Organization of deutocerebral neuropils and olfactory behavior in the centipede Scutigera coleoptrata (Linnaeus, 1758) (Myriapoda: Chilopoda)

Myriapods represent an arthropod lineage, that originating from a marine arthropod ancestor most likely conquered land independently from hexapods and crustaceans. Establishing aerial olfaction during a transition from the ocean to land requires molecules to be detected in gas phase instead of in water solution. Considering that the olfactory sense of myriapods has evolved independently from that in hexapods and crustaceans, the question arises if and how myriapods have solved the tasks of odor detection and odor information processing in air. Comparative studies between arthropod taxa that independently have established a terrestrial life style provide a powerful means of investigating the evolution of chemosensory adaptations in this environment and to understand how the arthropod nervous system evolved in response to new environmental and ecological challenges. In general, the neuroethology of myriapods and the architecture of their central nervous systems are insufficiently understood. In a set of experiments with the centipede Scutigera coleoptrata, we analyzed the central olfactory pathway with serial semi-thin sectioning combined with 3-dimensional reconstruction, antennal backfilling with neuronal tracers, and immunofluorescence combined with confocal laser-scanning microscopy. Furthermore, we conducted behavioral experiments to find out if these animals react to airborne stimuli. Our results show that the primary olfactory and mechanosensory centers are well developed in these organisms but that the shape of the olfactory neuropils in S. coleoptrata is strikingly different when compared with those of hexapods and malacostracan crustaceans. Nevertheless, the presence of distinct neuropils for chemosensory and mechanosensory qualities in S. coleoptrata, malacostracan Crustacea, and Hexapoda could indicate a common architectural principle within the Mandibulata. Furthermore, behavioral experiments indicate that S. coleoptrata is able to perceive airborne stimuli, both from live prey and from a chemical extract of the prey. These results are in line with the morphological findings concerning the well-developed olfactory centers in the deutocerebrum of this species.     

Brain architecture of the largest living land arthropod, the Giant Robber Crab Birgus latro (Crustacea, Anomura, Coenobitidae): evidence for a prominent central olfactory pathway?

Background

Several lineages within the Crustacea conquered land independently during evolution, thereby requiring physiological adaptations for a semi-terrestrial or even a fully terrestrial lifestyle. Birgus latro Linnaeus, 1767, the giant robber crab or coconut crab (Anomura, Coenobitidae), is the largest land-living arthropod and inhabits Indo-Pacific islands such as Christmas Island. B. latro has served as a model in numerous studies of physiological aspects related to the conquest of land by crustaceans. From an olfactory point of view, a transition from sea to land means that molecules need to be detected in gas phase instead of in water solution. Previous studies have provided physiological evidence that terrestrial hermit crabs (Coenobitidae) such as B. latro have a sensitive and well differentiated sense of smell. Here we analyze the brain, in particular the olfactory processing areas of B. latro, by morphological analysis followed by 3 D reconstruction and immunocytochemical studies of synaptic proteins and a neuropeptide.

Results

The primary and secondary olfactory centers dominate the brain of B. latro and together account for ca. 40% of the neuropil volume in its brain. The paired olfactory neuropils are tripartite and composed of more than 1,000 columnar olfactory glomeruli, which are radially arranged around the periphery of the olfactory neuropils. The glomeruli are innervated ca. 90,000 local interneurons and ca. 160,000 projection neurons per side. The secondary olfactory centers, the paired hemiellipsoid neuropils, are targeted by the axons of these olfactory projection neurons. The projection neuron axonal branches make contact to ca. 250.000 interneurons (per side) associated with the hemiellipsoid neuropils. The hemiellipsoid body neuropil is organized into parallel neuropil lamellae, a design that is quite unusual for decapod crustaceans. The architecture of the optic neuropils and areas associated with antenna two suggest that B. latro has visual and mechanosensory skills that are comparable to those of marine Crustacea.

Conclusions

In parallel to previous behavioral findings that B. latro has aerial olfaction, our results indicate that their central olfactory pathway is indeed most prominent. Similar findings from the closely related terrestrial hermit crab Coenobita clypeatus suggest that in Coenobitidae, olfaction is a major sensory modality processed by the brain, and that for these animals, exploring the olfactory landscape is vital for survival in their terrestrial habitat. Future studies on terrestrial members of other crustacean taxa such as Isopoda, Amphipoda, Astacida, and Brachyura will shed light on how frequently the establishment of an aerial sense of olfaction evolved in Crustacea during the transition from sea to land. Amounting to ca. 1,000,000, the numbers of interneurons that analyse the olfactory input in B. latro brains surpasses that in other terrestrial arthropods, as e.g. the honeybee Apis mellifera or the moth Manduca sexta, by two orders of magnitude suggesting that B. latro in fact is a land-living arthropod that has devoted a substantial amount of nervous tissue to the sense of smell.     

Brain organization and the origin of insects: an assessment

Within the Arthropoda, morphologies of neurons, the organization of neurons within neuropils and the occurrence of neuropils can be highly conserved and provide robust characters for phylogenetic analyses. The present paper reviews some features of insect and crustacean brains that speak against an entomostracan origin of the insects, contrary to received opinion. Neural organization in brain centres, comprising olfactory pathways, optic lobes and a central neuropil that is thought to play a cardinal role in multi-joint movement, support affinities between insects and malacostracan crustaceans.     

New insights into an ancient insect nose: the olfactory pathway of Lepismachilis y-signata (Archaeognatha: Machilidae)

Hexapods most likely derived from an aquatic ancestor, which they shared with crustaceans. During the transition from water to land, their sensory systems had to face the new physiological demands that terrestrial conditions impose. This process also concerns the sense of smell and, more specifically, detection of volatile, air-borne chemicals. In insects, olfaction plays an important role in orientation, mating choice, and food and host finding behavior. The first integration center of odor information in the insect brain is the antennal lobe, which is targeted by the afferents from olfactory sensory neurons on the antennae. Within the antennal lobe of most pterygote insects, spherical substructures called olfactory glomeruli are present. In order to gain insights into the evolution of the structure of the central olfactory pathway in insects, we analyzed a representative of the wingless Archaeognatha or jumping bristletails, using immunocytochemistry, antennal backfills and histological section series combined with 3D reconstruction. In the deutocerebrum of Lepismachilis y-signata, we found three different neuropil regions. Two of them show a glomerular organization, but these glomeruli differ in their shape from those in all other insect groups. The connection of the glomerular neuropils to higher brain centers remains unclear and mushroom bodies are absent as reported from other archaeognathan species. We discuss the evolutionary implications of these findings.     

No sight,no smell? – Brain anatomy of two amphipod crustaceans with different lifestyles

The brain anatomy of Niphargus puteanus and Orchestia cavimana, two amphipod species with different lifestyles, has been studied using a variety of recent techniques. The general aspects of the brain anatomy of both species correspond to those of other malacostracans. However, both species lack hemiellipsoid bodies. Furthermore, related to their lifestyle certain differences have been observed. The aquatic subterranean species N. puteanus lacks eye structures, the optic nerve, and the two outer optic neuropils lamina and medulla. Only partial remains of the lobula have been detected. In contrast to this, the central complex in the protocerebrum and the olfactory glomeruli in the deutocerebrum are well differentiated. The terrestrial species Orchestia cavimana shows a reduced first antenna, the absence of olfactory neuropils in the deutocerebrum, and a reduction of the olfactory globular tract. The characteristics in defining the hemiellipsoid bodies are critically discussed. Contradictions about presence or absence of this neuropil are due to different conceptualizations. A comparison with other crustaceans that live in dark environments reveal similar patterns of optic system reduction, but to different degrees following a centripetal pattern. Retaining the olfactory system seems a general problem of terrestrialization in crustaceans with the notable exception of terrestrial hermit crabs.     

Morphology of the brain in Hutchinsoniella macracantha (Cephalocarida, Crustacea)

External morphological features of Cephalocarida have long been interpreted as plesiomorphic with regard to those of other crustaceans. Based on transmission electron microscopy and light microscopy, however, the brain in the cephalocarid Hutchinsoniella macracantha has been shown to contain a number of structures that are more difficult to interpret in an evolutionary context. These include the multi-lobed complex, a unique cluster of neuropils associated with the olfactory lobes. To establish a well-founded comparison of phylogenetically relevant, neuroanatomical data from Cephalocarida to other arthropods, we investigated the brain in H. macracantha using immunolabeling (acetylated α-tubulin, serotonin, RFamide, histamine) and nuclear counter stains of whole mounts and vibratome sections analyzing specimens with confocal laser scanning microscopy and computer-aided 3D-reconstruction. Other 3D-reconstructions were based on serial 1 μm semi-thin sections. The multi-lobed complex features a pedunculus and shows detailed homologies with the mushroom bodies of certain Insecta and Lithobiomorpha (Chilopoda), suggesting that the hemiellipsoid bodies in Remipedia and Malacostraca have derived from a cephalocarid-like pattern. Like the corresponding tracts in Insecta, the olfactory globular tracts linking the multi-lobed complex to the olfactory lobes are ipsilateral, probably constituting the plesiomorphic pattern from which the decussating tracts in Remipedia and Malacostraca have evolved. The olfactory lobes in H. macracantha are uniquely organized into vertical stacks of olfactory glomeruli whose exact shape could not be identified. Similarly to Malacostraca and Insecta, the olfactory glomeruli in H. macracantha are innervated by serotonin-like, RFamide-like, and histamine-like immunoreactive interneurons. This suggests homology of the olfactory lobes across Tetraconata, despite the different morphological organization. Although H. macracantha lacks elongated, unpaired midline neuropils known from the protocerebrum of other Arthropoda, the possible rudiment of a central-body-like neuropil that receives decussating fibers from anterior somata was revealed by the serotonin-like immunoreactive pattern.     

The evolution of crustacean and insect optic lobes and the origins of chiasmata

In malacostracan crustaceans and insects three nested optic lobe neuropils are linked by two successive chiasmata that reverse and then reverse again horizontal rows of retinotopic columns. Entomostracan crustaceans possess but two retinotopic neuropils connected by uncrossed axons: a distal lamina and an inner plate-like neuropil, here termed the visual tectum that is contiguous with the protocerebrum. This account proposes an evolutionary trajectory that explains the origin of chiasmata from an ancestral taxon lacking chiasmata. A central argument employed is that the two optic lobe neuropils of entomostracans are homologous to the lamina and lobula plate of insects and malacostracans, all of which contain circuits for motion detection—an archaic attribute of visual systems. An ancestral duplication of a cell lineage originally providing the entomostracan lamina is proposed to have given rise to an outer and inner plexiform layer. It is suggested that a single evolutionary step resulted in the separation of these layers and, as a consequence, their developmental connection by a chiasma with the inner layer, the malacostracan-insect medulla, still retaining its uncrossed connections to the deep plate-like neuropil. It is postulated that duplication of cell lineages of the inner proliferation zone gave rise to a novel neuropil, the lobula. An explanation for the second chiasma is that it derives from uncrossed axons originally supplying the visual tectum that subsequently supply collaterals to the opposing surface of the newly evolved lobula. A cladistic analysis based on optic lobe anatomy of taxa possessing compound eyes supports a common ancestor of the entomostracans, malacostracan crustaceans, and insects.     

The organization of the olfactory lobes in Euphausiacea and Mysidacea (Crustacea,Malacostraca)

Summary The structural organization of the olfactory lobes in representatives of euphausiid and mysid crustaceans was investigated and compared, also with these structures described in other crustaceans and in insects. In the investigated euphasiid and mysid species, the olfactory-globular tract and the position of cell clusters associated with the olfactory lobes show a similar arrangement. This arrangement is in agreement with that described in decapod crustaceans. The olfactory lobe neuropil in representatives of both taxa shows glomerular arrangement. These glomeruli are partly enclosed in a glial wrapping, and they represent the only site where synaptic contacts are established within the olfactory lobes. This glomerular arrangement appears similar to that described in the antennal lobe of insects, but differs from the columnar arrangement described in decapod crustaceans. Furthermore, about 15–20 FMRFamide-like immunoreactive globuli cells were labeled and they occupy a similar position in the investigated species. Neurites from these cells terminate only in the olfactory lobe glomeruli, and they are therefore regarded as intrinsic interneurons. The absence of serotonin-like immunoreactivity in the olfactory lobes is a feature only ascribed to the euphausiids and mysids. A specific neuropil area is present in male mysids, and it occupy a position forward of the olfactory lobe. The male-specific neuropil in mysids and the macro-glomerular in insects complex are interpreted as analogous structures.     

SIFamide in the brain of the sphinx moth, Manduca sexta

SIFamides form a group of highly conserved neuropeptides in insects, crustaceans, and chelicerates. Beyond their biochemical commonalities, the neuroanatomical distribution of SIFamide in the insect nervous system also shows a remarkable degree of conservation. Thus, expression of SIFamide has been found to be restricted to four neurons of the pars intercerebralis in different holometabolous species. By means of immunohistological stainings, we here show that in Manduca sexta, those four cells are complemented by additional immunoreactive cells located in the vicinity of the mushroom body calyx. Immunopositive processes form arborizations throughout the brain, innervating major neuropils like the antennal lobes, the central complex, and the optic neuropils.     

The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides rowelli

This account describes the organization of the brain of the adult Euperipatoides rowelli, a member of the Onychophora or "velvet worms." The present account identifies three cerebral divisions, the first of which contains primary olfactory neuropils, visual neuropils, and brain regions that correspond anatomically to the mushroom bodies of annelids, chelicerates, myriapods, and insects. In common with the brains of many chelicerates, the onychophoran brain is supplied by many thousands of uniformly small basophilic perikarya. Other chelicerate-like features include mushroom body lobes that extend across the brain's midline, an unpaired arch-shaped midline neuropil, and visual pathways that supply midline neuropil and that of the mushroom bodies. These and other similarities with chelicerate brains are discussed in the context of arthropod evolution and with reference to recent molecular phylogenies.     

Multisensory convergence in the mushroom bodies of ants and bees

The mushroom bodies, central neuropils in the arthropod brain, are involved in learning and memory and in the control of complex behavior. In most insects, the mushroom bodies receive direct olfactory input in their calyx region. In Hymenoptera, olfactory input is layered in the calyx. In ants, several layers can be discriminated that correspond to different clusters of glomeruli in the antennal lobes, perhaps corresponding to different classes of odors. Only in Hymenoptera, the mushroom body calyx also receives direct visual input from the optic lobes. In bees, six calycal layers receive input from different classes of visual interneurons, probably representing different parts of the visual field and different visual properties. Taken together, the mushroom bodies receive distinct multisensory information in many segregated input layers.     

Serotonin immunoreactive interneurons in the brain of the Remipedia: new insights into the phylogenetic affinities of an enigmatic crustacean taxon

ABSTRACT: BACKGROUND: Remipedia, a group of homonomously segmented, cave-dwelling, eyeless arthropods have been regarded as basal crustaceans in most early morphological and taxonomic studies. However, molecular sequence information together with the discovery of a highly differentiated brain led to a reconsideration of their phylogenetic position. Various conflicting hypotheses have been proposed including the claim for a basal position of Remipedia up to a close relationship with Malacostraca or Hexapoda. To provide new morphological characters that may allow phylogenetic insights, we have analyzed the architecture of the remipede brain in more detail using immunocytochemistry (serotonin, acetylated alpha-tubulin, synapsin) combined with confocal laser-scanning microscopy and image reconstruction techniques. This approach allows for a comprehensive neuroanatomical comparison with other crustacean and hexapod taxa. RESULTS: The dominant structures of the brain are the deutocerebral olfactory neuropils, which are linked by the olfactory globular tracts to the protocerebral hemiellipsoid bodies. The olfactory globular tracts form a characteristic chiasm in the center of the brain. In Speleonectes tulumensis, each brain hemisphere contains about 120 serotonin immunoreactive neurons, which are distributed in distinct cell groups supplying fine, profusely branching neurites to 16 neuropilar domains. The olfactory neuropil comprises more than 300 spherical olfactory glomeruli arranged in sublobes. Eight serotonin immunoreactive neurons homogeneously innervate the olfactory glomeruli. In the protocerebrum, serotonin immunoreactivity revealed several structures, which, based on their position and connectivity resemble a central complex comprising a central body, a protocerebral bridge, W-, X-, Y-, Z-tracts, and lateral accessory lobes. CONCLUSIONS: The brain of Remipedia shows several plesiomorphic features shared with other Mandibulata, such as deutocerebral olfactory neuropils with a glomerular organization, innervations by serotonin immunoreactive interneurons, and connections to protocerebral neuropils. Also, we provided tentative evidence for W-, X-, Y-, Z-tracts in the remipedian central complex like in the brain of Malacostraca, and Hexapoda. Furthermore, Remipedia display several synapomorphies with Malacostraca supporting a sister group relationship between both taxa. These homologies include a chiasm of the olfactory globular tract, which connects the olfactory neuropils with the lateral protocerebrum and the presence of hemiellipsoid bodies. Even though a growing number of molecular investigations unites Remipedia and Cephalocarida, our neuroanatomical comparison does not provide support for such a sister group relationship.     

Common design in a unique midline neuropil in the brains of arthropods

Most insects possess an assemblage of midline neuropils in their protocerebrum called the central complex. Recent studies have identified comparable assemblages in the malacostracan protocerebrum. Studies of Drosophila melanogaster locomotory mutants suggest that in insects one role for the central complex might be to orchestrate limb actions. This is anecdotally supported by comparisons amongst insects suggesting that elaboration of central complex architecture correlates with complexity of limb motor repertoires. The present account describes immunocytochemical and neuroanatomical observations that reveal common design principles amongst midline neuropils in four arthropod clades, the hexapods, crustaceans, chilopods, and chelicerates and the absence of midline neuropils in diplopods. The chilopod midline neuropil, which is columnar and stratified and lacks chiasmal axons to the dorsal protocerebrum or connections to discrete satellite regions, may represent the plesiomorphous condition. The complete absence of a midline neuropil in diplopods supports previous neuroanatomical studies suggesting that the 'Myriapoda' are an artificial paraphyletic group. The columnar and layered arcuate midline neuropils of chelicerates are compared with columnar and layered midline neuropils of chilopods. No midline neuropil has been identified in a lophotrochozoan outgroup, the Polychaeta.     

The role of glomeruli in the neural representation of odours: results from optical recording studies

Odours are received by olfactory receptors, which send their axons to the first sensory neuropils, the antennal lobes (in insects) or the olfactory bulb (in vertebrates). From here, processed olfactory information is relayed to higher-order brain centres. A striking similarity in olfactory systems across animal phyla is the presence of glomeruli in this first sensory neuropil. Various experiments have shown that odours elicit a mosaic of activated glomeruli, suggesting that odour quality is coded in an 'across-glomeruli' activity code. In recent years, studies using optical recording techniques have greatly improved our understanding of the resulting 'across-glomeruli pattern', making it possible to simultaneously measure responses in several, often identifiable, glomeruli. For the honeybee Apis mellifera, a functional atlas of odour representation is being created: in this atlas, the glomeruli that are activated by different odorants are named. However, several limitations remain to be investigated. In this paper, we review what optical recording of odour-evoked glomerular activity patterns has revealed so far, and discuss the necessary next steps, with emphasis on the honeybee.     

Olfaction at depth: Cribriform plate size declines with dive depth and duration in aquatic arctoid carnivorans

It is widely accepted that obligate aquatic mammals, specifically toothed whales, rely relatively little on olfaction. There is less agreement about the importance of smell among aquatic mammals with residual ties to land, such as pinnipeds and sea otters. Field observations of marine carnivorans stress their keen use of smell while on land or pack ice. Yet, one dimension of olfactory ecology is often overlooked: while underwater, aquatic carnivorans forage “noseblind,” diving with nares closed, removed from airborne chemical cues. For this reason, we predicted marine carnivorans would have reduced olfactory anatomy relative to closely related terrestrial carnivorans. Moreover, because species that dive deeper and longer forage farther removed from surface scent cues, we predicted further reductions in their olfactory anatomy. To test these hypotheses, we looked to the cribriform plate (CP), a perforated bone in the posterior nasal chamber of mammals that serves as the only passageway for olfactory nerves crossing from the periphery to the olfactory bulb and thus covaries in size with relative olfactory innervation. Using CT scans and digital quantification, we compared CP morphology across Arctoidea, a clade at the interface of terrestrial and aquatic ecologies. We found that aquatic carnivoran species from two lineages that independently reinvaded marine environments (Pinnipedia and Mustelidae), have significantly reduced relative CP than terrestrial species. Furthermore, within these aquatic lineages, diving depth and duration were strongly correlated with CP loss, and the most extreme divers, elephant seals, displayed the greatest reductions. These observations suggest that CP reduction in carnivorans is an adaptive response to shifting selection pressures during secondary invasion of marine environments, particularly to foraging at great depths. Because the CP is fairly well preserved in the fossil record, using methods presented here to quantify CP morphology in extinct species could further clarify evolutionary patterns of olfactory loss across aquatic mammal lineages that have independently committed to life in water.     

Über die facettenaugen von land- und wasserbewohnenden crustacean

Terrestrial crustaceans have larger eyes, more ommatidia and smaller angles of ommatidial divergence than their nearest aquatic relatives. The speed of the eyes, as calculated from anatomical data, is greater in aquatic than in terrestrial Crustacea. These adaptative changes have taken place independently in different lines of Amphipoda, Isopoda, Anomura and Brachyura.     

Insect-like olfactory adaptations in the terrestrial giant robber crab

The robber crab (Birgus latro), also known as the coconut crab, is the world's largest land-living arthropod, with a weight reaching 4 kg and a length of over half a meter [1]. Apart from the marine larval stage 2, 3, this crab is fully terrestrial, and will actually drown if submerged in water [4]. A transition from sea to land raises dramatically new demands on the sensory equipment of an animal. In olfaction, the stimulus changes from hydrophilic molecules in aqueous solution to mainly hydrophobic in the gaseous phase [5]. The olfactory system of land crabs thus represents an excellent opportunity for investigating the effects of the transition from sea to land. Have land crabs come to the same solutions as other terrestrial animals, or is their olfactory sense characterized by unique innovations? Here, we show that the robber crab has evolved an olfactory sense with a high degree of resemblance to the insect system. The similarities extend to physiological, behavioral, and morphological characters. The insect nose of the robber crab is a striking example of convergent evolution and nicely illustrates how similar selection pressures result in similar adaptation     

Immunolocalisation of crustacean-SIFamide in the median brain and eyestalk neuropils of the marbled crayfish

Crustacean-SIFamide (GYRKPPFNGSIFamide) is a novel neuropeptide that was recently isolated from crayfish nervous tissue. We mapped the localisation of this peptide in the median brain and eyestalk neuropils of the marbled crayfish (Marmorkrebs), a parthenogenetic crustacean. Our experiments showed that crustacean-SIFamide is strongly expressed in all major compartments of the crayfish brain, including all three optic neuropils, the lateral protocerebrum with the hemiellipsoid body, and the medial protocerebrum with the central complex. These findings imply a role of this peptide in visual processing already at the level of the lamina but also at the level of the deeper relay stations. Immunolabelling is particularly strong in the accessory lobes and the deutocerebral olfactory lobes that receive a chemosensory input from the first antennae. Most cells of the olfactory globular tract, a projection neuron pathway that links deuto- and protocerebrum, are labelled. This pathway plays a central role in conveying tactile and olfactory stimuli to the lateral protocerebrum, where this input converges with optic information. Weak labelling is also present in the tritocerebrum that is associated with the mechanosensory second antennae. Taken together, we suggest an important role of crustacean-SIFamidergic neurons in processing high-order, multimodal input in the crayfish brain.     

Origin and occurrence of sexual and mating systems in Crustacea: A progression towards communal living and eusociality

Crustaceans are known for their unrivalled diversity of sexual systems, as well as peculiar mating associations to achieve maximum mating success and fertilization accomplishment. Although sexes are separate in most species, various types of hermaphroditism characterize these predominantly aquatic arthropods. A low operational sex ratio between female and male, together with temporally limited receptivity of females towards males, imposes restrictions on the structuring of mating systems in crustaceans. The basic mating systems consist of monogamy, polygamy, mate guarding and pure searching. Understandably, ecological influences may also play a determinative role in the evolution of such sexual and mating systems in crustaceans. An important outcome of the crustacean sexual biology is the development of complex social structures in many aquatic species, in much the same way insects have established them in terrestrial conditions. In addition, groups like isopods and certain families of brachyuran crabs have shown terrestrial adaptation, exhibiting peculiar reproductive modes, sometimes reminiscent of their terrestrial counterparts, insects. Many caridean shrimps, living in symbiotic relationship with other marine invertebrates in the coral reef habitats, have reached pinnacle of complexity in sexuality and peculiar mating behaviours, resulting in communal living and establishing advanced social systems, such as eusociality.     

Better than fish on land? Hearing across metamorphosis in salamanders

Early tetrapods faced an auditory challenge from the impedance mismatch between air and tissue in the transition from aquatic to terrestrial lifestyles during the Early Carboniferous (350 Ma). Consequently, tetrapods may have been deaf to airborne sounds for up to 100 Myr until tympanic middle ears evolved during the Triassic. The middle ear morphology of recent urodeles is similar to that of early ‘lepospondyl’ microsaur tetrapods, and experimental studies on their hearing capabilities are therefore useful to understand the evolutionary and functional drivers behind the shift from aquatic to aerial hearing in early tetrapods. Here, we combine imaging techniques with neurophysiological measurements to resolve how the change from aquatic larvae to terrestrial adult affects the ear morphology and sensory capabilities of salamanders. We show that air-induced pressure detection enhances underwater hearing sensitivity of salamanders at frequencies above 120 Hz, and that both terrestrial adults and fully aquatic juvenile salamanders can detect airborne sound. Collectively, these findings suggest that early atympanic tetrapods may have been pre-equipped to aerial hearing and are able to hear airborne sound better than fish on land. When selected for, this rudimentary hearing could have led to the evolution of tympanic middle ears.