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Left bony labyrinth of Canis lupus (Grey wolf). (a) lateral view, (b) dorsal view. ASC, anterior semicircular canal; ASCh, height of the anterior semicircular canal; ASCw, width of the anterior semicircular canal; Cc, crus commune; Co, cochlea; ed, endolymphatic duct; LSC, lateral semicircular canal; LSCh, height of the lateral semicircular canal; LSCw, width of the lateral semicircular canal; oW, oval window; pd, perilymphatic duct; PSC, posterior semicircular canal; PSCd; diameter of the posterior semicircular canal; rW, round window; sCc, secondary crus commune. Scale 1 mm.
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Abstract Carnivorans are a highly diverse and successful group of mammals, found on the top of the food chain. They originated in the Palaeocene (ca. 60 Ma) and have developed numerous lifestyles, locomotion modes and hunting strategies during their evolutionary history. Mechanosensory organs, such as the inner ear (which houses senses of equilibri...
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... second principal component (PC2) correlates positively with the width and diameter of the ASC; the length and diameter of the PSC and LSC; the length of the Cc; the height, width and length of the Co and the angles LSC/PSC and LSC/Co, but correlates neg- atively with the height, length and radius of the ASC; the height, width and radius of the PSC and LSC and the angles ASC/PSC and ASC/LSC. The third principal component (PC3) correlates positively with the width and length of the ASC; the height and length of the PSC; the width, radius and length of the LSC; the length of the Cc; the height of the Co and all measured angles (ASC/PSC, ASC/LSC, LSC/PSC, LSC/Co), but correlates nega- tively with the height, diameter and radius of the ASC; the height, diameter and radius of the PSC; the height and diameter of the LSC and the width and length of the Co.A detailed list of the PCA scores is found in the electronic supplementary material (Supplementary Dataset 1). ...
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... were visualised, bony labyrinths were segmented manually and virtually reconstructed three dimensionally using the software Amira 5.4.5 (Visualization Sciences Group). For comparison of morphological traits, only left labyrinths were reconstructed. Measurements were taken directly on the 3D labyrinths following the protocol of previous studies (Fig. 1) 19,26,28,44,52 . All measurements were scaled in millimetre related to the voxel (three-dimensional pixel) size. A detailed list of the 3D measurements is found in the electronic supplementary material (Supplementary Dataset ...
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... measurements were scaled in millimetre related to the voxel (three-dimensional pixel) size. A detailed list of the 3D measurements is found in the electronic supplementary material (Supplementary Dataset 1). ...
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... analyses are based on the carnivoran supertree 3 . A detailed list of the calculated phylogenetic values is found in the electronic supplemen- tary material (Supplementary Dataset 1). The anatomical variance of the semicircular canals of the bony labyrinth was calculated for all specimens of the species Vulpes vulpes and additionally for all specimens of the genus Canis using the 'coefficient of variabil- ity' 63 (Supplementary Data 4). ...
Citations
... One goal is to understand the lifestyles of extinct taxa by comparing their skeletal morphology with their modern relatives, which can provide insights into the evolution of species and how they have adapted to their environments over time (e.g. [7,8]). Ecomorphological studies can also clarify the relationships between form, function, and environment, shed light on the mechanisms of evolution and adaptation, and inform conservation efforts (e.g. ...
... The size and morphology of the soft tissue is thought to be mirrored by its bony cavity and hence can be used to compare fossils with their extant relatives to draw inferences about their ecomorphological adaptations (e.g. [8,[50][51][52]). The inner ear labyrinth can be divided into two systems. ...
... In mustelids (weasels, otters and kin), both the vestibular system and the cochlea are associated with ecology, providing a strong signal for semiaquatic lifestyle, as well as for terrestrial, semi-arboreal, arboreal and semi-fossorial [53]. The bony labyrinth of Canidae and Feloidea varies based on their hunting strategies (pursuit, pounce, ambush and occasional) [8], with species using faster modes of locomotion (e.g. wolf, leopards) showing larger semicircular canals compared to slower taxa. ...
Carnivores (cats, dogs and kin) are a diverse group of mammals that inhabit a remarkable range of ecological niches. While the relationship between ecology and morphology has long been of interest in carnivorans, the application of quantitative techniques has resulted in a recent explosion of work in the field. Therefore, they provide a case study of how quantitative techniques, such as geometric morphometrics (GMM), have impacted our ability to tease apart complex ecological signals from skeletal anatomy, and the implications for our understanding of the relationships between form, function and ecological specialization. This review provides a synthesis of current research on carnivoran ecomorphology, with the goal of illustrating the complex interaction between ecology and morphology in the skeleton. We explore the ecomorphological diversity across major carnivoran lineages and anatomical systems. We examine cranial elements (skull, sensory systems) and postcranial elements (limbs, vertebral column) to reveal mosaic patterns of adaptation related to feeding and hunting strategies, locomotion and habitat preference. We highlight the crucial role that new approaches have played in advancing our understanding of carnivoran ecomorphology, while addressing challenges that remain in the field, such as ecological classifications, form–function relationships and multi-element analysis, offering new avenues for future research.
... Petrosal bones often survive fossilization due to their high density and, as such, they represent a crucial source of information for paleontological studies. Microtomography-assisted analysis of the inner ear, which is used as an equivalent term to the endocast of the bony labyrinth in this study, has proven to be of value for inferring phylogenetic affinities and ecological correlates in a number of mammalian groups such as primates (e.g., Spoor et al. 2007;Lebrun et al. 2010;Benoit et al. 2013;Ekdale 2013;Perier et al. 2016;del Río et al. 2021), artiodactyls Costeur 2014;Mennecart and Costeur 2016), cetaceans (e.g., Geisler and Luo 1996;Ekdale 2013Ekdale , 2016Mourlam and Orliac 2017), xenarthrans (e.g., Billet et al. 2012Billet et al. , 2015aBoscaini et al. 2018), carnivorans (e.g., Ekdale 2013Grohé et al. 2016;Schwab et al. 2019), marsupials (Alloing-Séguier et al. 2013, and rodents (Ekdale 2013;Arnaudo et al. 2020). With reference to the latter, Ekdale (2013) has demonstrated that caviomorph cochleas are notably elongated in comparison to those of other mammals. ...
With their past and current diversities, West Indian caviomorph rodents dominate the terrestrial mammalian fauna of the Caribbean archipelago. Many of these species have recently become extinct, including the emblematic giant forms known as Heptaxodontidae. The higher-level systematics and content of this family have been widely disputed over the last decades (i.e., membership in Cavioidea vs. Chinchilloidea vs. Octodontoidea). Here we analyzed the phylogenetic signal provided by several characters of the caviomorph inner ear to adress the phylogenetic affinities of the West Indian heptaxodontids. For this, we assembled an exhaustive taxonomic sampling (N = 100) of extant North and South American caviomorphs (including representatives of all families) and a wide array of West Indian forms among octodontoid echimyids (extant and extinct capromyines, as well as extinct heteropsomyines), and some heptaxodontid subfossil taxa such as Amblyrhiza, Clidomys, and Elasmodontomys. Geometric morphometrics and comparative phylogenetic methods were employed to explore shape differences of the inner ear and their potential systematic implications. Our results show that: (1) allometry is a major contributor to shape variation in the bony labyrinth; (2) shape variation bears a strong phylogenetic signal, providing diagnostic characters for Caviidae and Erethizontoidea; and (3) Amblyrhiza and Clidomys are morphologically closer to Chinchilloidea with which they have potential phylogenetic affinities. Elasmodontomys remains a problematic taxon as it exhibits inner ear features that are consistent with either Chinchilloidea or Octodontoidea, depending on how the allometric component is evaluated.
... Size and shape of the bony labyrinth (the bony wall surrounding the inner ear) differs considerably across mammalian lineages, which is assumed to reflect evolutionary adaptations to different locomotor behaviours, postures, and hearing capacities in mammals (e.g., Billet et al. 2013, Crumpton et al. 2015Pfaff et al. 2015, Ekdale 2016, Grohe5 et al. 2016, Schwab et al. 2019, Benoit et al. 2020. For example, the semicircular canals, important for balance and posture control, are strongly reduced in size in cetaceans, which has been linked to their aquatic lifestyle (Spoor et al. 2002, Ekdale 2013. ...
... An extended secondary bony lamina of the cochlea is associated with ultrasonic hearing in cetaceans (Mourlam & Orliac 2017, Costeur et al 2018, Park et al 2019. Apart from these strong functional signals, bony labyrinth morphology is also indicative of phylogenetic relatedness (e.g., Ekdale 2013, Benoit et al. 2015, Grohe5 et al 2016, Costeur et al 2018, Schwab et al 2019, del Rio et al 2021, Le Maî/ tre et al. 2023). ...
Evolutionary convergence in distantly related species is among the most convincing evidence of adaptive evolution. The mammalian ear, responsible for balance and hearing, is not only characterised by its spectacular evolutionary incorporation of several bones of the jaw, it also varies considerably in shape across modern mammals. Using a new multivariate approach, we show that in Afrotheria, a monophyletic clade with morphologically and ecologically highly disparate species, inner ear shape evolved similar adaptations as in non-afrotherian mammals. We identified four trait combinations that underlie this convergence. The high evolvability of the mammalian ear is surprising: nowhere else in the skeleton are different functional units so close together; it includes the smallest bones of the skeleton, and is encapsulated within the densest bone. We suggest that this evolvability is a direct consequence of the increased genetic and developmental complexity of the mammalian ear compared to other vertebrates.
... Previous studies have demonstrated that the mammalian cochlea and semicircular canals contain strong phylogenetic signals (Billet et al., 2015;Braga et al., 2015;Ekdale, 2016;Mennecart and Costeur, 2016;Costeur et al., 2018;Pfaff et al., 2019;Schwab et al., 2019). The bony labyrinth has also been shown to contain phylogenetic information in primates, including humans and fossil hominins Lebrun et al., 2010;Braga et al., 2015;Quam et al., 2016;Morimoto et al., 2020). ...
The bony labyrinth contains phylogenetic information that can be used to determine interspecific differences between fossil hominins. The present study conducted a comparative 3D geometric morphometric analysis on the bony labyrinth of the Middle Pleistocene Sima de los Huesos (SH) hominins. The findings of this study corroborate previous multivariate analyses of the SH hominin bony labyrinth. The analysis of the semicircular canals revealed the SH hominin canal morphologies appear closer to those of the Neandertals than to those of Homo sapiens. This is attributable to a Neandertal-like ovoid anterior canal, and mediolaterally expanded, circular posterior canal. However, the SH hominins lack the increased torsion in the anterior canal and the inferior orientation of the lateral canal seen in Neandertals. The results of the cochlear analysis indicated that, although there is some overlap, there are notable differences between the SH hominins and the Neandertals. In particular, the SH hominin cochlea appears more constricted than in Neandertals in the first and second turns. A principal component analysis of the full bony labyrinth separated most SH hominins from the Neandertals, which largely clustered with modern humans. A covariance ratio analysis found a significant degree of modularity within the bony labyrinth of all three groups, with the SH hominins and Neandertals displaying the highest modularity. This modular signal in the bony labyrinth may be attributable to different selective pressures related to locomotion and audition. Overall, the results of this study confirm previous suggestions that the semicircular canals in the SH hominins are somewhat derived toward Neandertals, while their cochlea is largely primitive within the genus Homo.
... The felid subfamily Pantherinae comprises the genera Panthera and Neofelis, which are found in a variety of habitats and characterized by different kinds of ecology, e.g., hunting and locomotion style as well as habitat (Nowak 1991;Sunquist and Sunquist 2002;Wilson and Mittermeier 2009;Davis et al. 2010;Billet et al. 2012Pfaff et al. 2015Pfaff et al. , 2017Schwab et al. 2019). Extant Panthera species comprise the lion (P. ...
... Several authors associate the shape of the bony labyrinth with ecological and phylogenetic information of extant species. Hence, bony labyrinth morphology and morphometry can serve as a functional and ecological proxy but also provides characters for phylogenetic analyses in extant and extinct mammals (e.g., Spoor et al. 2007;Billet et al. 2012Pfaff et al. 2015Pfaff et al. , 2017Schwab et al. 2019). ...
... Previous studies on the inner ear and/or bony labyrinth that also include members of Pantherinae are restricted to selected species that are mostly used for comparison as part of a larger sample. Panthera leo (Spoor et al. 2007;Pfaff et al. 2017;Schwab et al. 2019) and Panthera tigris Úlehlová et al. 1984;Spoor et al. 2007;Grohé et al. 2018;Schwab et al. 2019) are the most prominent species, followed by Panthera pardus (Pfaff et al. 2017;Grohé et al. 2018), Panthera onca Úlehlová et al. 1984) and Neofelis nebulosa (Grohé et al. 2018). To our knowledge, there is no published data of the bony labyrinth of Panthera uncia and Neofelis diardi. ...
The bony labyrinth (inner ear) of mammals reveals systematic as well as morphofunctional information. However, detailed knowledge of bony labyrinth morphology and ontogeny in Pantherinae, that comprise some of the most iconic mammals, is still pending. Hence, we present the first comparative description of the bony labyrinth in all extant species of Panthera and Neofelis some of which are represented by several postnatal stages; particular focus is set on Panthera leo. Our study is based on µCT scans and virtual 3D reconstructions and accompanied by selected morphometric measurements. Even though quite similar in morphology, both genera as well as their species can be distinguished by several features, e.g., shape and relative size of the semicircular canals and presence or absence of an osseous secondary crus commune. In case of the latter, P. pardus shows some intraspecific variation. We also traced the reduction of the fossa subarcuata during ontogeny in P. leo which conforms with previous studies. Negative allometry of the bony labyrinth in relation to skull basal length can be observed during ontogeny as demonstrated by P. leo as well as between different sized species. Although not correlated with the length of the cochlear canal, the number of cochlear turns is higher in captive non-adult P. leo and P. tigris, but lower in adult captive P. pardus. If these intraspecific differences are related to captivity or represent an ontogenetic pattern, needs to be evaluated in future studies based on larger samples.
... In mammals, the semicircular canal morphology was found to be linked to agility (Spoor et al., 2007;Silcox et al., 2009;Perier et al., 2016;Gonzales et al., 2019;contra Morimoto et al., 2020), posture (Le Maître et al., 2017;Spoor & Zonneveld, 1998;Spoor et al., 1994Spoor et al., , 1996, locomotion (Georgi, 2008; but see Rae et al., 2016), and ecology (Grohé et al., 2016;Pfaff et al., 2015;Ekdale, 2016;Schwab et al., Lebrun et al. (2010), as detailed in Appendix S2. ASC, anterior semicircular canal; CC, common crus; Co, cochlea; LSC, lateral semicircular canal; OW, oval window; PSC, posterior semicircular canal; RW, round window; VA, vestibular aqueduct; Ve, vestibule. ...
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Discoveries in recent decades indicate that the large papionin monkeys Paradolipopithecus and Procynocephalus are key members of the Late Pliocene - Early Pleistocene mammalian faunas of Eurasia. However, their taxonomical status, phylogenetic relationships, and ecological profile remain unclear. Here we investigate the two latter aspects through the study of the inner ear anatomy, as revealed by applying micro-CT scan imaging techniques on the cranium LGPUT DFN3-150 of Paradolichopithecus from the lower Pleistocene (2.3 Ma) fossil site Dafnero-3 in Northwestern Greece. Using geometric morphometric methods, we quantified shape variation and the allometric and phylogenetic signals in extant cercopithecines (n = 80), and explored the morphological affinities of the fossil specimen with extant taxa. LGPUT DFN3-150 has a large centroid size similar to that of baboons and their relatives. It shares several shape features with Macacina and Cercopithecini, which we interpret as probable retention of a primitive morphology. Overall, its inner ear morphology is more consistent with a stem Papionini more closely related to Papionina than Macacina, or to a basal crown Papionina. Our results, along with morphometrical and ecological features from previous studies, call into question the traditional hypothesis of a Paradolichopithecus-Macacina clade, and provide alternative perspectives in the study of Eurasian primate evolution during the late Neogene-Quaternary.
Supplementary information:
The online version contains supplementary material available at 10.1007/s10764-022-00329-4.
... Semicircular canal morphology has previously been associated with habitat, behaviour and locomotion in various vertebrate groups (e.g. Hanson et al., 2021;Neenan et al., 2017;Schwab et al., 2019Schwab et al., , 2020Spoor et al., 2002; see also Bronzati et al., 2021). ...
... As the inner ear is involved in the sensation of balance and equilibrium, it has previously been demonstrated that morphological changes in crocodylomorphs and various other vertebrate groups over evolutionary time and across phylogeny are linked to their lifestyle and ecology (e.g. Neenan et al., 2017;Schwab et al., 2019Schwab et al., , 2020Spoor et al., 2002). The vestibular system, including the three semicircular canals, plays an important role in head and gaze stabilisation (vestibulo-ocular and vestibulo-collic reflexes), and hence is crucial for an animal to balance its body in complex threedimensional environments. ...
... Significant differences in labyrinth morphology have been noted between secondarily fully aquatic (pelagic) amniote species and their more terrestrial or semi-aquatic ancestors (Neenan et al., 2017;Schwab et al., 2020;Spoor et al., 2002). Other differences have also been recognised within taxonomic groups associated with different lifestyles and hunting strategies (Capshaw et al., 2019;Pfaff et al., 2015;Schwab et al., 2019). This raises the question: if labyrinth size and shape changes across phylogeny were linked to changes in habitat or behaviour, do labyrinth size and shape changes across ontogeny correlate with behavioural or biological shifts in crocodylians? ...
Crocodylians today live in tropical to subtropical environments, occupying mostly shallow waters. Their body size changes drastically during ontogeny, as do their skull dimensions and bite forces, which are associated with changes in prey preferences. Endocranial neurosensory structures have also shown to change ontogenetically, but less is known about the vestibular system of the inner ear. Here we use 30 high-resolution computed tomography (CT) scans and three-dimensional geometric morphometrics to investigate the size and shape changes of crocodylian endosseous labyrinths throughout ontogeny, across four stages (hatchling, juvenile, subadult and adult). We find two major patterns of ontogenetic change. First, the labyrinth increases in size during ontogeny, with negative allometry in relation to skull size. Second, labyrinth shape changes significantly, with hatchlings having shorter semicircular canal radii, with thicker diameters and an overall dorsoventrally shorter labyrinth than those of more mature individuals. We argue that the modification of the labyrinth during crocodylian ontogeny is related to constraints imposed by skull growth, due to fundamental changes in the crocodylian braincase during ontogeny (e.g. verticalisation of the basicranium), rather than changes in locomotion, diet, or other biological functions or behaviours.
... The anatomy of the bony labyrinth is generally conservative in vertebrates. It could be relevant in morphofunctional studies and could provide some information to solve phylogenetic and paleobiological problems that have mainly been scrutinized by studying teeth [5], although the cochlea provides more phylogenetic signals than the semicircular canals [6][7][8][9]. Indeed, mechanosensory organs are useful anatomical systems to learn about the function, ecology, and phylogeny of living and extinct vertebrates [9]. ...
... It could be relevant in morphofunctional studies and could provide some information to solve phylogenetic and paleobiological problems that have mainly been scrutinized by studying teeth [5], although the cochlea provides more phylogenetic signals than the semicircular canals [6][7][8][9]. Indeed, mechanosensory organs are useful anatomical systems to learn about the function, ecology, and phylogeny of living and extinct vertebrates [9]. The vestibular system regulates the sense of balance and spatial orientation in movement coordination, while the semicircular canals (sensory detectors of head rotational acceleration and their mutual degree of orthogonality) may provide useful clues for inferring agility and head angular velocity during locomotion [7,[10][11][12][13][14]. ...
This is the first study on the bony labyrinth of Cynotherium sardous, an intriguing extinct canid that inhabited Sardinia in the late Middle and Late Pleistocene. The morphological features of the cochlea indicate that C. sardous had a lower number of cochlear turns (2.25) than all extant canids. This feature, as well as the reduced length of the spiral canal, the cochlear curvature rate, and the narrow basal membrane, indicates that C. sardous had poor hearing abilities limited to high-frequency sounds with a low limit of 250 Hz and poor echolocalization skills. From the data available, it is not possible to infer whether C. sardous was unable to echolocalize its prey and relied on other senses (e.g., smell and sight) to locate them or whether the acoustic range of C. sardous was specialized for identifying the sounds produced by its most common prey to transmit signals for predator warnings or group communication. All things considered, the results obtained confirm the utility of cochlea morphological studies in reconstructing the hearing abilities of this species and in providing some suggestions about its ethology, but they fall short of providing any new sound evidence regarding the ecological role of C. sardous in the Late Pleistocene Sardinian ecosystem.
... Semicircular canal morphologies of the "slow" lorisids and "fast" galagids are clearly differentiated in shape space. As tempting as it is to link these shape differences to variation in locomotor behaviours and/or agility, such morphological differences might also largely be explained by phylogeny [93][94][95][96][97][98]. ...
The vestibular system of the mammalian inner ear senses angular and linear velocity of the head and enables animals to maintain their balance. Vestibular anatomy has been studied extensively in order to link its structure to particular kinds of locomotion. Available evidence indicates that, in primates, slow-moving species show higher levels of vestibular variation than fast-moving taxa. We analysed intraspecific morphological variation and fluctuating asymmetry (FA) levels in the semicircular canal systems of six species of lorisiform primates: three slow-moving lorisids and three fast-moving galagids. Our results showed clear differences in levels of intraspecific variation between slow-moving and fast-moving taxa. Higher levels of variation were responsible for deviations from coplanarity for synergistic pairs of canals in slower taxa. Lorisids also presented higher levels of FA than galagids. FA is a better indicator of agility than intraspecific variation. These results suggest that in order to function efficiently in fast taxa, semicircular canal systems must develop as symmetrically as possible, and should minimise the deviation from coplanarity for synergistic pairs. Higher levels of variation and asymmetry in slow-moving taxa may be related to lower levels of stabilising selection on the vestibular system, linked to a lower demand for rapid postural changes.
... As a crucial component of the system of balance and equilibrium, bony labyrinth morphology is regularly used to reveal insights into ancient animal behavior and lifestyles (e.g., refs. [15][16][17]. Because of the physical differences between air and water, this system shouldand does-differ in terrestrial and aquatic species (18). ...
Major evolutionary transitions, in which animals develop new body plans and adapt to dramatically new habitats and lifestyles, have punctuated the history of life. The origin of cetaceans from land-living mammals is among the most famous of these events. Much earlier, during the Mesozoic Era, many reptile groups also moved from land to water, but these transitions are more poorly understood. We use computed tomography to study changes in the inner ear vestibular system, involved in sensing balance and equilibrium, as one of these groups, extinct crocodile relatives called thalattosuchians, transitioned from terrestrial ancestors into pelagic (open-ocean) swimmers. We find that the morphology of the vestibular system corresponds to habitat, with pelagic thalattosuchians exhibiting a more compact labyrinth with wider semicircular canal diameters and an enlarged vestibule, reminiscent of modified and miniaturized labyrinths of other marine reptiles and cetaceans. Pelagic thalattosuchians with modified inner ears were the culmination of an evolutionary trend with a long semiaquatic phase, and their pelagic vestibular systems appeared after the first changes to the postcranial skeleton that enhanced their ability to swim. This is strikingly different than cetaceans, which miniaturized their labyrinths soon after entering the water, without a prolonged semiaquatic stage. Thus, thalattosuchians and cetaceans became secondarily aquatic in different ways and at different paces, showing that there are different routes for the same type of transition.
