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Frontal view of an adult dwarf sperm whale (Kogia sima). The view is through the axis of the bony left nasal passage. Note the high degree of skewing and asymmetry. Main bony structures: FR‐frontal, LP‐left nasal passage, GR‐groove of rostral cartilage (mesorostral groove), MX‐maxilla, PM‐premaxilla, RP‐right nasal passage, PS‐presphenoid (note that the bony structure termed mesethmoid is actually the presphenoid; Ichishima, 2016).
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In this study, the nasal asymmetry of odontocetes (toothed whales) was analyzed morphometrically by placing landmarks on photographed nasofacial skulls from 12 different species and genera that belong to four odontocete families. The results show that the degree of asymmetry tends to be linked with the mechanism of click sound generation in odontoc...
Citations
... For example, subtle directional asymmetries in insect wings have been repeatedly demonstrated, but may be of little adaptive significance, due to limited functional consequences (Klingenberg et al., 1998;Pélabon & Hansen, 2008;Pither & Taylor, 2000). On the other hand, conspicuous DA in the skull of toothed whales was argued to be related to feeding or biosonar function (Churchill et al., 2019;del Castillo et al., 2016;Huggenberger et al., 2017;Laeta et al., 2023;Lanzetti et al., 2022;Macleod et al., 2007), while extreme conspicuous DA in the skulls of flatfishes relates to their benthic ecology (Evans et al., 2021), conspicuous antisymmetry in many Crustacean appendages is related to divergent left and right functions (Govind, 1989;Govind & Blundon, 1985;Levinton, 2016;Pratt & Mclain, 2002), and in humans and mice, the mirroring of internal organs, or situs inversus, is mostly problematic when only 2 Ginot et al. some of the organs are concerned, while complete situs inversus entails no major health defects (Palmer, 2004). ...
Bilateral symmetry is widespread across animals, yet, among bilaterians, many cases of conspicuous asymmetries evolved. This means that bilaterally homologous structures on the left and right sides display divergent phenotypes. The evolution of such divergent phenotypes between otherwise similarly shaped structures can be thought to be favored by modularity, but this has rarely been studied in the context of left-right differences. Here, we provide an empirical example, using geometric morphometrics to assess patterns of asymmetry and covariation between landmark partitions in a grasshopper with conspicuously asymmetric mandibles. Our morphometric data confirm the presence of strictly directional conspicuous asymmetry in the mandibles and surrounding structures. Covariance patterns and tests hint at a strong integration between mandibles despite their divergent morphologies, and variational modularity with the head capsule. While mandibles have been selected to achieve a key-and-lock morphology by having interlocking shapes, the developmental modularity required to achieve this seems to be overwritten by developmental and/or functional integration, allowing the precise matching required for feeding. The consequent conflicting covariation patterns are reminiscent of the palimpsest model. Finally, the degree of directional asymmetry appears to be under selection, although we find no relationship between bite force and mandible shape or asymmetry.
... Directional asymmetry is the expression of a feature with consistent laterality, ranging from atomic to bodily feature (Neville, 1976;Palmer, 2009). In Cetacea (originating during the asymmetry (Ness, 1967;Hirose et al., 2015;Huggenberger et al., 2016a). Extant members of the latest diverging families, Monodontidae, Phocoenidae and Delphinidae, forming the superfamily Delphinoidea (Milinkovitch et al., 1994;Waddell et al., 2000;McGowen et al., 2020), present highly variable levels of asymmetry (Ness, 1967;Galatius & Goodall, 2016;Laeta et al., 2020). ...
... Further studies investigating the relationship between magnitude of asymmetry and frequencies of echolocation clicks among odontocete taxa have not detected a clear signal. Huggenberger et al. (2016a) compared the highly asymmetric Kogia sima (Owen, 1866) and the subtly asymmetric Pontoporia blainvillei (Gervais & d'Orbigny, 1844), the phocoenids P. ...
... Asymmetric shape variation was consistent in its directionality and in the structures involved across all ten odontocete families, with the skull midline and premaxillae shifting to the left as observed by Ness (1967), Mead (1975) and Heyning (1989). The skull outline and suture crest between the frontal and interparietal were displaced to the right with concomitant greater dimensions of the right premaxilla and maxilla compared to the left (Figure 2), in accordance with Galatius & Goodall (2016), Huggenberger et al. (2016a) and Laeta et al. (2020). The landmark at the suture between the frontals, close to the nasal bones, indicates a leftward deviation of the skull midline in this area. ...
Directional cranial asymmetry is an intriguing condition that has evolved in all odontocetes which has mostly been associated with sound production for echolocation. In this study, we investigated how cranial asymmetry varies across odontocete species both in terms of quality (i.e., shape), and quantity (magnitude of deviation from symmetry). We investigated 72 species across all ten families of Odontoceti using two-dimensional geometric morphometrics. The average asymmetric shape was largely consistent across odontocetes - the rostral tip, maxillae, antorbital notches and braincase, as well as the suture crest between the frontal and interparietal bones were displaced to the right, whereas the nasal septum and premaxillae showed leftward shifts, in concert with an enlargement of the right premaxilla and maxilla. A clear phylogenetic signal related to asymmetric shape variation was identified across odontocetes using squared-change parsimony. The magnitude of asymmetry was widely variable across Odontoceti, with greatest asymmetry in Kogiidae, Monodontidae and Globicephalinae, followed by Physeteridae, Platanistidae and Lipotidae, while the asymmetry was lowest in Lissodelphininae, Phocoenidae, Iniidae and Pontoporiidae. Ziphiidae presented a wide spectrum of asymmetry. Generalized linear models explaining magnitude of asymmetry found associations with click source level while accounting for cranial size. Using phylogenetic generalized least squares, we reconfirm that source level and centroid size significantly predict the level of cranial asymmetry, with more asymmetric marine taxa generally consisting of bigger species emitting higher output sonar signal, i.e. louder sounds. Both characteristics theoretically support foraging at depth, the former by allowing extended diving and the latter being adaptive for prey detection at longer distances. Thus, cranial asymmetry seems to be an evolutionary pathway that allows odontocetes to devote more space for sound-generating structures associated with echolocation and thus increases biosonar search range and foraging efficiency beyond simple phylogenetic scaling predictions.
... Geometric Morphometrics (GM) permits partitioning of the asymmetric and symmetric components of shape variation (Klingenberg et al. 2002). As many species of toothed whales show a high degree of asymmetry in their crania (MacLeod 2002;MacLeod et al. 2007;Fahlke et al. 2011;Galatius and Goodall 2016;del Castillo et al. 2017;Huggenberger et al. 2017;Coombs et al. 2020) and as the asymmetric component is relevant to answer the intended research questions, these variables were partitioned using the function bilateral.symmetry in geomorph package (Adams et al. 2016). Analyses were also performed on the whole skull No. ...
... The asymmetric shape and presence of specialized fats in the melon allow for the focussing of vocalizations into a highly directional sonar beam for prey echolocation (Surlykke et al. 2014). This system of sound production for echolocation has diversified into distinct forms resulting in varying degrees of skull directional asymmetry within toothed whales (Fahlke et al. 2011;Huggenberger et al. 2017;Coombs et al. 2020). Trade-offs between size, frequencies emitted, and beam directionality are known (Jensen et al. 2018), and our results confirm the correlation between skull size, biosonar mode and maximum peak frequencies. ...
Extant odontocetes (toothed whales) exhibit differences in body size and brain mass, biosonar mode, feeding strategies, and diving and habitat adaptations. Strong selective pressures associated with these factors have likely contributed to the morphological diversification of their skull. Here, we used 3D landmark geometric morphometric data from the skulls of 60 out of ~ 72 extant odontocete species and a well-supported phylogenetic tree to test whether size and shape variation are associated with ecological adaptations at an interspecific scale. Odontocete skull morphology exhibited a significant phylogenetic signal, with skull size showing stronger signal than shape. After accounting for phylogeny, significant associations were detected between skull size and biosonar mode, body length, brain and body mass, maximum and minimum prey size, and maximum peak frequency. Brain mass was also strongly correlated with skull shape together with surface temperature and average and minimum prey size. When asymmetric and symmetric components of shape were analysed separately, a significant correlation was detected between sea surface temperature and both symmetric and asymmetric components of skull shape, and between diving ecology and the asymmetric component. Skull shape variation of odontocetes was strongly influenced by evolutionary allometry but most of the associations with ecological variables were not supported after phylogenetic correction. This suggests that ecomorphological feeding adaptations vary more between, rather than within, odontocete families, and functional anatomical patterns across odontocete clades are canalised by size constraints.
... In adult modern odontocetes, asymmetry is mostly prominent in the neurocranium and nasal openings [2,12]. The bones of the right side of the skull are typically larger and expand leftward, reflecting the morphology of the overlying soft tissues [2,13], in particular the melon, the fat body that is involved in focusing and transmitting high frequency sounds to the surrounding water, and the phonic lips, valves located in the nasals passages that control sound emission [11,14]. It has been shown that varying levels of asymmetry in odontocetes are directly correlated with production of sound and its frequency [13,15], as well as in directionality of hearing [9]. ...
... The bones of the right side of the skull are typically larger and expand leftward, reflecting the morphology of the overlying soft tissues [2,13], in particular the melon, the fat body that is involved in focusing and transmitting high frequency sounds to the surrounding water, and the phonic lips, valves located in the nasals passages that control sound emission [11,14]. It has been shown that varying levels of asymmetry in odontocetes are directly correlated with production of sound and its frequency [13,15], as well as in directionality of hearing [9]. ...
... While evolutionary changes in skull asymmetry and its possible drivers have been studied extensively in Odontoceti (e.g. [2,12,13]), the developmental origin of this trait remains largely unexplored, despite the established importance of ontogenetic shifts in the rise of other unique cetacean traits, such as hind limb reduction or tooth loss [16,17]. Here, we address this gap with quantitative analysis to answer the question: how does skull asymmetry develop in toothed whales ? ...
Extreme asymmetry of the skull is one of the most distinctive traits that characterizes toothed whales (Odontoceti, Cetacea). The origin and function of cranial asymmetry are connected to the evolution of echolocation, the ability to use high-frequency sounds to navigate the surrounding environment. Although this novel phenotype must arise through changes in cranial development, the ontogeny of cetacean asymmetry has never been investigated. Here we use three-dimensional geometric morphometrics to quantify the changes in degree of asymmetry and skull shape during prenatal and postnatal ontogeny for five genera spanning odontocete diversity (oceanic dolphins, porpoises and beluga). Asymmetry in early ontogeny starts low and tracks phylogenetic relatedness of taxa. Distantly related taxa that share aspects of their ecology overwrite these initial differences via heterochronic shifts, ultimately converging on comparable high levels of skull asymmetry. Porpoises maintain low levels of asymmetry into maturity and present a decelerated rate of growth, probably retained from the ancestral condition. Ancestral state reconstruction of allometric trajectories demonstrates that both paedomorphism and peramorphism contribute to cranial shape diversity across odontocetes. This study provides a striking example of how divergent developmental pathways can produce convergent ecological adaptations, even for some of the most unusual phenotypes exhibited among vertebrates.
... In adult modern odontocetes, asymmetry is mostly prominent in the neurocranium and nasal openings [2,12]. The bones of the right side of the skull are typically larger and expand leftward, reflecting the morphology of the overlying soft tissues [2,13], in particular the melon, the fat body that is involved in focusing and transmitting high frequency sounds to the surrounding water, and the phonic lips, valves located in the nasals passages that control sound emission [11,14]. It has been shown that varying levels of asymmetry in odontocetes are directly correlated with production of sound and its frequency [13,15], as well as in directionality of hearing [9]. ...
... The bones of the right side of the skull are typically larger and expand leftward, reflecting the morphology of the overlying soft tissues [2,13], in particular the melon, the fat body that is involved in focusing and transmitting high frequency sounds to the surrounding water, and the phonic lips, valves located in the nasals passages that control sound emission [11,14]. It has been shown that varying levels of asymmetry in odontocetes are directly correlated with production of sound and its frequency [13,15], as well as in directionality of hearing [9]. ...
... While evolutionary changes in skull asymmetry and its possible drivers have been studied extensively in Odontoceti [e.g. 2,12,13], the developmental origin of this trait remains largely unexplored, despite the established importance of ontogenetic shifts in the rise of other unique cetacean traits, such as hind limb reduction or tooth loss [16,17]. Here, we address this gap with a quantitative analysis to answer the question: how does skull asymmetry develop in toothed whales? ...
Extreme asymmetry of the skull is one of the most distinctive traits that characterizes toothed whales (Odontoceti, Cetacea). The origin and function of cranial asymmetry are connected to the evolution of echolocation, the ability to use high frequency sounds to navigate the surrounding environment. Although this novel phenotype must arise through changes in cranial development, the ontogeny of cetacean asymmetry has never been investigated. Here we use three-dimensional geometric morphometric to quantify the changes in degree of asymmetry and skull shape during prenatal and postnatal ontogeny for five genera spanning odontocete diversity (oceanic dolphins, porpoises, and beluga). Asymmetry in early ontogeny starts low and tracks phylogenetic relatedness of taxa. Distantly-related taxa that share aspects of their ecology overwrite these initial differences via heterochronic shifts, ultimately converging on comparable high levels of skull asymmetry. Porpoises maintain low levels of asymmetry into maturity and present a decelerated rate of growth, likely retained from the ancestral condition. Ancestral state reconstruction of allometric trajectories demonstrates that both paedomorphism and peramorphism contribute to cranial shape diversity across odontocetes. This study provides a striking example of how divergent developmental pathways can produce convergent ecological adaptations, even for some of the most unusual phenotypes exhibited among vertebrates.
... This suggests that periotics have specific characteristics that are useful for taxonomic identification. Odontoceti are characterized by asymmetric skulls in the Delphinidae, Physeteridae, and Kogiidae and to a lesser degree in the Phocoenidae (Ness 1967;Huggenberger et al. 2017). Our results show that this asymmetry did not affect taxonomic identification of any family based on periotics, regardless of right or left. ...
Twenty-three species and four subspecies of odontocete belonging to five families (Delphinidae, Physeteridae, Kogiidae, Phocoenidae, and Ziphiidae) are distributed along the Pacific coast of northern Mexico. The morphological variability of these species has been studied extensively and a number of taxonomic studies have focused on cranial characteristics. The goal of this study was to describe the periotics of the odontocetes of the Pacific coast of northern Mexico and develop a taxonomic tool using descriptions of each species. We used a geometric morphometric analysis of 186 periotics housed in local and national osteological collections. Our results show the taxonomic value of periotics and a significant phylogenetic signal associated with this structure. Based on these results we present a descriptive catalog that can be used for identification purposes.
... Geometric morphometrics permit partitioning of the asymmetric and symmetric components of shape variation (Klingenberg et al. 2002). As many species of odontocetes show a high degree of directional asymmetry in their crania (MacLeod 2002;Fahlke et al. 2011;Fahlke and Hampe 2015;Huggenberger et al. 2017;Churchill et al. 2019) and because the asymmetric component is relevant for the aim of the study, these variables were partitioned following the guidelines of Klingenberg et al. (2002). ...
The false killer whale (Pseudorca crassidens (Owen, 1846)) is a globally distributed delphinid that shows geographical differentiation in its skull morphology. We explored cranial morphological variation in a sample of 85 skulls belonging to a mixed sex population stranded in the Moray Firth, Scotland, in 1927. A three-dimensional digitizer (Microscribe 2GX) was used to record 37 anatomical landmarks on the cranium and 25 on the mandible to investigate size and shape variation and to explore sexual dimorphism using geometric morphometric. Males showed greater overall skull size than females, whereas no sexual dimorphism could be identified in cranial and mandibular shape. Allometric skull changes occurred in parallel for both males and females, supporting the lack of sexual shape dimorphism for this particular sample. Also, fluctuating asymmetry did not differ between crania of males and females. This study confirms the absence of sexual shape dimorphism and the presence of a sexual size dimorphism in this false killer whale population.
... Some of the greatest morphological changes in response to the environment observed in any mammalian skull are that of Cetacea. Evolution of telescoping and asymmetry within the cetacean skull have, respectively, facilitated breathing and echolocation enabling cetacean species to thrive within aquatic environments (Miller, 1923;Huggenberger et al., 2017). Telescoping is seen in both odontocetes (toothed whales) and mysticetes (baleen whales), although differs slightly between the clades (Miller, 1923). ...
Phenotypic variation across mammals is extensive and reflects their ecological diversification into a remarkable range of habitats on every continent and in every ocean. The skull performs many functions to enable each species to thrive within its unique ecological niche, from prey acquisition, feeding, sensory capture (supporting vision and hearing) to brain protection. Diversity of skull function is reflected by its complex and highly variable morphology. Cranial morphology can be quantified using geometric morphometric techniques to offer invaluable insights into evolutionary patterns, ecomorphology, development, taxonomy, and phylogenetics. Therefore, the skull is one of the best suited skeletal elements for developmental and evolutionary analyses. In contrast, less attention is dedicated to the fibrous sutural joints separating the cranial bones. Throughout postnatal craniofacial development, sutures function as sites of bone growth, accommodating expansion of a growing brain. As growth frontiers, cranial sutures are actively responsible for the size and shape of the cranial bones, with overall skull shape being altered by changes to both the level and time period of activity of a given cranial suture. In keeping with this, pathological premature closure of sutures postnatally causes profound misshaping of the skull (craniosynostosis). Beyond this crucial role, sutures also function postnatally to provide locomotive shock absorption, allow joint mobility during feeding, and, in later postnatal stages, suture fusion acts to protect the developed brain. All these sutural functions have a clear impact on overall cranial function, development and morphology, and highlight the importance that patterns of suture development have in shaping the diversity of cranial morphology across taxa. Here we focus on the mammalian cranial system and review the intrinsic relationship between suture development and morphology and cranial shape from an evolutionary developmental biology perspective, with a view to understanding the influence of sutures on evolutionary diversity. Future work integrating suture development into a comparative evolutionary framework will be instrumental to understanding how developmental mechanisms shaping sutures ultimately influence evolutionary diversity.
... Skull asymmetry was believed to be involved in the production of NBHF clicks, but Galatius and Goodall (2016) and Huggenberger et al. (2017) did not support this hypothesis based on investigation of the skulls of 10 and 12 species, respectively. Although the skulls of odontocetes differ in their morphology, the basic parabolic structure that supports the soft tissue from below is the same for all species. ...
1. The pulse-like clicking sounds made by odontocetes for echolocation (biosonar) can be roughly classified by their frequency characteristics into narrowband high-frequency (NBHF) clicks with a sharp peak at around 130 kHz and wide-band (WB) clicks with a moderate peak at 30–100 kHz. Structural differences in the sound-producing organs between NBHF species and WB species have not been comprehensively discussed, nor has the formation of NBHF and WB clicks.
2. A review of the sound-producing organs, including the latest findings, could lead to a new hypothesis about the sound production mechanisms. In the current review, data on echolocation click characteristics and on the anatomical structure of the sound-producing organs were compared in 33 species (14 NBHF species and 19 WB species).
3. We review interspecific information on the characteristics of click frequencies and data from computed tomography scans and morphology of the sound producing organs, accumulated in conventional studies. The morphology of several characteristic structures, such as the melon, the dense connective tissue over the melon (the ‘porpoise capsule’), and the vestibular sacs, was compared interspecifically.
4. Interspecific comparisons suggest that the presence or absence of the porpoise capsule is unlikely to affect echolocation frequency. Folded structures in the vestibular sacs, features that have been overlooked until now, are present in most species with NBHF sound production and not in WB species; the vestibular sacs are therefore likely to be important in determining echolocation click frequency characteristics. The acoustical properties of the shape of the melon and vestibular sacs are important topics for future investigations about the relationship between anatomical structure and sound-producing mechanisms for echolocation clicks.
... Odontocete asymmetry is thought to have evolved as a result of an evolutionary hyperallometric investment into sound-producing structures to facilitate the production of high frequency vocalisations [11,[19][20][21][22], but alternative explanations have been put forward. MacLeod et al. [18] proposed that skull asymmetry is a by-product of the selection pressure for an asymmetrically positioned larynx, an aquatic adaptation which enables the swallowing of large prey underwater without mastication. ...
... The highest asymmetry is seen in the platanistids, monodontids, and physeteroids ( Fig. 3 (6-8)). There are some exceptions within odontocetes, however, such as lower levels of asymmetry in the other extant river dolphins (Inia, Pontoporia, and Lipotes) [21,31]. Lower asymmetry is also observed in the family Eurhinodelphinidae [32], the extant phocoenids [26,33], and genus Sousa [14] (Fig. 3 (5)). ...
... Quantifying cranial asymmetry in living and extinct mysticetes allows reconsideration of the evolution of echolocation in this clade. The consensus is that cranial asymmetry in whales evolved due to the production of high-frequency vocalisations [19][20][21]. The consistent level of symmetry in the mysticetes corroborates the hypothesis that mysticetes never evolved sophisticated echolocation [25,62] and also contradicts the hypothesis that this suborder secondarily lost their echolocation capabilities [63]. ...
Background:
Unlike most mammals, toothed whale (Odontoceti) skulls lack symmetry in the nasal and facial (nasofacial) region. This asymmetry is hypothesised to relate to echolocation, which may have evolved in the earliest diverging odontocetes. Early cetaceans (whales, dolphins, and porpoises) such as archaeocetes, namely the protocetids and basilosaurids, have asymmetric rostra, but it is unclear when nasofacial asymmetry evolved during the transition from archaeocetes to modern whales. We used three-dimensional geometric morphometrics and phylogenetic comparative methods to reconstruct the evolution of asymmetry in the skulls of 162 living and extinct cetaceans over 50 million years.
Results:
In archaeocetes, we found asymmetry is prevalent in the rostrum and also in the squamosal, jugal, and orbit, possibly reflecting preservational deformation. Asymmetry in odontocetes is predominant in the nasofacial region. Mysticetes (baleen whales) show symmetry similar to terrestrial artiodactyls such as bovines. The first significant shift in asymmetry occurred in the stem odontocete family Xenorophidae during the Early Oligocene. Further increases in asymmetry occur in the physeteroids in the Late Oligocene, Squalodelphinidae and Platanistidae in the Late Oligocene/Early Miocene, and in the Monodontidae in the Late Miocene/Early Pliocene. Additional episodes of rapid change in odontocete skull asymmetry were found in the Mid-Late Oligocene, a period of rapid evolution and diversification. No high-probability increases or jumps in asymmetry were found in mysticetes or archaeocetes. Unexpectedly, no increases in asymmetry were recovered within the highly asymmetric ziphiids, which may result from the extreme, asymmetric shape of premaxillary crests in these taxa not being captured by landmarks alone.
Conclusions:
Early ancestors of living whales had little cranial asymmetry and likely were not able to echolocate. Archaeocetes display high levels of asymmetry in the rostrum, potentially related to directional hearing, which is lost in early neocetes-the taxon including the most recent common ancestor of living cetaceans. Nasofacial asymmetry becomes a significant feature of Odontoceti skulls in the Early Oligocene, reaching its highest levels in extant taxa. Separate evolutionary regimes are reconstructed for odontocetes living in acoustically complex environments, suggesting that these niches impose strong selective pressure on echolocation ability and thus increased cranial asymmetry.
