Skull shapes of the Lissodelphininae: radiation,adaptation and asymmetry

Within Delphinidae, the sub‐family Lissodelphininae consists of 8 Southern Ocean species and 2 North Pacific species. Lissodelphininae is a result of recent phylogenetic revisions based on molecular methods. Thus, morphological radiation within the taxon has not been investigated previously. The sub‐family consists of ecologically diverse groups such as (1) the Cephalorhynchus genus of 4 small species inhabiting coastal and shelf waters, (2) the robust species in the Lagenorhynchus genus with the coastal La. australis, the offshore La. cruciger, the pelagic species La. obscurus and La. obliquidens, and (3) the morphologically aberrant genus Lissodelphis. Here, the shapes of 164 skulls from adults of all 10 species were compared using 3‐dimensional geometric morphometrics. The Lissodelphininae skulls were supplemented by samples of Lagenorhynchus albirostris and Delphinus delphis to obtain a context for the variation found within the subfamily. Principal components analysis was used to map the most important components of shape variation on phylogeny. The first component of shape variation described an elongation of the rostrum, lateral and dorsoventral compression of the neurocranium and smaller temporal fossa. The two Lissodelphis species were on the high extreme of this spectrum, while Lagenorhynchus australis, La. cruciger and Cephalorhynchus heavisidii were at the low extreme. Along the second component, La. cruciger was isolated from the other species by its expanded neurocranium and concave facial profile. Shape variation supports the gross phylogenetic relationships proposed by recent molecular studies. However, despite the great diversity of ecology and external morphology within the subfamily, shape variation of the feeding apparatus was modest, indicating a similar mode of feeding across the subfamily. All 10 species were similar in their pattern of skull asymmetry, but interestingly, two species using narrowband high frequency clicks (La. cruciger and C. hectori) were among the most asymmetric species, contradicting previous interpretations of odontocete skull asymmetry. J. Morphol. 277:776–785, 2016. © 2016 Wiley Periodicals, Inc.     

Interspecific variation of ontogeny and skull shape among porpoises (Phocoenidae)

All extant members of Phocoenidae (porpoises) have been characterized as pedomorphic based on skeletal characters. To investigate the ontogenetic background for pedomorphosis and assess interspecific differences in ontogeny among phocoenids, samples of the six extant species were compared in terms of development of both epiphyseal and cranial suture fusion. Across all species, full maturity of the vertebral column was rare. Vertebral epiphyseal development did not progress so far in most Phocoena phocoena as in Phocoenoides dalli and Phocoena dioptrica. P. phocoena, Phocoena spinipinnis, Ph. dalli, and P. dioptrica, for which large series were available, were further compared in terms of ontogeny of cranial shape by three‐dimensional geometric morphometrics. Ph. dalli and P. dioptrica generally showed further development of cranial sutures than the other species. Postnatal skull shape development was similar for all species studied; the majority of interspecific shape differences are present at parturition. Smaller species had a higher rate of shape development relative to growth in size than Ph. dalli and P. dioptrica, but they still showed less allometric development due to less postnatal growth. Interspecific shape differences indicate phylogenetic relationships similar to that proposed based on morphology or convergent evolution of the two pelagic species, Ph. dalli and P. dioptrica, under the scenarios suggested by recent molecular studies. A shape trend coinciding with habitat preference was detected; in species with pelagic preference the position and orientation of the foramen magnum aligned the skull with the vertebral column; the rostrum showed less ventral inclination, and the facial region was larger and more concave in lateral aspect. J. Morphol., 2011. © 2010 Wiley‐Liss, Inc.     

Ontogenetic development and sexual dimorphism of franciscana dolphin skull: A 3D geometric morphometric approach

The aim of this work was to study the postnatal ontogenetic development of Pontoporia blainvillei skull, identifying major changes on shape, and relating them to relevant factors in the life history of the species. We analyzed a complete ontogenetic series (73♂, 83♀) with three‐dimensional geometric morphometric techniques. Immature dolphins showed a very well‐developed braincase and a poorly developed rostrum, and the principal postnatal changes affected the rostrum and the temporal fossa, both structures implied functionally to the feeding apparatus, thus suggesting a specialized mode for catch fast prey in P. blainvillei. Osseous elements associated with sound production were already well developed on immature dolphins, suggesting the importance of this apparatus since the beginning of postnatal life. Sexual dimorphism was detected on both shape and size variables. Females were bigger than males, in accordance with previous studies. Shape differences between sexes were found on the posterior part of premaxillaries and external bony nares (P < 0.01), suggesting that this sexual dimorphism is related to differences on vocalization capabilities. J. Morphol. 275:1366–1375, 2014. © 2014 Wiley Periodicals, Inc.     

A complete survey of normal pores on a smooth shell ostracod (Crustacea): Landmark‐based versus outline geometric morphometrics

Pores and sensilla on ostracod shell have often been used in studies of ontogeny, taxonomy, and phylogeny of the group. However, an analysis of sexual dimorphism and variation between valves in the number and distribution of pores is lacking. Also, such studies have never been done on a widely distributed, morphologically variable, and weakly ornamented freshwater ostracod. Here, we survey pores in one such species, Physocypria kraepelini . We choose 27 homologous pores as landmarks for 2D‐geometric morphometric analysis, with the aim to assess intersexual and between valves variation in size and shape relative to the Fourier outline analysis. This species has only simple (Type A) pores with and without a lip, and each pore carries an undivided sensory seta. Our results show that the total number of pores varies (from 270 to 296), but this is not associated with a specific valve. Males carry fewer pores than females, however no sex specific pores are found. Small intrapopulation divergence of the Cyt b molecular marker (1%) indicates that morphological variability is not species related. We found that P. kraepelini exhibits directional asymmetry of size and shape, sexual size dimorphism (SSD) but lacks sexual shape dimorphism (SShD). Two geometric morphometrics methods were congruent in the estimation of SSD, SShD, and directional asymmetry of shape but differ in the statistical evaluation of directional asymmetry of size. Contrary to other animal groups, our study suggests that ostracods have more pronounced directional asymmetry of shape compared to directional asymmetry of size.     

Measuring and evaluating morphological asymmetry in fish: distinct lateral dimorphism in the jaws of scale‐eating cichlids

The left–right asymmetry of scale‐eating Tanganyikan cichlids is described as a unilateral topographical shift of the quadratomandibular joints. This morphological laterality has a genetic basis and has therefore been used as a model for studying negative frequency‐dependent selection and the resulting oscillation in frequencies of two genotypes, lefty and righty, in a population. This study aims were to confirm this laterality in Perissodus microlepis Boulenger and P. straeleni (Poll) and evaluate an appropriate method for measuring and testing the asymmetry. Left–right differences in the height of the mandible posterior ends (HMPE) and the angle between the neurocranium and vertebrae of P. microlepis and P. straeleni were measured on skeletal specimens. Snout‐bending angle was also measured using a dorsal image of the same individuals following a previous method. To define which distribution model, fluctuating asymmetry (FA), directional asymmetry (DA), or antisymmetry (AS), best fit to the lateral asymmetry of the traits, we provided an R package, IASD. As a result, HMPE and neurocranium–vertebrae angle of both species were best fitted to AS, suggesting that P. microlepis and P. straeleni showed a distinct dimorphism in these traits, although snout‐bending angle of P. microlepis was best fitted to FA. Measurement error was low for HMPE comparing the snout‐bending angle in P. microlepis, indicating that measuring HMPE is a more accurate method. The scale‐eating tribe Perissodini showed distinct antisymmetry in the jaw skeleton and neurocranium–vertebrae angle, and this laterality remains a valid marker for further evolutionary studies.     

Timing of ontogenetic changes of two cranial regions in Sotalia guianensis (Delphinidae)

Despite the fact that heterochronic processes seem to be an important process determining morphological evolution of the delphinid skull, previous workers have not found allometric scaling as relevant factor in the differentiation within the genus Sotalia. Here we analyzed the skull ontogeny of the estuarine dolphin S. guianensis and investigate differential growth and shape changes of two cranial regions – the neurocranium and the face – in order to evaluate the relevance of cranial compartmentalization on the ontogeny of this structure. Our results show that, even though both cranial regions stop growing at adulthood, the face has higher initial growth rates than the neurocranium. The rate of shape changes is also different for both regions, with the face showing a initially higher, but rapidly decreasing rate of change, while the neurocranium shows a slow decreasing rate, leading to persistent and localized shape changes throughout adult life, a pattern that could be related to epigenetic regional factors. The pattern of ontogenetic shape change described here is similar to those described for other groups of Delphinidae and also match intra and interspecific variation found within the family, suggesting that mosaic heterochrony could be an important factor in the morphological evolution of this group.     

Analysis of asymmetries in the African fruit bats Eidolon helvum and Rousettus egyptiacus (Mammalia: Megachiroptera) from the islands of the Gulf of Guinea. I. Variance and size components of bilateral variation

A set of cranial characters was examined in the fruit bats Rousettus egyptiacus and Eidolon helvum to compare trends and relative importance of major components of bilateral morphometric variation, and their relationship with character size. Using two‐way, sides‐by‐individuals ANOVA , four components of variation were estimated for each bilateral variable: individual variation (I), directional asymmetry (DA), non‐directional asymmetry (NDA) and measurement error (E). Both species exhibit similar major trends of variation in asymmetry across characters, as shown by principal component analysis, using variance components as variables. Degree of interspecific congruence among characters was confirmed by a two‐way ANOVA with species and variance components as fixed factors. Congruence of asymmetry patterns between species suggests that the concept of population asymmetry parameter (PAP) could be extended to higher hierarchies. PAPs above the species level may result from common mechanisms or similar developmental constraints acting on species’ buffering capacities and morphological integration processes.     

Morphology of the vertebral centra in dolphins from the southwestern South Atlantic: A 3D morphometric approach and functional implications

In dolphins, centrum shape is one of the features that allows determination of stable and flexible regions in the vertebral column. The Commerson's (Cephalorhynchus commersonii; n = 37), Peale's (Lagenorhynchus australis; n = 24), dusky (Lagenorhynchus obscurus; n = 29), and hourglass dolphins (Lagenorhynchus cruciger; n = 10) are closely related species inhabiting the Southern Hemisphere that have diverse prey and habitat preferences. We applied 3D geometric morphometrics to describe differences in centrum shape along the vertebral columns of these species, and hypothesize how these differences may affect swimming. On each column, we chose a maximum of eight vertebrae and digitized 18 landmarks on each centrum with a Microscribe G2X. We explored shape differences amongst regions employing principal components analyses and computing Mahalanobis distances. We describe differences in centrum shape in relation to functional regions and among species; and analyze shape changes in relation to particular biomechanical requirements. The species studied here may be partially sympatric in the Southern Hemisphere, but they have important differences in foraging ecology and habitat preferences that could be related to differences in centrum shape along the vertebral column.     

Growth of cranial synchondroses and sutures requires polycystin-1

In vertebrates, coordinated embryonic and postnatal growth of the craniofacial bones and the skull base is essential during the expansion of the rostrum and the brain. Identification of molecules that regulate skull growth is important for understanding the nature of craniofacial defects and for development of non-invasive biologically based diagnostics and therapies.Here we report on spatially restricted growth defects at the skull base and in craniofacial sutures of mice deficient for polycystin-1 (Pkd1). Mutant animals reveal a premature closure of both presphenoid and sphenooccipital synchondroses at the cranial base. Furthermore, knockout mice lacking Pkd1 in neural crest cells are characterized by impaired postnatal growth at the osteogenic fronts in craniofacial sutures that are subjected to tensile forces. Our data suggest that polycystin-1 is required for proliferation of subpopulations of cranial osteochondroprogenitor cells of both mesodermal and neural crest origin during skull growth. However, the Erk1/2 signalling pathway is up-regulated in the Pkd1-deficient skeletal tissue, similarly to that previously reported for polycystic kidney.     

Early development of the chondrocranium in Salmo letnica(Karaman, 1924)(Teleostei: Salmonidae)

The ontogenetic development of the chondrocranium of Ohrid trout Salmo letnica was studied from hatching until 92 days post‐hatching (dph). Most of the samples were in toto trypsin cleared and stained, some specimens were used for serial histological sectioning. The serial histological sections of fish specimens at the age of 92 dph were used for a graphical reconstruction of the cartilaginous neurocranium. A chronological evaluation of the formation of the cartilaginous skull in the early development of S. letnica was performed. In order to investigate to what degree the ontogeny of the Ohrid trout is unique, the results were compared with data of the development of other salmonids, as well as some non‐salmonid teleosts. The development of the cartilaginous structures of the Ohrid trout was found to be similar to that of other salmonids. Most of the cartilage structures of the neurocranium and the viscerocranium are present at the moment of hatching of this species. A fully developed chondrocranium was observed at the age of 92 dph, when the first signs of cartilage resorption could also be observed.     

Evolutionary development of the neurocranium in Dissorophoidea (Tetrapoda: Temnospondyli), an integrative approach

SUMMARY Ontogenetic data can play a prominent role in addressing questions in tetrapod evolution, but such evidence from the fossil record is often incompletely considered because it is limited to initiation of ossification, or allometric changes with increasing size. In the present study, specimens of a new species of an archaic amphibian (280 Myr old), Acheloma n. sp., a member of the temnospondyl superfamily Dissorophoidea and the sister group to Amphibamidae, which is thought to include at least two of our modern amphibian clades, anurans and caudatans (Batrachia), provides us with new developmental data. We identify five ontogenetic events, enabling us to construct a partial ontogenetic trajectory (integration of developmental and transformation sequence data) related to the relative timing of completion of neurocranial structures. Comparison of the adult amphibamid morphology with this partial ontogeny identifies a heterochronic event that occurred within the neurocranium at some point in time between the two taxa, which is consistent with the predictions of miniaturization in amphibamids, providing the first insights into the influence of miniaturization on the neurocranium in a fossil tetrapod group. This study refines hypotheses of large‐scale evolutionary trends within Dissorophoidea that may have facilitated the radiation of amphibamids and, projected forward, the origin of the generalized batrachian skull. Most importantly, this study highlights the importance of integrating developmental and transformation sequence data, instead of onset of ossification alone, into investigations of major events in tetrapod evolution using evidence provided by the fossil record, and highlights the value of even highly incomplete growth series comprised of relatively late‐stage individuals.     

Post-weaning cranial ontogeny in two bandicoots (Mammalia,Peramelomorphia, Peramelidae) and comparison with carnivorous marsupials

The ontogeny of the skull has been studied in several marsupial groups such as didelphids, microbiotheriids, and dasyurids. Here, we describe and compare the post-weaning ontogeny of the skull in two species of bandicoots, Echymipera kalubu (Echymiperinae) and Isoodon macrourus (Peramelinae), analyzing specific allometric trends in both groups, describing common (and specific) patterns, and discussing them on functional and phylogenetic grounds. Growth patterns were analyzed both qualitatively and quantitatively, including bivariate and multivariate analyses of allometry. We also evaluated character transformation and phylogenetic signals of the allometric patterns in several groups of marsupials and some placentals. We identified morphological changes between juvenile and adult stages in both species of peramelids, many related to the development of the trophic apparatus. Notable differences were detected in the patterns of growth, suggesting divergences in ontogenetic trajectories between both species. Both bivariate and multivariate methods indicate that positive allometries in E. kalubu apply to longitudinal dimensions, whereas in I. macrourus, positive allometries are restricted to vertical dimensions of the skull. The comparison of the allometric trends of two bandicoots with previously studied taxa reveals that although peramelids exhibit a particularly short gestation period and divergent morphology compared to other marsupials, their pattern does not show any particular trend. Some allometric trends seem to be highly conserved among the species studied, showing weak phylogenetic signal. Marsupials in general do not show particular patterns of post-weaning skull growth compared with placentals.     

A quantitative approach to the cranial ontogeny of the puma

The cranial ontogeny of specialized mammals is relevant to the understanding of the connection of form and function in a developmental, ecological, and evolutionary context. As highly specialized carnivores, felids are of especial interest. We studied the postnatal ontogeny of the skull in Puma concolor (Mammalia: Carnivora: Felidae) using a quantitative approach. We interpreted our results in the light of a previous qualitative assessment of ontogenetic changes in the species. This represents one of the few integrative studies of skull development in any extant species of wild felids. We report patterns of multivariate allometry of 19 linear skull dimensions measured in 48 Argentine specimens. We examined the (jackknife resampled) departures from isometry as well as the interplay of isometric and allometric trends in shaping the puma skull. Both the qualitative and quantitative results indicate that the major ontogenetic changes are directly linked to cranial structures that support a developing masticatory apparatus and its associated jaw and neck musculature, which are essential for the action of canines and carnassials during the killing bite and slicing flesh. Sexual differences suggest allometric scaling (hypo- or hyper-morphosis) as key processes in the development of the puma skull.     

Morphometric variation of the skull during postnatal development in the Lowland European bisonBison bonasus bonasus

We studied the variation of linear measurements and skull capacity in Lowland European bisonBison bonasus bonasus (Linnaeus, 1758) during postnatal development, and the dependencies of the parameters in relation to sex, age, and body mass of the animals. Material consisted of 599 bison skulls (310 males and 289 females), within the age range of 1 month to 21 years (males) and to 27 years (females). In the group of calves to 1 year old, no sex connected differences in skull measurements were observed, whereas the skull capacity in older calves was significantly larger (0.01>p>0.001) in males than in females. From the third year of life, most skull measurements display characteristics of sexual dimorphism. Skull development in both sexes is most intensive during the first three years of life, and slows from the age of 5. In older individuals of both sexes (≥ 6 years), orbital breadth continues growing and, in females, breadth of splanchnocranium continues increasing. Growth in a bison’s skull capacity is most intensive up to the third year of life and slows from the age of 5. During postnatal development, a bison skull grows proportionally except the neurocranium, which grows slightly slower in comparison with basal length and its development finishes earlier than that of splanchnocranium. In ontogenesis, a bison skull grows much slower compared to body mass. In relation to body mass, skull capacity and the height of neurocranium grow most slowly while orbital breadth grows most intensively. The results obtained were compared with data on skull sizes of bison born in 1930–1950 and bred in captivity and with skulls of the American bisonBison bison. Inbreeding is probably responsible for some types of phenotypic abnormalities in the skull which appear in modern European bison.     

Cranial ontogeny in the Puma lineage,Puma concolor,Herpailurus yagouaroundi,and Acinonyx jubatus (Carnivora: Felidae): a three‐dimensional geometric morphometric approach

The Puma lineage is a monophyletic group that includes three living species: Puma concolor, Herpailurus yagouaroundi, and Acinonyx jubatus. It has been analysed from ecological and taxonomic perspectives, but their cranial ontogeny has been poorly studied. In this study, we assessed the cranial shape and size variation through three‐dimensional geometric morphometric techniques, and explored the acquisition of definitive shape and size in relation to key life‐history events. Each species occupied different locations in the shape morphospace: A. jubatus and P. concolor showed shorter and wider skulls, with more expanded zygomatic arches, than H. yagouaroundi, which presented the most divergent pattern of change. Ontogeny was more similar between P. concolor and A. jubatus than between the closely related P. concolor and H. yagouaroundi. The evolution of ontogenetic change in the lineage seems to be more influenced by size. Changes detected between juvenile and adult skulls enhanced predatory skills, coincident with the change from a diet of milk to a carnivorous diet. Change patterns suggest that the skull is not morphologically conservative in the lineage, in contrast with other carnivores such as canids and hyaenids. The enlargement of the rostrum observed in some canids and the reinforcement of the bite mechanism of hyaenids were not detected in this group. © 2013 The Linnean Society of London     

Sexual dimorphism in the skull of the European mink<Emphasis Type="Italic">Mustela lutreola</Emphasis> from NW part of Russia

Morphometric variation in 22 characters of 86 skulls of the European minkMustela lutreola (Linnaeus, 1761), from the NW part of Russia, has been analysed. Stepwise discriminant analysis was used to estimate craniometric variables for sex determinations. Two characters (zygomatic breadth and interorbital width) are enough for the 96.5% correct classification. The male skull ofM. lutreola is characterised by a relatively high neurocranium, widely arranged zygomatic arches, a wide rostrum, and by wider auditory bullae and higher mandibles. Sexual size dimorphism ofM. lutreola is less than that of other similar-sized mustelids —Mustela putorius, M. eversmanii, M. sibirica, Neovison vison. The results are discussed in relation to the existing theories on sexual dimorphism in mustelids.     

Climate and morphological change on decadal scales: Multiannual variation in the common shrew <Emphasis Type="Italic">Sorex araneus</Emphasis> in northeast Russia

Multiannual variation is one of several types of species morphological variability, one that is directly related to ecophenotypic and evolutionary responses to changing environments. The morphology of small mammal populations can change quickly because generation length is short, usually one year, and individual lifespans are often only a year or two. We studied the response of skull and mandible morphology in the common shrew Sorex araneus Linnaeus, 1758 to nine climate factors related to snow cover, temperature and precipitation at a study site near Syktyvkar, Russia through the period 1976 to 2003. We found that these multivariate phenotypes changed significantly from year to year, though there were no clear directional trends in the change. The phenotype itself was closely associated with the range of annual temperature and winter precipitation. Changes in summer temperatures and precipitation seem to drive change in size-related phenotypes, whereas changes in snow cover and winter temperature seem to drive change in shape.     

Can habitat characteristics shape vertebral morphology in dolphins? An example of two phylogenetically related species from southern South America

Fast swimming pelagic cetacean species have osteological characteristics that promote a more stable spine in comparison to that of coastal species. The Peale's dolphin (Lagenorhynchus australis) and the hourglass dolphin (Lagenorhynchus cruciger) have a close phylogenetic relationship and are found in coastal and pelagic waters in the Southern Hemisphere, respectively. The aim of this work was to study the relationship between the vertebral column's morphology and its flexibility, across these species of contrasting habitats. Vertebral counts and multiple measurements of each vertebra were used to infer intervertebral flexibility. Bivariate plots and discriminant multivariate analyses were employed to compare each functional region along the vertebral column. Both species displayed a regionalization of the column into three stable regions and two flexible areas, which statistically differ in the proportion of the skeleton occupied in each species. While the Peale's dolphin has rounder vertebrae, associated with higher flexibility, the hourglass dolphin has disk‐shaped vertebrae and strongly inclined processes related to high stability. Although the species are closely related phylogenetically, vertebral morphology is influenced by a diverse set of ecological and behavioral factors, reflecting a high degree of vertebral plasticity within the genus.     

Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees

Facial heights, i.e. the vertical distances between the superior and inferior limits of facial compartments, contribute to the orientation of the viscerocranium in the primate skull. In humans, vertical facial variation is among the main sources of diversity and frequently associated with an integrated suite of other cranio-mandibular traits. Facial heights and kyphosis are also important factors in interspecific variation and models of hominoid evolution. The ontogenetic determination of adult facial orientation and its relation to phylogenetic variation are unclear, but crucial in all previously mentioned respects. We addressed these issues in a sample of 175 humans and chimpanzees with Procrustes based geometric morphometrics, testing hypotheses of interspecific similarity in postnatal ontogenetic trajectories, early versus later ontogenetic facial pattern determination, and a developmental model of morphological integration. We analyzed the contribution of postnatal morphogenesis to adult vertical facial variation by partitioning morphological variation into a portion of pure growth allometry and a non-allometric fraction. A statistically significant difference of growth-allometries revealed that in both species growth established the adult skull proportions by vertical facial expansion, but while in chimpanzees the complete viscerocranium showed reorientation, in humans only the lower face was modified. In both species the results support a hypothesis of early facial pattern determination. A coincident emergence of morphological traits favors a hypothesis of developmental integration of the face, excluding traits of the basi- and neurocranium. Interspecific differences in integration may have implications for evolutionary studies. The present findings indicate that growth establishes the adult skull proportions and integrates principal facial orientation patterns, already there in early postnatal ontogeny.