PROCEEDINGS of the
23rd International Congress on Acoustics
9 to 13 September 2019 in Aachen, Germany

Why did solid otoliths evolve in the ears of modern bony fishes?
Tanja SCHULZ-MIRBACH1; Martin PLATH2; Friedrich LADICH3, Martin HEß4
1,4

Ludwig-Maximilians-University, Germany
2

Northwest A&F University, China
3

University of Vienna, Austria

ABSTRACT
Modern bony fishes (Teleostei), which comprise almost one-half of all extant vertebrate species, show aremarkable diversity in ear morphology, including otolith shape. Fish bioacousticians are still puzzling overthe question of why solid calcareous otoliths with species-specific shapes evolved, whereas most“non-teleost” vertebrates possess numerous tiny otoconia. This question is linked to when and how often aswitch from loosely aggregated material towards a solid structure—and from apatite to calcium
carbonate—occurred during the vertebrate radiation and whether those character shifts are related to alteredhearing. In a recent study, we constructed a hypothetical framework for otolith evolution by compiling theavailable information on the structure of otoliths and otoconia in > 160 species covering all major vertebrategroups. We concluded that solid teleost otoliths may have initially evolved as a selectively neutral by-productof other key innovations, and that the teleost-specific genome duplication event may have facilitated theirsubsequent diversification. Differences in otolith mass and shape might have enabled the perception ofdifferent ranges of acoustic information and may have evolved during the diversification of auditory abilities.
In some teleost groups, otolith morphology may have co-evolved with ancillary hearing structures, especially
if ears are closely connected to a gas bladder.
Keywords: otolith, otoconia, aragonite, hearing, teleost-specific genome duplication event

1. Hypothetical framework
Fossil and extant species of modern bony fishes (Teleostei) show a remarkable diversity of otolithmorphology (regarding size and shape) in their inner ears (e.g. (1, 2)). Sciaenids (drums or croakers),
for example, possess large saccular otoliths that are often characterized by pronounced humps andprotuberances whereas all otophysans, such as zebrafish, goldfish and catfishes, display a thin andneedle-shaped saccular otolith (2). In most other vertebrates, the sensory epithelia of the otolith end
organs, namely the utricle, saccule and—if present—the lagena, are overlain by numerous loosely
attached tiny otoconia (3). The questions arise of why solid calcareous otoliths with species-specificshapes evolved in teleost fishes and if this shape-diversity is correlated with (improved) hearing acrossspecies. Based on a recent compilation on data related to the morphology, number, and mineralizedmaterial of the inertial masses in vertebrate inner ears (3), we provide a brief overview of hypotheseson the origin of teleost otoliths (Fig. 1). Initially, solid otoliths may have been a by-product ofdifferences in biomineralization processes (see the evolution of cycloid scales, (4)) or of theemergence of other key innovations in teleost fishes. Hence, the initial emergence of solid otoliths inteleosts may have been selectively neutral, or solid otoliths with rather simple shapes might haveprovided a slightly positive selective advantage. They may have improved the detection of linear
accelerations and sound stimuli and were thus retained and even diversified during the subsequent
radiation of teleosts. Species-specific otolith shapes may have evolved later, closely correlated todifferent auditory demands and abilities in different species together with the diversification of swim
bladder morphology during the radiation of teleosts. Studies on the formation of otoliths and the swim
bladder walls during early larval development in zebrafish found genes like Sparc and Starmaker to1schulz-mirbach@biologie.uni-muenchen.de
mplath-zoology@gmx.de3
friedrich.ladich@univie.ac.at
4
hess@bio.lmu.de23387

play crucial roles during the development of both otoliths and the swim bladder (5, 6). In addition, in
vocal fish taxa, otolith morphology may also have co-evolved with acoustic communication because
larger otoliths were found in taxa producing sounds compared to closely related non -vocal taxa (7). In
addition, the emergence of solid otoliths might have been as well favoured due to a better surfacearea-to-volume ratio in a solid inertial mass compared to a (loose) aggregate of numerous otoconia.
Due to this improved surface area-to-volume ratio the biomineralization of otoliths might be more
“efficient” by saving energy, i.e. less organic matrix might need to be produced overall than in the caseof an otoconial mass.

Figure 1 – Overview of the characteristics of inertial masses found in vertebrate inner ears (fordetails see (3)). Fossil taxa are indicated in red. L. = Lower, U. = Upper.
All non-tetrapod vertebrates and some aquatic anuran larvae (3) display a trend towards a compact,
inertial mass overlying the sensory epithelium in the form of amorphous microotoliths(Petromyzontida) or “composite otoliths” (Sarcopterygii, some chondrichthyan species). “Composite
otoliths” are formed by fused otoconia (8, 9) whereas “true otoliths”, as found in actinopterygians,
especially teleosts, are formed by daily accreted layers of organic and inorganic material (10). Gauldie(11) proposed that solid otoliths may have been initially formed by a fusion of otoconia. Comparisonsof otoconial masses dissected from fresh and formalin-fixed ears of lungfishes and lizards, however,indicated that otoconia are rather loosely attached in fresh material whereas compact otolith-likestructures were only found in animals stored in fixative (12). Especially in lungfishes and cartilaginous
fishes, a (re-)examination of these otoconial masses is needed to evaluate their rigidity and the degreeof species-specificity of their shapes and to characterize their motion patterns relative to theunderlying sensory epithelium.
The fossil record (13) as well as crystallographic studies on extant otoliths and otoconia (14, 15)
indicated that calcareous otoliths may represent the ancestral otolith type of gnathostome fishes (13)and that three pairs of solid otoliths may have already been present in the ancestor of bony fishes(Teleostomi sensu (16)). The latter assumption might be supported by fossil Acanthodii, in which threedifferent otolith types might have already been present. The fossil record of teleosts (including
specimens with their otoliths in situ) further suggests that the overall shape of saccular otoliths was
mainly oval with a straight sulcus in Early Jurassic taxa, followed by radiations and diversification of3388

otolith shapes in the Late Cretaceous and Paleogene (17). The fossil record provides important
information on otolith evolution; however, limitations with respect to incompleteness,misinterpretations, and material re-crystallization—when the preserved material found in otoliths or
otolith-like structures does not represent the initial condition, which may even affect the overallmorphology of the otolith—have to be considered. Rather loosely attached otoconia are more prone todisintegration during taphonomic and diagenetic processes than solid otoliths. Thus, the likelihood tofind fossil specimens with otoconial masses in situ is extremely low. As a consequence, it remains
unknown what the diversity in otoconial masses or “composite otoliths” may have looked like inextinct cartilaginous and bony fishes, or in basal (Cambrian) vertebrates. Even though solid otoliths offossil taxa have a greater likelihood to be found in situ, the fossil record can be incomplete because not
all otolith types of the left and right inner ear were preserved (18). It is difficult to interpret findings ofonly one otolith or otolith pair in basic actinopterygians (19) or extinct sarcopterygians (20) and to
draw conclusions regarding the evolution of otolith numbers. In taxa that possess—or are assumed topossess—open endolymphatic ducts (such as cartilaginous fishes) and show poor preservation, while
the fossil “otoliths” lack characteristic features, the remains may simply represent post-mortem
sedimentary infillings. These infillings may indeed have been misinterpreted as fossil otoliths in situ
(21). The unambiguous identification of the original biominerals is another issue when examining
fossil specimens. The otolith-like structures detected in a Carboniferous lamprey appear to be made up
by apatite (22), which may support the idea that both fossil and extant Petromyzontida possess apatite
inertial masses in their ears. However, fossil hard tissue is prone to re-crystallization due to diagenetic
effects (23), which becomes a more severe problem the older the fossils are. To overcome theselimitations and to formulate hypotheses on otolith evolution, one needs to include a genetic (i.e.,“EvoDevo”) perspective so as to identify 1) genes/gene families that play important roles in otoconia
and otolith formation and 2) which genes might be differentially expressed in teleost or
actinopterygian inner ears during the initial stages of otolith mineralization as well as du ring later
increment formation.

2. What may have triggered the evolution of solid otoliths?
2.1 The potential role of whole genome duplication events
The high evolvability of otolith size and shape may be related to the teleost-specific whole genome
duplication event (TGD, (24)), or even the preceding vertebrate-specific whole genome duplication
event(s) (25). Both genome duplications events provided the basis for a sub- or neo-functionalizationof duplicated genes (26), probably including genes related to ear and otolith formation. Especially the
TGD may have paved the way—in the sense of a genomic exaptation (27)—for the evolution oftaxon-specific otolith shapes.
Claudin genes may represent one example for the importance of gene/genome duplications in thecontext of ear evolution. Some of these genes encode proteins that are assumed to reduce theparacellular membrane permeability to water and dissolved ions (28). Teleost-specific claudins, suchas claudin 8-like (claudin j, (29)) and claudin 7a ((28); but termed claudin 7b in (30)) are indispensable
during the early formation of the ear and otoliths. Mutations in claudin 8-like and claudin 7a result insmaller or no otoliths (29, 30). While both claudin 7a and claudin 7b are expressed in several organs inzebrafish, such as the kidney, spleen, and testes, only claudin 7a is also expressed in the brain and theeyes. It appears as if the teleost-specific duplication of claudin 7 into claudin 7a and 7b enabled a
subsequent sub-functionalization of the duplicated gene (28).
Following the TGD, otolith diversification was likely driven by different forms of natural selection
arising from the variety of habitat types that teleost fishes were able to co lonize (31), whereby some
habitats types may be imposed specific selection on improved hearing. Examples of different(eco-acoustical) environmental conditions imposing different selection on hearing capacities are, forinstance, the “cut-off frequency phenomenon” observed in shallow waters (e.g. 0.4-2 kHz at a total
water depth of 1 m (32)). Moreover, noisy versus quiet habitats (eco-acoustical constraints hypothesis(33)) have been hypothesized to select for an improved ability to detect higher frequencies in shallow
waters—as found in otophysans, such as goldfish or carp—and have triggered higher auditory
sensitivities in quiet water bodies (31). Extreme habitats, such as the deep-sea, can be characterized byhigh water pressure, which may hamper efficient sound pressure transmission to the ears through thegas-filled swim bladder, while permanent darkness renders non-visual senses (including hearing) more
important, for example, for navigation and communication (34).

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2.2 Are solid otoliths related to improved hearing and/or acoustic communication?
The “vestibular first hypothesis” (35) assumes that the vestibular sense evolved during early stagesof vertebrate evolution, followed by the evolution of the auditory sense. Otoconia are already found in
the basal bauplan of vertebrates and probably evolved first, mainly in the form of loose aggregates,
even though lampreys (Petromyzontida) already show a trend toward more solid inertial masses (36).
Hence, otoconia and “composite otoliths” may initially have served for gravity perception, similar tothe statoconia and statoliths found in many invertebrates (37). More elaborate auditory abilities
probably required derived morphological structures such as 1) tympana, audi tory ossicles, andtectorial membranes in tetrapods (38) or 2) gas-filled bladders in close proximity (or connected) to theears (which function similar to tympana), along with solid otoliths, displaying species-specific shapes
in teleosts (39). In this way, solid otoliths with daily growth patterns instead of numerous loosely
aggregated otoconia or “composite otoliths” may have enabled the evolution of improved hearing
abilities in teleosts (40). Sound detection might be improved by teleost otoliths compared to otoconia
because otoliths represent rigid bodies with a specific shape which are likely to result in mass- andshape-specific motion patterns (11, 39, 41). “Composite otoliths” either lack a uniform shape and/or
may not be rigid enough to efficiently transduce frequency-specific movement patterns to the sensory
epithelia (11, 40). Otoliths may vibrate at—and, therefore, enable perception of—higher frequencies
up to several kHz (41). It seems that frequencies above approx. 1 kHz cannot be perceived by fishes
possessing otoconia and/or “composite otoliths” (e.g. sharks and rays, see (42)). This idea receives
support from the observation that teleost species possessing ancillary auditory structures and enhanced
audition usually also display strongly divergent otolith shapes. These include te trahedral utricularotoliths in clupeiform fishes (43) or the needle-shaped saccular and star-like lagenar otoliths inotophysans (2). In addition, mathematical modelling (41) and recent experimental studies usingsynchrotron radiation-based imaging ((44), unpublished data) suggest that otolith motion patterns
strongly depend on otolith shape and the type of ancillary auditory structures (i.e. a Weberian
apparatus in otophysans versus anterior swim bladder extensions contacting the inner ears in othergroups).
Although enhanced hearing in teleosts was probably not triggered by the ability to communicate
acoustically (45), otolith morphology may have co-evolved with acoustic communication in vocal fishtaxa. Otolith size might also be evolving under constraints imposed by sound production: vocal species,
such as Nezumia aequalis (Macrouridae), appear to display larger and heavier (saccular) otoliths thannon-vocal species like Nezumia parini (46). Heavier otoliths may avoid over-stimulation of the ears
when the fish produces sound using, for example, its swim bladder (47).

3. Is the “choice” of biominerals related to otolith/otoconia function?
A better understanding of the evolution of solid, mainly aragonitic otoliths is also linked to thequestion of why different types of biominerals occur in vertebrate inertial masses. Differences in themineralized material may be related to the function of the inertial mass in inner ear physiology and/or
to metabolic and biomineralization processes.
3.1 Apatite versus calcium carbonate
A comparison of the chemical composition of otoconia and otoliths indicates a switch from apatite
in cyclostomes (hagfishes and lampreys) to calcium carbonate in gnathostomes (14, 15). The
apatite-to-calcium carbonate switch may be related to improved inner ear function. However, apatite
has a higher density (e.g. hydroxyapatite: 3.16 g cm -3 , (48)) than aragonite (2.93 g cm -3 , (10)) which
would mean a greater inertial mass per given otolith size and thus may result in improved sensitivity to
low frequency sounds (cf. (14)). From this viewpoint, an inertial mass consisting of apatite shouldhave been favoured over calcareous otoconia or otoliths in aquatic habitats. Alternatively, using
apatite for the formation of bones and teeth but calcium carbonate in the inertial masses of the ears may
have been advantageous as it allows decoupling the homeostatic control of the mineralization ofskeletal biominerals from those in the ears (49). In the ears of bony fishes, the ionic composition of theendolymphatic fluid is more strictly regulated than that of the b lood plasma (50) and decoupling ofsomatic and otolith growth rates is partly possible (51). Under stressful conditions like starvation (52)this decoupling may allow for the maintenance of continuous otolith growth—and thus, proper ear
functioning—even when somatic growth rates are reduced or come to a halt, which may be important
if the sensory epithelium also continues to grow (53).

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In contrast to earlier findings of purely calcareous endogenous otoconia/“composite otoliths” incartilaginous fishes (54), some species seem to possess apatitic inertial masses (55). If this holds true,
two hypotheses can be formulated that should be tested in future studies. 1) Calcareous inertial masses
evolved at least twice in parallel, i.e. in bony fishes (Osteichthyes) and in some cartilaginous fishes. 2)
Some cartilaginous species secondarily developed apatitic otoconia/“composite otoliths”.
3.2 Aragonite versus calcite
The switch from a predominance of aragonitic otoliths and otoconia in “fishes” to calcitic otoconia
in birds and mammals may be related to the functional role of an aragonitic inertial mass in the innerear. In aquatic habitats, the greater density of aragonite compared to calcite may be advantageous if theinertial mass acts as an accelerometer (36). Moreover, certain features related to the growth ofaragonite, namely aragonite twinning, have been hypothesized to be more suitable for the formation ofsolid otoliths, as it may facilitate a daily incremental growth pattern and ultimately, taxon-specificotolith shapes (56). The mode of thermoregulation may play an additional role because inertial masses
made up by aragonite and, in part, vaterite are found in poikilothermic vertebrates, whereas only
calcitic inertial masses are present in homoeothermic vertebrates (14). Note, however, that calcitic
otoconia also occur in cartilaginous fishes (14, 54), but these otoconia show a cuboidal crystal habit,
which is distinctly different from the barrel-shaped (cylindrical) calcitic otoconia found in tetrapods.
As some squamates possess both aragonitic and calcitic otoconia (3), it is unlikely that the mode ofthermoregulation is the only factor accounting for the predominance of calcite in mammals and birds(12). The transition from an aquatic to a terrestrial lifestyle may have been another important driver ofthis material switch. Support for this assumption may come from studies on different genes and geneproducts involved in otoconia and otolith formation. Even though similar molecular mechanisms are
involved in the formation of mouse otoconia and zebrafish otoliths and despite the fact that bothpossess homologues in their organic matrix like Sparc and Otoconin -90 (Oc90, (57)), eight genes
involved in ear development were lost in tetrapods when compared to Latimeria and zebrafish (58).
One of those genes is otolith matrix protein 1 precursor (otomp). The corresponding otolith matrix
protein 1 (OMP-1) is part of the organic matrix of zebrafish otoliths but not of the matrix ofmammalian otoconia (57) and might determine the mineralized calcium carbonate polymorph ( i.e.
aragonite). Likewise, Starmaker (Stm) is part of the zebrafish otolith matrix but is not found in mouse
otoconia (57). Stm was shown to be essential for the normal development of spherical to hemisphericalaragonitic otoliths, while silencing gene expression results in star-like, calcitic otoliths (59). An
experimental study on aragonite biomineralization focussed on the potential roles of other matrix
proteins, namely OMM-64 and otolin-1, and hypothesized that either the entire protein aggregate of
the otolith matrix induces aragonite mineralization or that the studied aggregate contained an aragonite
inducer other than OMM-64 or otolin-1 (60). Hence, OMP-1 and/or Stm might be potential candidates
that act (alone or in concert) as inducers of aragonite mineralization and were lost in tetrapods either
due to genetic drift or selection related to the transition from an aquatic to a terrestrial lifestyle(OMP-1, (58)): OMP-1 binds calcium and is important for the recruitment of other proteins into theotolith matrix (61), whereas Starmaker represents a so-called “intrinsically disordered” protein which
potentially interacts with multiple other proteins (62).

4. CONCLUSIONS
Solid teleost otoliths and especially the diversity in otolith shapes seems to be correlated with thediversification of hearing abilities. Solid, continuously growing otoliths with species-specific shapes
might have enabled the perception of different ranges of acoustic information in diverse habitats, suchas shallow versus deep or quiet versus noisy waters. However, this diversity might also have arisen as
adaptations to specific demands of the vestibular sense and the ability to manoeuver, or as a by-productof other evolutionary adaptations. The teleost-specific whole genome duplication event might haveprovided a genomic “toolbox” for the evolutionary diversification of otolith size and shape, as itallows sub- or neo-functionalization of duplicated genes.

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