Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear

The middle ear bones of Mesozoic mammals are rarely preserved as fossils and the morphology of these ossicles in the earliest mammals remains poorly known. Here, we report the stapes and incus of the euharamiyidan Arboroharamiya from the lower Upper Jurassic (～160 Ma) of northern China, which represent the earliest known mammalian middle ear ossicles. Both bones are miniscule in relation to those in non‐mammalian cynodonts. The skull length/stapedial footplate diameter ratio is estimated as 51.74 and the stapes length as the percentage of the skull length is 4%; both numbers fall into the stapes size ranges of mammals. The stapes is “rod‐like” and has a large stapedial foramen. It is unique among mammaliaforms in having a distinct posterior process that is interpreted as for insertion of the stapedius muscle and homologized to the ossified proximal (stapedial) end of the interhyal, on which the stapedius muscle attached. The incus differs from the quadrate of non‐mammalian cynodonts such as morganucodontids in having small size and a slim short process. Along with lack of the postdentary trough and Meckelian groove on the medial surface of the dentary, the ossicles suggest development of the definitive mammalian middle ear (DMME) in Arboroharamiya. Among various higher‐level phylogenetic hypotheses of mammals, the one we preferred places “haramiyidans” within Mammalia. Given this phylogeny, development of the DMME took place once in the allotherian clade containing euharamiyidans and multituberculates, probably independent to those of monotremes and therians. Thus, the DMME has evolved at least three times independently in mammals. Alternative hypothesis that placed “haramiyidans” outside of Mammalia would require independent acquisition of the DMME in multituberculates and euharamiyidans as well as parallel evolution of numerous derived similarities in the dentition, occlusion pattern, mandibles, cranium, and postcranium between the two groups and between “haramiyidans” and other mammals. J. Morphol. 279:441–457, 2018. © 2016 Wiley Periodicals, Inc.     

Auditory development in the mouse: Structural maturation of the middle ear

The development of middle-ear structures in the mouse was examined in nine groups of pups between 1 and 45 days of age. The area of the tympanic membrane (pars tensa and pars flaccida), the length of the lever arms of the malleus and incus, the surface area of the oval window, and the volume of the bulla all showed systematic changes during neonatal life. The area of the oval window reached maturity first and the lever arms achieved 90% of their adult size on day 11. The tympanic membrane achieved the same criterion on day 18. These data help us further to understand the processes that contribute to the functional ontogeny of the middle ear.     

Scaling of the marsupial middle ear and its functional significance

The marsupial middle ear performs an anatomical impedance matching for acoustic energy travelling in air to reach the cochlea. The size of the middle ear sets constraints for the frequencies transmitted. For generalized placental mammals, it has been shown that the limit for high-frequency hearing can be predicted on the basis of middle ear ossicle mass, provided that the ears fulfil requirements of isometry. We studied the interspecific size variation of the middle ear in 23 marsupial species, with the following measurable parameters: skull mass, condylobasal length, ossicular masses for malleus, incus and stapes, tympanic membrane area, oval window area, and lever arm lengths for malleus and incus. Our results show that the middle ear size grows with negative allometry in relation to body size and that the internal proportions of the marsupial middle ear are largely isometric. This resembles the situation in placental mammals and allows us to use their isometric middle ear model to predict the high-frequency hearing limit for marsupials. We found that the isometry model predicts the high-frequency hearing limit for different marsupials well, indicating that marsupials can be used as auditory models for general therian mammalian hearing. At very high frequencies, other factors, such as the inner ear, seem to constrain mammalian hearing.     

Resolving the evolution of the mammalian middle ear using Bayesian inference

Background

The minute, finely-tuned ear ossicles of mammals arose through a spectacular evolutionary transformation from their origins as a load-bearing jaw joint. This involved detachment from the postdentary trough of the mandible, and final separation from the dentary through resorption of Meckel’s cartilage. Recent parsimony analyses of modern and fossil mammals imply up to seven independent postdentary trough losses or even reversals, which is unexpected given the complexity of these transformations. Here we employ the first model-based, probabilistic analysis of the evolution of the definitive mammalian middle ear, supported by virtual 3D erosion simulations to assess for potential fossil preservation artifacts.

Results

Our results support a simple, biologically plausible scenario without reversals. The middle ear bones detach from the postdentary trough only twice among mammals, once each in the ancestors of therians and monotremes. Disappearance of Meckel’s cartilage occurred independently in numerous lineages from the Late Jurassic to the Late Cretaceous. This final separation is recapitulated during early development of extant mammals, while the earlier-occurring disappearance of a postdentary trough is not.

Conclusions

Our results therefore suggest a developmentally congruent and directional two-step scenario, in which the parallel uncoupling of the auditory and feeding systems in northern and southern hemisphere mammals underpinned further specialization in both lineages. Until ~168 Ma, all known mammals retained attached middle ear bones, yet all groups that diversified from ~163 Ma onwards had lost the postdentary trough, emphasizing the adaptive significance of this transformation.

     

Habits, functional morphology and the evolution of pycnogonids

Recent work on functional morphology has revealed not only how a wide range of animals work, but shows the significance of their shapes in great detail. Also, sound evidence of evolution is provided. A new approach towards the understanding of Pycnogonida comes from an appreciation of the significance of their general habits and shapes and from the structure and mode of action of their legs. Recent fossil evidence shows that the arachnids had at least two terrestrial landings, occurring millions of years apart in time. At least two, but probably more, separate arachnid lines lived in the sea. It is concluded that pycnogonids evolved from one such aquatic group which never became terrestrial.     

Auditory sensitivity and ecological relevance: the functional audiogram as modelled by the bat detecting moth ear

Auditory sensitivity has often been measured by identifying neural threshold in real-time (online) which can introduce bias in the audiograms that are produced. We tested this by recording auditory nerve activity of the notodontid moth Nadata gibbosa elicited by bat-like ultrasound and analysing the response offline. We compared this audiogram with a published online audiogram showing that the bias introduced can result in a difference in the audiogram shape. In the second part of our study we compared offline audiograms using spike number as threshold with others that used spike period and stimulus/spike latency, variables that have been suggested as providing behaviourally functional criteria. These comparisons reveal that functional audiograms are more flatly tuned than simple spike audiograms. The shapes of behavioural audiograms are discussed in the context of the selection pressure that maintains their shape, bat predation. Finally, we make predictions on the distance from bats at which notodontid moths use negative phonotaxis or the acoustic startle response.     

Evolution of the mammalian middle ear.

The structure and evolution of the mandible, suspensorium, and stapes of mammal-like reptiles and early mammals are examined in an attempt to determine how, why, and when in phylogeny the precursors of the mammalian tympanic bone, malleus, and incus (postdentary jaw elements and quadrate) came to function in the reception of air-borne sound. The following conclusions are reached: It is possible that at no stage in mammalian phylogeny was there a middle ear similar to that of "typical" living reptiles, with a postquadrate tympanic membrane contracted by an extrastapes. The aquamosal sulcus of cynodonts and other therapsids, usually thought to have housed a long external acoustic meatus, possibly held a depressor mandibulae muscle. In therapsids an air-filled chamber (recessus mandibularis of Westoll) extended deep to the reflected lamina and into the depression (external fossa) on the outer aspect of the angular element. A similar chamber was present in sphenacodontids but pterygoideus musculature occupied the small external fossa. The thin tissues superficial to the recessus mandibularis served as eardrum. Primitively, vibrations reached the stapes mainly via the anterior hyoid cornu, but in dicynodonts, therocephalians, and cynodants vibrations passed mainly or exclusively from mandible to quadrate to stapes and the reflected lamina was a component of the eardrum. In the therapsid phase of mammalian phylogeny, auditory adaptation was an important aspect of jaw evolution. Auditory efficiency, and sensitivity to higher sound frequencies were enhanced by diminution and loosening of the postdentary elements and quadrate, along with transference of musculature from postdentary elements to the dentary. These changes were made possible by associated modifications, including posterior expansion of the dentary. Establishment of a dentary-squamosal articulation permitted continuation of these trends, leading to the definitive mammalian condition, with no major change in auditory mechanism except that in most mammals (not monotremes) the angular, as tympanic, eventually bcame a non-vibrating structure.     

Environmental influences in the evolution of tetrapod hearing sensitivity and middle ear tuning

Vertebrates inhabit and communicate acoustically in most natural environments. We review the influence of environmental factors on the hearing sensitivity of terrestrial vertebrates, and on the anatomy and mechanics of the middle ears. Evidence suggests that both biotic and abiotic environmental factors affect the evolution of bandwidth and frequency of peak sensitivity of the hearing spectrum. Relevant abiotic factors include medium type, temperature, and noise produced by nonliving sources. Biotic factors include heterospecific, conspecific, or self-produced sounds that animals are selected to recognize, and acoustic interference by sounds that other animals generate. Within each class of tetrapods, the size of the middle ear structures correlates directly to body size and inversely to frequency of peak sensitivity. Adaptation to the underwater medium in cetaceans involved reorganization of the middle ear for novel acoustic pathways, whereas adaptation to subterranean life in several mammals resulted in hypertrophy of the middle ear ossicles to enhance their inertial mass for detection of seismic vibrations. The comparative approach has revealed a number of generalities about the effect of environmental factors on hearing performance and middle ear structure across species. The current taxonomic sampling of the major tetrapod groups is still highly unbalanced and incomplete. Future expansion of the comparative evidence should continue to reveal general patterns and novel mechanisms.     

Auditory brainstem responses to airborne sounds in the aquatic frog Xenopus laevis: correlation with middle ear characteristics

In this study we recorded auditory brainstem responses to airborne sounds to determine the hearing sensitivity of Xenopus laevis frogs and correlated their hearing profiles with middle ear characteristics. In newly metamorphosed frogs (body mass 0.5–0.76 gm, snout-vent length 17–20 mm) best hearing sensitivities were measured in the 2.4–2.8 kHz range, whereas optimal hearing sensitivity of older adults (body mass 18–90 gm; snout-vent length 57–100 mm) ranged from 1.0 to 1.2 kHz. Middle ear volumes reconstructed from serial sections showed approximate volume of 0.002 cc and 0.04–0.07 cc in newly metamorphosed and older frogs, respectively. This inverse frequency–volume relationship is consistent with the properties of an acoustic resonator indicating that differences in best hearing sensitivity are at least in part correlated to variation in middle ear volumes for airborne sounds. These results are consistent with peak frequency vibrational velocity profiles of Xenopus tympanic disk that have been shown to be dependent on underlying middle ear volumes and corroborate the occurrence of peak amplitudes of otoacoustic emissions in the 1.0–1.2 kHz region in adult Xenopus frogs.     

Using functional morphology to examine the ecology and evolution of specialization

Researchers strive to understand what makes species different,and what allows them to survive in the time and space that theydo. Many models have been advanced which encompass an arrayof ecological, evolutionary, mathematical, and logical principles.The goal has been to develop ecological theories that can, amongother things, make specific and robust predictions about howand where organisms should live and what organisms should utilize.The role of functional morphology is often an under-appreciatedparameter of these models. A more complete understanding ofhow anatomical features work to allow the organism to accomplishcertain tasks has allowed us to revisit some of these ideaswith a new perspective. We illustrate our view of this rolefor functional morphology in ecology by considering the issueof specialization: we attempt to align several definitions ofspecialization based upon shared ecological and evolutionaryprinciples, and we summarize theoretical predictions regardingwhy an organism might specialize. Kinematic studies of preycapture in several types of fishes are explored with regardto the potential ecological and evolutionary consequences ofspecialization, most notably in the area of trade-offs. We suggestthat a functional morphological perspective can increase ourunderstanding of the ecological concepts of specialization andit consequences. The kinds of data that functional morphologistscollect can help us to quantify organismal performance associatedwith specialization and the union of functional morphology withecology can help us to better understand not just how but whyorganisms interact in the manner that they do.     

Enigmatic ear stones: what we know about the functional role and evolution of fish otoliths

Otoliths in bony fishes play an important role in the senses of balance and hearing. Otolith mass and shape are, among others, likely to be decisive factors influencing otolith motion and thus ear functioning. Yet our knowledge of how exactly these factors influence otolith motion is incomplete. In addition, experimental studies directly investigating the function of otoliths in the inner ear are scarce and yield partly conflicting results. Herein, we discuss questions and hypotheses on how otolith mass and shape, and the relationship between the sensory epithelium and overlying otolith, influence otolith motion. We discuss (i) the state‐of‐the‐art knowledge regarding otolith function, (ii) gaps in knowledge that remain to be filled, and (iii) future approaches that may improve our understanding of the role of otoliths in ear functioning. We further link these functional questions to the evolution of solid teleost otoliths instead of numerous tiny otoconia as found in most other vertebrates. Until now, the selective forces and/or constraints driving the evolution of solid calcareous otoliths and their diversity in shape in teleosts are largely unknown. Based on a data set on the structure of otoliths and otoconia in more than 160 species covering the main vertebrate groups, we present a hypothetical framework for teleost otolith evolution. We suggest that the advent of solid otoliths may have initially been a selectively neutral ‘by‐product’ of other key innovations during teleost evolution. The teleost‐specific genome duplication event may have paved the way for diversification in otolith shape. Otolith shapes may have evolved along with the considerable diversity of, and improvements in, auditory abilities in teleost fishes. However, phenotypic plasticity may also play an important role in the creation of different otolith types, and different portions of the otolith may show different degrees of phenotypic plasticity. Future studies should thus adopt a phylogenetic perspective and apply comparative and methodologically integrative approaches, including fossil otoliths, when investigating otoconia/otolith evolution and their function in the inner ear.     

The importance of global parsimony and historical bias in understanding tetrapod evolution. Part I. Systematics,middle ear evolution and jaw suspension

A phylogenetic analysis based on a data matrix of 43 taxa and 155 osteological characters has produced a new hypothesis of tetrapod phylogeny that is drastically different from the established consensus. Among Paleozoic taxa, only diadectomorphs appear to be related to amniotes. In contrast to previous hypotheses, lissamphibians appear to have been derived from lepospondyls. Seymouriamorphs, gephyrostegids, embolomeres, temnospondyls, and loxommatids are stem-tetrapods. The new phylogeny suggests that the absence of a tympanic middle ear in salamanders and gymnophiones is a primitive character.     

The mechanism of the middle ear: Part II. The drum

The ear drum is considered to be a thin circular membrane with radial and circular fibers, whose center is pulled inwards by the handle of the hammer. It is shown that such a membrane is equivalent to a rigid piston connected by a lever to the handle of the hammer, and subjected to elastic forces. The stability of the equivalent system is great, and the flexibility of the lever is very small. The lever is such that small pressures in the auditory canal are transformed into larger forces on the hammer. The leverage ratio increases with the tension of the tensor tympani and decreases with the number of circular fibers.     

Variation and evolution of biomolecular systems: searching for functional relevance

The availability of genome sequences and functional genomics data from multiple species enables us to compare the composition of biomolecular systems like biochemical pathways and protein complexes between species. Here, we review small- and large-scale, "genomics-based" approaches to biomolecular systems variation. In general, caution is required when comparing the results of bioinformatics analyses of genomes or of functional genomics data between species. Limitations to the sensitivity of sequence analysis tools and the noisy nature of genomics data tend to lead to systematic overestimates of the amount of variation. Nevertheless, the results from detailed manual analyses, and of large-scale analyses that filter out systematic biases, point to a large amount of variation in the composition of biomolecular systems. Such observations challenge our understanding of the function of the systems and their individual components and can potentially facilitate the identification and functional characterization of sub-systems within a system. Mapping the inter-species variation of complex biomolecular systems on a phylogenetic species tree allows one to reconstruct their evolution.