 1970, p.701).  Some lizards may also possess a tympanum which is in a depressed pocket rather than being located on the superificial portions of the head (Weichert, 1970, p.706).

 

COCHLEA

In therian mammals, the lagena and ramulus lagenae have been lost (Ariens, p. 484).  There was an increase in the size of the ventral cochlear connections in the medulla while dorsal connections decreased (Ariens, p. 497).  Mammalian embryos develop kinocilia in the organ of Corti but do not possess them as adults (Webster, 1974, p. 230).  Mammals possess an external auditory meatus and an external ear composed of elastic cartilage. The platypus lacks such an external ear but it does possess muscles which can move the opening of the ear (Weichert, 1970, p. 707).

     A number of vertebrate groups use sound waves to navigate through their environment.  All but one genus of magachiropteran bats (Rousettus) use vision as their only navigational sense; Rousettus produces clicks at night which humans can hear.  Oilbirds (Steatornis) produce clicks that humans can hear as can swifts of the genus Collocalia.  Rodents use ultrasonic communication for social interactions and some shrews (Blarina)  can use sounds to explore their environment.  Some marine mammals make use of these sounds as a sonar mechanism. (Hoar, 1983, p. 247-8; Prosser, 1973, p. 534-9).

EAR MODEL EAR MODEL
EAR MODEL

A number of mutations of the ear result in ears which resemble more primitive ancestral states. Mutations in Eya1, Gata3, and Fgf3/10 result in ears consisting only of a central gravity-sensing regions. Mutations in Pax2 and Shh form an ear with semicircular canals (although only the two vertical canals in Shh mutants) but without much development of the cochlea. Otx1 mutants also lack a horizontal semicircular canal (Fritzsch, 2006).

VISION

     Organisms evolved the ability to utilize light very early in the evolution of life and sensory mechanisms to detect light followed soon afterwards.  Bacteria, algae, protozoans, slime molds, and plants can respond to light using opsin proteins, the same proteins used to detect light in the human eye.  Opsins in archaea bind retinal, as in vertebrates, and function in phototaxis and in light-induced ion transport (Bieske, 1999).  Carotenoids, used by unicellular organisms and plants, are related to rhodopsin and these molecules change from a cis to trans orientation after being struck by light (Hoar, 1983, p. 251).  In some animals, light-sensing cells are not organized into an obvious eye: as in the detection of light by receptors along the body of an earthworm or in the 6th abdominal ganglion of crayfish (Prosser, 1973, p. 580).  In protozoans, the photosensitive molecules are associated with cilia and flagella, allowing these organisms to change the direction of movement based on the perception of light.  Some feel that the light detecting portions of photoreceptors in vertebrates and invertebrates evolved from cilia or flagella. During development, the outer segments of rods and cones develop from cilium-like structures (Hoar, 1983, p. 261-4).

     Cnidarians such as jellyfish are the simplest animals to have eyes.  Jellyfish have a receptor which is similar to vertebrate RXR (very similar to rhodopsin) which binds retinoic acid and then binds the DNA of crystallin genes, just as in both vertebrates and invertebrates (Kostrouch, 1998).

      The simplest eyes in flatworms are pigmented spots of epithelial cells.  Other flatworms possess sunken cups of cells.  In turbellarian flatworms, there are bipolar receptor cells (as in vertebrates) whose distal ends are rod-like.  These eyes cannot produce a visual image, merely distinguish between light and dark  (Barrington).

PLANARIA

PLANARIA

Annelid worms may possess eyes with ommatidia.  Simple eyes are observed in the ocelli of insects and onchyphora (Barrington). The two major types of photoreceptors, rhabdomeric and ciliary photoreceptors, each have distinct opsins, cell structures, and phototransduction cascades (Suga, 2008). Cnidarians possess photoreceptors and opsins of the ciliary type rather than the rhabdomeric type (Suga, 2008). Although they lack eyes, Hydra express opsin which functions in light detection for circadian rhythms.and light detection. They may represent an early lineage which precedes the divergence of ciliary and rhabdomeric systems (Santillo, 2005). Annelids possess both the rhabdomeric and ciliary types of photoreceptors (and can even possess a third class, phaosomous photoreceptors, which may derived from one of the other two classes). These two classes seem to represent a duplication and modification of an ancestral visual mechanisms which predates the bilaterans (Purschke, 2006). Arthropods are the only known animals which only possess rhabdomeric photoreceptors (Purschke, 2006). The brain of honey bees expresses a non-visual opsin called pteropsin. This new opsin (like one expressed in annelid brains) may represent a ciliary opsin (Velarde, 2005).

Vertebrates utilize ciliary photoreceptors for vision and rhabdomeric receptors for circadian rhythms. Lancelets possess both types of photoreceptor and molecular comparisons suggest that the vertebrate circadian receptors (ganglion cells) were originally photoreceptors similar to those of invertebrates (Koyangi, 2005). Ancestral bilaterans seem to have possessed both types of photoreceptor cell (based on ragworms Nilsson, 2005).

     Are the eyes of jellyfish, worms, and insects homologous to human eyes?  The vertebrate eye did not evolve from the compound eye of insects, and so in that sense the answer must be no.  However, there are a number of shared genetic mechanisms in both vertebrate and invertebrate eyes, indicating that the common ancestor of modern lineages possessed some sort of primitive eye in its head whose genetic mechanisms have been conserved in its descendants.  One of the first genes involved in the development of the eye is the Optx2 homeobox gene (a member of the sine-oculis-Six family) which is expressed in the eye field which forms during gastrulation.  It is expressed in both invertebrates and vertebrates in the early tissues which develop into eyes (Toy, 1998).  Sine oculis is a gene which functions downstream of Pax-6 and requires eyes absent in Drosophila .  Sine oculis is a homeobox gene in the family with Six genes which function in the development of eyes in vertebrates.   Planarians also involve sine oculis in eye development and regeneration (Pineda, 2000; Furukawa, 1997).  In addition to Pax6, other members of the Pax gene family function in the formation of eyes such as the PaxB gene of jellyfish and the Eye gone gene of Drosophila (Kozmik, 2005).  A PaxB homolog was identified in sponges, although sponges lack both eyes and nervous tissue (Kozmik, 2005).  DRx/Rx is a paired-like homeobox gene which is conserved in both protostomes such as Drosophila and vertebrates.  Inappropriate expression of Rx in frogs results in ectopic retinal tissue.  It is expressed in both fly and vertebrate brains at an early stage, before the expression of Pax-6/eyeless (Eggert, 1998). Although the box jellyfish Chironex possesses lenses capable of forming sharp images (although the lenses are only a tenth of a millimeter wide), a non-optimal distance between the lens and retina produces a blurred image (Wehner, 2005).

A number of developmental genes are shared in eye formation between protostomes and deuterostomes such as Pax-6 (eyeless), sine oculis, and eyes absent (the latter two being downstream in the cascade controlled by eyelss) (Eggert, 1998).  Tunicates express Pax genes in their eyes, as do vertebrates and fruit flies.  Ectopic expression of Pax genes can cause the formation of additional eyes (Glardon, 1997).

      Many primitive deuterostomes possess eyes.  Most chaetognaths possess eyes although some, such as those which live in caves, may lack them. (Harrison, 1997).  Among hemichordates, some enteropneust larvae have a pair of eyes (Nieuwenhuys, 2002).

   The tunicate CNS only possesses about 100 neurons including an eyespot which is composed of 3 lens cells, 1 pigment cup cell, and 20 photoreceptors.  There are 3 opsins in tunicates: Ci-opsin1 is expressed in the photoreceptors, Ci-opsin2 is expressed in a different set of brain cells and Ci-opsin3 (RGR) is expressed throughout the brain and visceral ganglion (Tsuda, 2003). The eyespot expresses the gene Ci-opsin1, a homolog of retinal and pineal opsins in vertebrates.  This median eyespot may be homologous to the pineal eye.  Although Ci-opsin1 is expressed in the developing brain at early embryonic stages, it is later restricted to the ocellus (Kusakebe, 2001).  In tunicates, three visual proteins, RGR (retinal G protein coupled receptor from which rhodopsin may have been derived), CRALBP (cellular retinaldehyde-binding protein which is important in the isomerizaiton of photopigments necessary for the perception of light), and BCO/RPE65 (required for mammalian vision) are expressed throughout the brain and visceral ganglion, indicating that the central nervous system in general participates in light detection in addition to the specialized eyespot (Tsuda, 2003). 

     Some have suggested that in lancelets, the frontal eye is homologous to vertebrate eyes, the lamellar body is homologous to the pineal gland, and motor neurons in first 2 somites are homologous to extrinsic eye muscles (Nieuwenhuys, 2002; Ruppert, from Harrison, 1997, p. 484).    

     In hagfish, optic nerves, a retina, and a lens placode form but they deteriorate. (Weichert, 1970, p.684).  .   Although modern hagfish lack eyes, fossil hagfish from the Carboniferous (Myxinikela) possessed well developed eyes (Bardack, 1991).

HAGFISH

In lampreys, the abducens nerve also supplies the inferior rectus which other vertebrates innervate with the oculomotor nerve. In lampreys and sharks, the center of the optic nerve still retains ependymal cells, which is not surprising since it was once part of the brain (and not an optic nerve)(Weichert, 1970, p.685).  

     Lamprey eyes are underdeveloped and the pineal gland is the major photosensitive organ, directing changes in sexual development, body coloration, and metamorphosis.  The pineal opsin of lampreys is homologous to that known in reptiles and birds (Yokoyama, 1997).  Opsin molecules exist in the pineal glands of birds, reptiles, bony fish, cartilaginous fish, lampreys, and amphibians.  It responds to green-blue light.  The pineal organ can be considered a folded retina (Vigh, 1998).  Zebrafish possess an exo-rhodopsin gene expressed only in the pineal gland (Asaoka, 2002).  Pinealocytes of newborn rats, unlike those of adults, resemble photoreceptors, synthesize rhodopsin, and can be responsive to light (Tosini, 2000).  Cone-like receptors exist in the lamprey pineal eye and in those of many gnathostome fish.  Endocrine cells are known in the pineal gland of bony fish (Hoar,Vol. IV, 1970, p. 27).  It may be that early mammals evolved the inhibition of pineal sensitivity as an adaptation to nocturnal life (Tosini, 2000).

          All non-mammals have photoreceptors in both their deep brains and their pineal glands, at least in embryonic development.  In halibut, the photoreceptors of the pineal gland rather than those of the retina, are capable of photoreception before hatching.  Light does enter the deep brain of vertebrates in sufficient quantity to provide information on the time of day.  Vertebrates from lampreys to birds can respond to light (with, for example, changes in circadian rhythms) when both their eyes and pineal organs are removed.  Dermal cells in some fish and amphibians can both detect light and initiate changes in pigment dispersal as a result.  Mammals are the only vertebrates (with the possible exception of neonatal mammals such as rats) which cannot respond to light without their eyes (Foster, 2002).  Mice which have no rods or cones can still detect light with their eyes which can alter circadian rhythms, induce pupil reflexes, influence pineal secretion, and affect locomotor activity Foster, 2002).  In blind subterranean mole rat, the eye is visually blind, yet it functions in circadian rhythms(Avivi, 2001).

     Sharks lack a fovea and cones (except in a few species) although there is an area centralis, similar to the macula lutea (Weichert, 1970, p.686).  All groups of gnathostomes except mammals possess twin or double cones (a pair of cone cells lying next to each other). (Prosser, 1973, p. 584).  In coelacanths, cones are rare.  Reptiles increased the number of cones in the eye compared to the amphibian condition (Weichert, 1970, p.691).  Color vision is known in turtles and lizards but does not seem to occur in other reptiles  (Weichert, 1970, p 691).  Birds have a greater visual acuity than humans, in part because their fovea lacks blood vessels in front of photoreceptors which interfere with vision.  In marsupials the conical papilla from the blind spot of reptiles exists in a reduced form; it is lost in placentals. (Weichert, 1970, p.693).  The “yellow spot” of the macula lutea where there are only cones in the center of the retina is known only in humans and some other primates (Weichert, 1970).

     Jawless fish lack a ciliary body and a corneal muscle can flatten the cornea to change the focus of the eye.  Although cartilaginous fish possess a ciliary body, it lacks muscles.  A muscle which attaches to the lens can accommodate the eye to focus on objects which are closer.  In amphibians, ciliary muscles change the position of the lens while in amniotes, ciliary muscles change the curvature of the lens (Webster, 1974, p. 211).  Reptiles are the first vertebrates to attach the lens to the ciliary body which can squeeze the lens and thus change its shape. (Weichert, 1970, p.691).  In mammals, these ciliary muscles are smooth muscles (unlike reptiles and birds in which they are striated) and thus accommodation occurs more slowly (Webster, 1974, p. 211).  The eyes of the platypus seem reptilian in their reduced ability to accommodate  (Weichert, 1970, p.693).  Small ciliary muscles exist for accommodation in marsupials. (Weichert, 1970).  The presence of ciliary muscle and the degree of accomodation varies in mammals.  Some mammals, such as some rodents, lack a ciliary muscle and are unable to perform accomodation.  The muscle is well developed in anthropoid primates, ungulates, and carnivores (with otters being extraordinary in this regard) (West, 1991),

LAMPREY EYE SHARK EYE

     Some lower vertebrates have adapted the sclera making it transparent.

A sclerotic ring (whose ring may be incomplete) of bones is known in actinopterygians, reptiles, birds, and a number of dinosaurs.   Mammals lack sclerotic rings.  The sclera can possess cartilage in a variety of vertebrates (from sharks through birds), including monotremes.  It is lost in marsupials, allowing the eye to attain a spherical shape. (Weichert, 1970).

     While the iris of amphibians and mammals contains only smooth muscle, that of crocodilians possesses both smooth and skeletal and that of birds possesses skeletal. (Weichert, 1970, p.674

     While sharks possess eyelids, they are usually immobile although some species can move the lower lid (Weichert, 1970, p.685).  Amphibians, with the new requirements of a terrestrial environment, were the first to evolve movable eyelids with moistening glands.  (Weichert, 1970, p.689).  Sebaceous glands called Harderian glands are known from all tetrapod groups including mammals, although many mammalian groups, such as primates, lack them (Weichert, 1970, p.693).  In reptiles and amphibians, lacrimal glands are in the lower eyelid and the lower eyelid has greater mobility than the upper.  Some mammals have accessory lacrimal glands in their lower eyelids. (Weichert, 1970).

    

Since monotremes and most marsupials are nocturnal, it is though that this is the ancestral mammalian condition. (Karlen, 2007). The platypus possesses a prominent nictitating membrane which is reduced in marsupials.  Most mammals have a reduced nictitating membrane which is supplied by the abducens nerve when it is present.  Nictitating membranes are known from some mammals such as aardvarks, horses, caribou, and some carnivores (such as pandas).  Other accessory visual structures unique to mammals include eyelashes, eyebrows, and an orbicularis oculi muscle of eyelids. (Weichert, 1970, p.683). 

The degree of orbital convergence increased in primates and in higher primates. Anthropoids evolved a retinal fovea, evolved larger optic nerves, more orbital convergence, and decreased the size of the cornea (Dominy, 2004).

 

EYE MODEL EYE MODEL
EYE MODEL EYE MODEL
EYE MODEL EYE MODEL
SHEEP EYE SHEEP EYE
SHEEP EYE SHEEP EYE
SHEEP EYE SHEEP EYE

PIG

PIG EYE

 

VERTEBRATE OPSIN PROTEINS

     Vertebrate responses to light involve multiple opsin molecules.  Most mammals have dichromatic vision because of short wave (blue) and long wave (red) cone pigments.  The mammalian blue pigments belong to the same subfamily as chicken violet pigments; chicken blue and goldfish blue pigments arose from separate duplications of rhodopsin (the chicken green pigment also arose from a separate duplication of rhodopsin and is not related to the green opsins of catarrhine primates).

Retinal ganglion cells utilize melanopsin to direct a variety of responses to light such as biological rhythms and pupil constriction. This represents the third photoreceptor system in the mammalian retina, in addition to those of rods and cones. While most vertebrates perform some photoreception in tissues other than the eyes (such as the brain), in mammals light detection occurs only in the retina (Hankins, 2008; Foster, 2007; Peirson, 2006).

     Melanopsin is more closely related to rhodopsin of invertebrates than other vertebrate opsins.  Human opsins belong to three separate groups: human RGR (homologous to squid retinochrome), peropsin, and the rhodopsin subgroup.  The rhodopsin subgroup includes a variety of opsins including human encephalopsin (the first to diverge from the rest of the group), VA opsin, parapinopsin (in fish), human rhodopsin, human red and green opsins (related to pinopsin in chickens), and blue opsin (related to goldfish UV opsin). 

     There are some members of the rhodopsin family which are expressed in the human brain, such as GPR21 (more specifically, the caudate and putamen).   The Retinal G-coupled Receptor, RGR,  represents one of the earliest branches from the vertebrate opsin family which would produce photoreceptors.  It is a light sensitive molecule (which converts trans-retinal to its cis conformation) expressed in the retina in cells adjacent to photoreceptor cells.

 

VERTEBRAL ANCIENT OPSIN (VA OPSIN)

     This opsin is known from the deep brains of lampreys and teleost fish, it is not yet known from tetrapods.  It is also present in retinal cells other than the photoreceptors for vision (i.e. it is present in horizontal and amacrine cells; those on the left and middle layers above).

 

PINOPSIN

     This opsin is known from the pineal glands of reptiles and birds and the deep brain of toads.  The pineal gland is photoreceptive in chickens and affects the production of melatonin.

 

EXORHODOPSIN

     This opsin evolved from the rhodopsin of teleosts and is present in the pineal glands of fish.

 

PARAPINOPSIN

     This opsin is present in the pineal gland of catfish.

 

MELANOPSIN

     This opsin is present in the deep brain, melanocytes, horizontal cells, and iris of toads.  In mice and primates (including ourselves) it is present in the ganglion and amacrine cells of the retina (layers on the left in the image below).  It is known that mammals need their eyes for circadian rhythms (“biological clocks”) but they do not need their rods and cones, the photoreceptor cells involved in vision.  The distribution of the cells which have melanopsin in the retina is similar to the distribution of cells which travel from the retina to the suprachiasmatic nuclei of the hypothalamus which controls circadian rhythms. 

RETINA

PEROPSIN

     This opsin is present in the retinal epithelia of the mouse.

 

PANOPSIN (ENCELPHALOPSIN)

     This opsin is expressed in both the retina and brain of humans.

 

RHODOPSIN

RETINA

    Rhodopsin is the pigment of rods which registers images in terms of dark and light (rather than color).  Rhodopsin works best in dim light.  It is important for the morphogenesis of photoreceptors and mutations result in retinitis pigmentosa.

 

OPSINS FOR COLOR

RETINA

     As membrane proteins, opsins are located in the cell membranes and disk membranes of photoreceptor cells.  Gene duplications on the X chromosome have produced multiple long and middle wave pigments. Red and green pigments are closely homologous, differing by about 12 amino acids.  Multiple copies of red or green pigments are more closely related to each other, having diverged more recently.  One study of two green genes indicated that they differed by only one nucleotide.  A duplication of a single ancestral red gene in the ancestors of Old World monkeys and apes produced the progenitor of the green pigment gene.  New World monkeys and nonprimate mammals possess only one red gene on the X chromosome and have dichromatic vision (although females with 2 functionally different alleles of the X linked gene could possess trichromatic vision).  Differences in the amino acids at positions 180, 230, and 285 are responsible for the differences in maximal light absorption of the red and green opsins.    The variations in the pigment proteins in the higher apes occur at sites which are not known to affect light absorption and, as a result, higher apes are thought to have equivalent color perception.

 Some marsupials have trichromatic vision (Karlen, 2007).

SHORT WAVE PIGMENTS

    The gene for the blue cone pigment is located on chromosome 7q31 and mutations in this gene, causing tritanopia, are not sex-linked.

 

 

LONG (red) AND MIDDLE (green) WAVE PIGMENTS

   These genes are located in tandem on the X chromosome.  While most people have one red opsin gene on each X chromosome, others have from two to four.  Some people have one copy of the green opsin gene but multiple copies (from two to seven) are more common.  It seems that multiple copies can be expressed, increasing an individual’s ability to make intermediate color matches.


Lampreys possess a UV-sensitive homolog of parapinopsin in their pineal gland.  Parapinopsin in the pineal glands of fish and frogs is also sensitive to UV light (Koyangi, 2004).  UV vision is present in some but not all fish, amphibians, reptiles, birds, and mammls.  It appears to have evolved at least four times: in frogs, birds, primates, and certiodactyls.  UV vision has arisen recently in the lineages of the budgerigar, zebra finch, and canary.  Most terrestrial vertebrates may have lost the ability to detect UV light as a form of protection against it.  The cornea deflects most of it (Zhang, 2003b).