DEVELOPMENT OF THE AUDITORY ORGAN IN

ECHOLOCATING SPECIES

G.N. Solntseva

A.N. Severtsov Institute of Problem Ecology and Evolution RAS

Leninsky Prospekt, 33, 119071 Moscow, Russia

e-mail: g-solntseva@yandex.ru

Basic features of structure and development of the peripheral auditory system in different mammalian species are common. Nevertheless, the usage of only definite acoustic characteristics of habitat by the separate groups of animals has caused the pronounced polymorphism of all parts of the auditory system beginning from the outer ear. Development of different habitats by mammals, forming of various forms of spatial orientation and communication have been accompanied by substantial morphological transformations of all units of the peripheral auditory system, especially of the phylogenetically young units, which are typical only for the mammalian class. During the adaptive radiation of biological forms, which are phylogenetically distant, but similar in habitat conditions, similar morphological features in the structure of different organs appear.

Having studied the features of structural organization of the outer, middle and inner ears in representatives of echolocating mammals in postnatal ontogenesis, we found it necessary to carry out a comparative-embryological research of all parts of the peripheral auditory system in prenatal ontogenesis (Solntseva, 1992).

The research allowed not only to study structural features of the auditory organ of investigated species in more detail, but also to find out the peculiarities of its formation linked to acoustic properties of their habitat, as well as to find an explanation of the appearance of some structural adaptations in semi-aquatic and aquatic forms, having defined a stage of formation.

The study of marine mammals' auditory organ (cetaceans), representing an absolutely specific direction of placental animals' evolution, was started more than three centuries ago. However, these works were carried out mainly at an anatomic level and had a fragmentary character (Reysenbach de Haan, 1957; Fraser, Purves, 1960; Fleischer, 1973). Besides, the research data on development of the cetaceans' auditory organ during an early pre-fetal period were completely absent (according to Schmidt's periodization, 1968), i.e. beginning with formation of an acoustic vesicle, or the stage of bud, up to the end of formation of basic anatomic structures of the auditory organ.

Great difficulties in gathering of embryonic material on marine mammals inevitably led to the fact that organs of hearing and equilibrium in a great group of mammals remained unstudied for a long time and dropped out of the general scheme of study of these organs’ development in mammals as a whole. All this prevented the solution of many questions concerning structural organization of the peripheral auditory system in various groups of mammals and did not allow for determination of the general patterns of the peripheral auditory system's development in mammals as a whole.

The most important data concerning adaptive and evolutionary changes of the auditory system could be obtained only by comparative studies of embryogenesis of the system in a wide set of species, phylogenetically close, but with different ecologies, as well as in species, phylogenetically distant, but with a similar way of life.

For the first time we carried out a comparative-embryological research of the peripheral part of the auditory system using unique embryonic collections on cetaceans, what allowed for study of structural organization of this part in more detail, to reveal the features of similarity and distinction in formation of hearing and equilibrium organs for different stages of development, and also to determine the stages of formation of structural adaptations revealed by us earlier.

On the basis of obtained results developmental patterns of the structures of the outer, middle and inner ears in representatives of echolocating mammals belonging to various ecological groups were established.

As it was known, while studying the development of various organs, including hearing and equilibrium organs, many researchers used basically a method of comparison the developing structures with the length of embryos. Such approach was not correct in comparative analysis of prenatal development of the auditory organ in a wide set of species as their terms of pregnancy and the length of embryos for similar stages of embryogenesis were sharply different. However, in experimental embryology conceptions about equivalent stages of development (Otis, Brent, 1954) were widely known.

To have an opportunity to compare rudiments of different species, a special research for normal development was undertaken on some laboratory animals by a group of scientists; as a result, the stages of development with common features for different species were marked out (Dyban et al., 1975).

With the view to carry out an adequate comparison on forming the peripheral part of the auditory system in various mammalian species, we applied a principle to compare the developing structures of the outer, middle and inner ear at similar stages of development using known tables on normal development of laboratory animals (Dyban, et al., 1975). In addition to this, the stages of structural formation of the outer, middle and inner ear were compared by us with the stages of mesenchymal tissue replacement by an embryonic cartilage.

As in majority of mammals, a similarity in a sequence of development of the structures of the outer, middle and inner ears was revealed; for the convenience of the description we used the known developmental stages of some terrestrial species (Dyban, et al., 1975).

A pair rudiment of a membranaceous labyrinth is marked at the stage of 2-3 pairs of somites (Wilson, 1914). At the stage of 6-9 pairs of somites, the membranaceous labyrinth's bud represents an acoustic placode (Kappers, 1941). Further, at the stage of 14-15 pairs of somites, an acoustic pit is formed, from which an acoustic vesicle develops at the stage of 20 pairs of somites (13th stage of development), which passes into an endolymphatic duct without any special borders. At this stage of development, an auditory ossicles’ bud in the form of mesenchyme’s thickening appears.

In all investigated species a subdivision of the acoustic vesicle into superior and anterior parts occurs at stages 14-15. Both parts are surrounded by mesenchyme. Further, a vestibular apparatus is formed from the superior part, and a formation of the cochlear canal begins from the anterior part, in which the basis, composed by a columnar epithelium, and the roof, consisting of a cuboidal epithelium, are well-distinct (stage 16). In the superior part of the acoustic vesicle, a differentiation of vestibular part into semicircular ducts and sacks is observed. In a cochlear part, only a lengthened canal is marked out: it is an endolymphatic duct, from which a cochlear will be formed later. At this stage, a subdivision of an acoustical nerve into the vestibular and cochlear branches, and their ganglions is observed .

The outer ear of a greater horseshoe bat includes an auricle (pinna) and an external auditory meatus. The pinna is noted for its huge size and, in contrast to other species of bats, lacks a tragus. The auditory meatus has a flared shape.

As well as in other terrestrial species, a development of an auricle begins at the 16th stage in the form of small prominences, located on the edge of a deepening formed due to a widening of the first branchial cleft. At the 17th stage, a fusion of these prominences takes place and an uniform mesenchymal bud of the auricle is formed. To the beginning of the 18th stage, the auricle acquires clearer contours. Further, by the end of the 19th stage, an external auditory meatus starts to fill up by the epithelium cells. This process finishes by the 21th stage of development (Solntseva, 1999 b).

In studied species, by the beginning of the 20th stage, the auditory meatus is completely filled with epithelial cells. In mature-born species, these cells are resorbed by the moment of birth, in immature-born species, the process of resorption finishes only in an early postnatal development.

To the middle ear of a greater horseshoe bat, the following features are typical: the presence of a small-sized tympanic membrane and its vertical disposition; the reduction of the auditory ossicles' size, their thinning and the presence of deep hollows in them; the malleus and incus are joined with each other at sharp angles in the area of an incudomalleal articulation; the stapes is very compact, its cruses are thickened and form a small inter-crura aperture; the long process of the malleus knits with a wall of the tympanic bone; the size of muscles of the middle ear are considerably increased. These features in the structure of the middle ear provide transmitting of ultrasound signals.

As well as in other mammals, the bud of the auditory ossicles appears at the 13th stage of development in the form of a mesenchyme's thickening. At the 16th stage, the contours of the auditory ossicles become apparent, and at the 17th stage, each bud of the auditory ossicles represents an independent formation. Their basis is formed by immature precartilaginous tissue. At the 18th stage, the elements of the auditory ossicles are formed. The basis of the auditory ossicles is formed by mature precartilaginous tissue. But, by the end of the given stage, the mature precartilaginous tissue has been already replaced by embryonic cartilage.

Tympanum is formed at the 16th stage in the form of a narrow channel located below the auditory ossicles' bud. At the 18th stage, tympanic and periotic bones are formed, and at the 19th stage, a turning of the tympanum around the sagittal and frontal axes of a body of a prefetus occurs.

Formation of the features connected with the interposition of the auditory ossicles in a tympanum occurs at the stages 18-19.

The bud of the tympanic membrane is formed at the 16th stage, and by the 17th stage, it is thick and friable. Its significant thinning is marked at the 18th stage; the tympanic membrane acquires a three-layer structure and lays almost vertically on the lateral surface of the middle ear's cavity.

The cochlea of a greater horseshoe bat is huge; it is formed by 3.5 turns. In the cochlea's structure the certain features aimed at the perception of high-frequency signals are marked. A significant development is reached by a lower, or basal, turn of the cochlea, as it is directly connected with the perception of high frequencies.

For the first time Griffin (1958) has noticed, that in bats the round window contacts with the liquid of the inner ear in a quite another place, than it does in other mammals, i.e. not at the end of the cochlea, but almost at a millimeter further than its first turn. Later on, he has revealed that the basilar membrane in bats is supplied with two additional thickenings in that part of the cochlea which is connected with the perception of the signals, having the important biological significance for these animals. The basilar membrane is narrow and thin and is very rigidly fixed between the primary and secondary osseous spiral laminas.

At the 13th stage of development, the acoustic vesicle is formed, as well as in other mammals, which on the stages 14-15 is subdivided into two parts. The vestibular apparatus is formed from the superior part, and the cochlear canal is formed from the inferior part.

At the 16th stage, the cochlear canal starts to twist spirally and the basal cochlea's turn is formed. At the 17th stage, the medial turn is formed, and at the 18th stage – the apical one and a half-turn. By the end of the 18th stage the cochlea is anatomically formed with 3.5 turns.

Further at the 19th stage, a formation of the elements of the cochlea's canal and differentiation of the cells of Corti's organ's occur, beginning from the basal turn of the cochlea and being gradually extended to the turns located above. Therefore, in all turns of the cochlea a different degree of anatomic formation of the cochlear canal and the cytodifferentiation of Corti's organ is noticed. Among the structures of the cochlear canal a Reissner’s membrane is the earliest to form, and a vascular stria is the latest (Fig. 1).

Fig. 1. The cochlea of Rhinolophus ferrumequinum’s prefetus, stages 20 – 21. 1 – cochlear canal; 2 -vestibular scala; 3 – tympanic scala; 4 – Reissner’s membrane; 5 – cochlear branch of n. acousticus; 6 – crista ampullaris; 7 – ampula of semicircular canal; 8 – axial thickening; 9 – lateral thickening; 10 - spiral ganglion

Thus, the development of the auditory organ of a greater horseshoe bat reveals a great similarity with terrestrial mammals. All structures of the outer, middle and inner ear are formed from homologous rudiments, in the certain sequence and at the similar stages of development.

Cetaceans represent one of two orders of recent mammals, who have completely adapted to aquatic way of life. However, alongside with general morphological features, typical to all representatives of the order, in each of the suborders species-specific features in the structure of organs and systems have appeared. Mysticetes have kept the olfactory analyzer and have not acquired an ability to echolocation, but odontocetes, having lost the olfactory analyzer, have got amazing opportunities for echolocation.

Well-developed hearing of odontocetes is supplemented with special organs of sound signals' generation. The combination of perfect auditory receiver with organs of the sound signals’ production has provided the odontocetes with unlimited opportunities for orientation in water environment by a reflected echo signal.

The stenella's and beluga's outer ear, as well as in other representatives of cetaceans, includes the external auditory meatus only, as the auricle is completely reduced.

At the 16th stage, from the lateral walls of the first branchial cleft the cartilaginous part of the external auditory meatus starts to develop in the form of a short and slightly bent tube opened along the whole extent. The osseous part of the auditory meatus is forming later. Filling of the cartilaginous part of the auditory meatus with epithelial cells occurs at the 19th stage, and its total closing by these cells comes to an end by the 21st stage of development (Solntseva, 1983, 1999 a).

At the 19th stage, the formation of the species-specific features of the outer ear in the form of a noticeable narrowing of the auditory meatus in its distal part is marked. Further, the auditory meatus lengthens and acquires a double bend shape, typical for definitive forms. To the 20th stage, the auditory meatus widens in the proximal part. At the later stages, the increase in the absolute size of the auditory meatus, which is carried out proportionally to the growth of a prefetus, is marked.

For the first time, we have found out the source of the epithelioid obliteration in the distal part of the auditory meatus of some dolphins and a white whale (Solntseva, 1992, 1999 a). In odontocetes, the structure of the auditory meatus differs from such of all investigated species of mammals. Only in odontocetes, the auditory meatus has a strongly pronounced S-shaped form. At some distance from the lumen, the cavity of the auditory meatus obliterates, as a result, its two parts are formed, distal and proximal ones. As we have already mentioned, at the 20 stage, the auditory meatus is already completely filled with epithelial cells, which in immature-born species are resorbed completely in the early postnatal ontogenesis only, and in mature-born - by the moment of birth. In mature-born odontocetes, the complete resorption of epithelial cells occurs in the proximal part of the auditory meatus only, while in the distal part, a piece of the embryonic epithelial obliteration is left, not being exposed to a resorption, and later the epithelial tissue of adult forms, which has been found out by us earlier, is formed upon its basis (Solntseva, 1971).

All elements of the middle ear develop from mesenchymal and mesodermal elements. In a spotted dolphin and in a white whale, as well as in other species of mammals, the bud of the auditory ossicles appears at the 13th stage in the form of a mesenchymal condensation. At the 14-15th stages, the contours of the auditory ossicles’ buds are visible, but their form is not similar to that they will adopt at the later stages of development. Junction between the auditory ossicles is continuous. The differentiation of the auditory ossicles into the elements, forming them, is absent. In the mesenchyme, from which the buds of the auditory ossicles consist, large nuclei, occupying the most part of a cell, are found.

In the bud at the 16th stage, the contours of the auditory ossicles are revealed and the process of the tympanum’s formation starts. The buds of the auditory ossicles slowly plunge into the depth of the tympanum. The basis of the auditory ossicles is formed by a mature precartilaginous tissue, the cells of which acquire more distinct outlines. At the given stage, the process of differentiation of the precartilaginous tissue to the embryonic hyaline cartilage begins. The process of cartilaginification begins in the center of each bud of the auditory ossicles and spreads gradually to their periphery. Around the chondrocytes the pericellular substance is located. Cells’ nuclei are large and surrounded by a narrow band of cytoplasm and are located at a distance from each other. The auditory ossicles are surrounded by a perichondrium, which consists of small flat cells, whose chondroblasts have no distinct borders. Due to the perichondrium the areas of the auditory ossicles junctures are clearly visible. At the given stage of development, the differentiation of the tympanic membrane-ligament, stapedius and tympanic muscles starts. The tympanum is represented by a narrow blind canal located below the buds of the auditory ossicles.

At the 17-18th stages of development, there is a formation of tympanic and periotic bones. At the 19th stage, the tympanum's turning around the sagittal and frontal axes of a body of an animal occurs. The location of the auditory ossicles in the tympanum is similar to definitive forms, i.e. the malleus and incus are connected with each other at right angles.

At the 18th stage, the formation of structural elements of the auditory ossicles is marked. The auditory ossicles are increased in size. In the malleus, a head, a neck and a handle are well-expressed. In the incus, a body and both processes are formed. In the stapes, there is no differentiation into cruses; therefore the stapes acquires the form of a smoothed cone. The basis of the auditory ossicles is formed by a mature precartilaginous tissue. Further, the replacement of the mature precartilaginous tissue by the embryonic hyaline cartilage occurs. The process of cartilaginification of the auditory ossicles starts in the center of each bud and spreads gradually to their periphery.

The formation of the features connected with interposition of the auditory ossicles in the tympanum of a spotted dolphin and a white whale is marked at the 16th stage of development, whereas in the majority of the species, which don't possess abilities for echolocation, it occurs on the 18-19th stages of development.

The tympanic membrane is formed in the place of the contact of the entoderm of a pharyngeal recess and the ectoderm of the first branchial cleft. The bud of the tympanic membrane appears at the 16th stage and to the 17th stage it is thick and friable. At the 18th stage, the tympanic membrane becomes considerably thinner, acquires a three-layer structure and is located almost horizontally on the lateral surface of the middle ear's cavity. The ligament, connecting the tympanic membrane with the handle of the malleus, is formed. In odontocetes and mysticetes the tympanic membranes reveal similarity in structure at similar stages of development, whereas during the fetal period they adopt species-specific features.

The formation of a cavernous plexus is marked at the 18-19th stages. The development of the venous and peribullar sinuses occurs a little bit later, beginning from the 21st stage of development. The replacement of the cartilaginous tissue by the osseous tissue is marked at the 20th stage in the form of separate centers of ossification in the integumentary bones of a cranium, tympanic and periotic bones. The initial ossification of the auditory ossicles is marked at the 21st stage. The process of formation of the ear muscles and a ring-shaped ligament of the stapes has ended. The aural capsule is formed by a slightly differentiated cartilage.

In the inner ear at the 13th stage, the acoustic vesicle develops; its subdivision into superior and inferior parts occurs at the 15th stage like in other mammals. The vestibular apparatus is formed out of the superior part, and from inferior part the cochlear canal is formed.

At the 16th stage, the cochlear canal starts to twist spirally, forming a lower, or a basal turn of the cochlea, which is surrounded by the aural capsule consisting of a compact mesenchyme. Cellular elements of Corti's organ are approximately on identical stage of differentiation.

At the 17th stage, the next turn of the cochlea is formed. The process of formation of turns is accompanied by the formation of a cochlear nerve (n. cochlearis). The dorso-medial part of this nerve goes to the apical turn, and its ventro-lateral one - to the basal turn, the size of which considerably surpasses those of the turn located above.

At the 18th stage, the cartilaginification of an aural capsule begins. The cochlea is formed by 2.0 turns. The beginning of the cellular differentiation of Corti's organ is marked. At this stage, the columnar epithelium of the cochlear canal moves apart, therefore two thickenings are formed: an axial and a lateral, from which the elements of the cochlear canal and Corti's organ are formed. Nuclei of the cells of the future Corti's organ are large, have an oval form and include numerous nucleoli. Cells have not formed a typical mosaic in their location yet. Their cytoplasm is light and hardly visible. The structure and location of these cells enable to suppose, that further the outer hair cells will be formed from them. Under these cells the cells with large nuclei including nucleoli are located. Most likely, it is Deuter's cells; under them the cells with small pyknotic nuclei are located. The cytoplasm of these cells is light and forms a narrow band. These are epithelial cells under which the basilar membrane is located. The Hensen's and Claudius's cells are presented by a cuboidal epithelium located in 1-2 rows. The Reissner’s membrane is formed. The formation of a cavernous plexus is marked (Fig. 2).

Fig. 2. Histotopography of the peripheral auditory system in dorsoventral head sections in Stenella attenuata’s prefetus, stages 18-19. 1 – cochlear canal; 2 – vestibular apparatus; 3 –cochlear branch of n. acousticus; 4 – vestibular branch of n. acousticus; 5 – n. acousticus; 6 – tympanum; 7 – malleus; 8 – incus; 9 – m. stapedius; 10 - cavernous plexus; 11 – cerebrum.

At the 19th stage, the supporting cells, as well as the receptor cells of Corti’s organ, are involved in the process of differentiation. Cells are located in the order, forming 3 rows. The nuclei of the cells have a roundish and an oval form. The outlines of the cells are clearly visible. The neurons of the spiral ganglion are large and densely adjoin each other, forming characteristic clusters. The formed modiolus is penetrated by numerous blood vessels.

At the 20th stage, the formation of the supporting elements of Corti's organ (outer cells-columns) continues. These cells have a thin bent body with a nucleus located in the basal part of a cell. Cells of a cylindrical form with a roundish basis are differentiated simultaneously. These are the internal hair cells. Cells of the precartilaginous tissue acquire more distinct borders, and in the central sites they increase in size. The quantity of the intercellular substance grows. The cochlea is increased. In the cochlear canal the differentiation of a spiral limb, a vascular stria and a spiral incisure began. The spiral limb is represented by the cells of an extended form. The vascular stria is formed by the undifferentiated epithelium. The future spiral incisure consists of a multi-row high columnar epithelium including transparent nuclei of an oval and roundish form. The nucleus includes one nucleolus which is centrally located. The outlines of the cells are hardly visible. The basal membrane, on which the cells of Corti's organ are located, consists of a connective tissue. The tunnel is not formed yet. The sizes of the neurons of the spiral ganglion are increased and nerve fibres are clearly visible. Their nuclei are large, have a roundish form and are eccentrically located.

At the 21st stage, the connection of the tympanic membrane-ligament with the handle of the malleus is clearly visible. The process of formation of ear muscles and a ring-shaped ligament of the stapes has finished. The aural capsule is formed by a slightly differentiated cartilage. In comparison with the previous stage, the cochlea acquires much bigger sizes. The basic process of the cellular differentiation of Corti's organ has ended. In the cartilage there is an extension of the intercellular substance and the capsules of the cartilaginous cells are clearly visible. The process of formation of the isogenic groups of chondrocytes occurs. In the cochlear canal the process of formation of the tunnel begins. The cells of the spiral ganglion are located more rarefiedly.

In the white whale’s embryo of the length of 250 mm the auditory ossicles are connected at right angles in the area of the incudomalleal joint. In the malleus the centers of ossification have appeared. The tympanic membrane is thick; it is connected with the handle of the malleus with the help of a ligament. The long process of the malleus knits with the wall of tympanic bone. The structures of the cochlear canal are basically formed. The tympanic and vestibular scalae, the cochlear canal, the Reissner’s membrane and the spiral ligament are distinctly visible; the differentiation of the cells of Corti's organ's continues.

In the process of embryogenesis of the peripheral part of the stenella's and beluga's acoustic analyzer the morphological differentiation and maturation of the structures of the outer, middle and inner ear occurs in the same sequence, as in echolocating bats (Solntseva, 1983, 1999 a).

Thus, in the early embryogenesis of echolocating species the original features of the auditory organ's formation are found, which are connected with the way of life as well as with the perception of frequencies of a wide range. Adaptive features in the structure of the auditory organ are revealed at different stages of embryogenesis, even at the earliest, in spite of the fact, that the development in the mother’s womb occurs without direct influence of the environmental conditions.

The results of comparative study of the peripheral auditory system's development in representatives of echolocating species shown that formation of their structures of the outer, middle and inner ear in the early prefetal period occurs at a similar sequence and approximately at the similar stages of development. The greatest similarity in the formation of the peripheral auditory system of mammals is marked in the first half of the early prefetal period. Species-specific features in the structural organization of the auditory organ are formed in the second half of the early prefetal period, depending on an ecological specialization of species. The process of cellular differentiation of Corti's organ and resorption of epithelial cells of the auditory meatus in the mature-born animals (cetaceans) finishes, basically, by a moment of their birth (Solntseva, 2007).

In the immature-born species (bats), the differentiation of elements of the cochlear canal, cells of Corti's organ, and also the resorption of the epithelium of the auditory meatus comes to the end only by the 25-30th days (Airapetyantz, Konstantinov, 1974), since a part of their fetal period is completed only after the birth.

In echolocating forms (bats, dolphins), belonging to different taxonomic and ecological groups, the development of middle and inner ears acquired general properties due to the parallel evolution during which the development of traits for their intraspecific acoustic communication have been created in conditions, adverse for vision, and in connection with specific properties of the environment as a chanal of acoustic communication.

On the basis of results obtained, the following general regularities of the peripheral auditory system’s development in representatives of different ecological groups have been determined:

1. In first half of an early prefetal period (stages 13-16), the peripheral auditory system has common features in structure in most of mammals;

2. Species-specific features in the structural organization of the peripheral auditory system are formed in the second half of an early prefetal period (stages 18-20), depending on an ecological specialization of species;

3. The morphological features of the mammalian peripheral auditory system, which were formed in the early prefetal period, continue to develop in the late prefetal, fetal periods, and during an early postnatal ontogenesis.

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