Morphospace occupation in thalattosuchian crocodylomorphs: skull shape variation, species delineation and temporal patterns

Abstract: Skull shape variation in thalattosuchians is examined using geometric morphometric techniques in order to delineate species, especially with respect to the classification of Callovian species, and to explore patterns of disparity during their evolutionary history. The pattern of morphological diversity in thalattosuchian skulls was found to be very similar to modern crocodilians: the main sources of variation are the length and the width of the snout, but these broad changes are correlated with size of supratemporal fenestra and frontal bone, length of the nasal bone, size of the orbit and premaxilla and position of the narial opening. Patterns of shape variation, in combination with discrete‐state morphology and stratigraphic and geographic range data were used to distinguish nine species of teleosaurid and 14 species of metriorhynchid, with the four currently recognized Callovian species being split into eight. Metriorhynchids were found to be more disparate from the average shape of morphospace than teleosaurids. However, short‐snouted metriorhynchids and long‐snouted teleosaurids showed the greatest amount of disparity with respect to snout morphotypes, indicating that each group tended to explore opposite areas of morphospace. Phylogeny was found to have a moderate influence on the pattern of morphospace occupation in metriorhynchids, but little effect in teleosaurids suggesting that other factors or constraints control the pattern of skull shape variation in thalattosuchians. A comparison of thalattosuchians with dyrosaur/pholidosaurids shows that thalattosuchians have a unique skull morphology, implying that there are multiple ways to construct a ‘long snout’. Moreover, the skull geometry of the problematic species Pelagosaurus typus was found to converge on the teleosaurid area of morphospace. Finally, the temporal distribution of thalattosuchian species and morphotypes demonstrate a clear and highly correlated relationship with sea level curves and mass extinction events through the Jurassic and the Early Cretaceous.     

Evolutionary trends on extant cat skull morphology (Carnivora: Felidae): a three‐dimensional geometrical approach

The skulls of 33 extant cat species were characterized through three‐dimensional geometric morphometrics using 20 landmarks. A principal component analysis (PCA) was performed with Procrustes fitted coordinates, and the PC‐scores were phylogenetically corrected by independent contrasts method. Three PCs allowed for the definition of five cat skull patterns. PC1: ‘snouted/massive‐headed cats’ (genus Panthera) opposing the ‘round‐headed small cats’ (genus Oncifelis, Prionailurus rubiginosus, Prionailurus bengalensis, among other small cats); PC2: ‘tapering‐headed cats’ (Neofelis nebulosa, Herpailurus yagouaroundi, Prionailurus planiceps) opposing the ‘stout‐headed cats’ (Acinonyx jubatus, Uncia uncia, Otocolobus manul, Felis margarita, and Felis nigripes); and PC3: ‘low profiled‐headed cats’ (mostly, Pr. planiceps). A sixth pattern, the ‘generalized skull’, observed in the Caracal lineage, genus Lynx, Leopardus pardalis, and Catopuma temminckii, indicates a morphological convergence among midsized‐cats. The morphological trends ‘snouted/massive’ and ‘round’ clearly denote a co‐evolution between size and shape. The other skull patterns evolved unrelatedly to the size (i.e. their allometric variations are not a size function). Nevertheless, each species comprises an amalgam of these patterns, so the influence of the size permeates, in some extent, the skull morphology along all cat lineages. The felid ecomorphological fit to hypercarnivory is obvious; however, different skull shapes in same‐sized species with similar habits, indicate that the variation in the skull morphology may result from phenotypic fluctuations, whose adaptive value (if indeed there is any) is still obscure. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 176–190.     

Microevolutionary patterns in the common caiman predict macroevolutionary trends across extant crocodilians

Both extinct and extant crocodilians have repeatedly diversified in skull shape along a continuum, from narrow‐snouted to broad‐snouted phenotypes. These patterns occur with striking regularity, although it is currently unknown whether these trends also apply to microevolutionary divergence during population differentiation or the early stages of speciation. Assessing patterns of intraspecific variation within a single taxon can potentially provide insight into the processes of macroevolutionary differentiation. For example, high levels of intraspecific variation along a narrow‐broad axis would be consistent with the view that cranial shapes can show predictable patterns of differentiation on relatively short timescales, and potentially scale up to explain broader macroevolutionary patterns. In the present study, we use geometric morphometric methods to characterize intraspecific cranial shape variation among groups within a single, widely distributed clade, Caiman crocodilus. We show that C. crocodilus skulls vary along a narrow/broad‐snouted continuum, with different subspecies strongly clustered at distinct ends of the continuum. We quantitatively compare these microevolutionary trends with patterns of diversity at macroevolutionary scales (among all extant crocodilians). We find that morphological differences among the subspecies of C. crocodilus parallel the patterns of morphological differentiation across extant crocodilians, with the primary axes of morphological diversity being highly correlated across the two scales. We find intraspecific cranial shape variation within C. crocodilus to span variation characterized by more than half of living species. We show the main axis of intraspecific phenotypic variation to align with the principal direction of macroevolutionary diversification in crocodilian cranial shape, suggesting that mechanisms of microevolutionary divergence within species may also explain broader patterns of diversification at higher taxonomic levels.     

The evolutionary improbability of ‘generalism’ in nature,with special reference to insects

In addition to feeding, many vertebrates use their skulls for other functions that are highly relevant to fitness. One such function is roost excavation by the bat Lophostoma silvicolum. Males of this species use their canines to create cavities inside active termite nests, which are significantly harder than the prey they eat. Here we investigate whether the skull of L. silvicolum is specialized for roost excavation relative to the ecologically similar species Tonatia saurophila and Micronycteris hirsuta, which do not excavate roosts. We conducted a finite element analysis that simulated roost excavating and feeding behaviours. These analyses were informed by our observations of feeding and roost‐excavating behaviours, bite force, and dissections of the cranial musculature of the three bat species. During the simulation of roost excavation (bilateral canine biting), our data indicate that most regions of the skull of L. silvicolum exhibit less stress than those of T. saurophila and M. hirsuta; however, the latter exhibited the lowest peak stress at the zygomatic arches. During loads that simulate feeding (bilateral molar biting), the three species exhibit similar stress levels. It is not clear whether L. silvicolum has a skull shape that is stronger under the loads imposed by excavation, but it does exhibit relatively higher bilateral canine bite forces that are generated via relatively larger temporalis muscles. Based on the muscle data, our study suggests that the feeding apparatus of mammals can exhibit performance and morphological adaptations to functions other than feeding. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 1–10.     

Squalus bassi sp. nov., a new long‐snouted spurdog (Chondrichthyes: Squaliformes: Squalidae) from the Agulhas Bank

The long‐snouted African spurdog Squalus bassi sp. nov. is described based on material collected from the outer shelf and upper continental slope off South Africa and Mozambique. Squalus bassi shares with S. mitsukurii, S. montalbani, S. chloroculus, S. grahami, S. griffini, S. edmundsi, S. quasimodo and S. lobularis a large snout with prenarial length greater than distance between nostrils and upper labial furrows, dermal denticles tricuspidate and rhomboid and elevated number of vertebrae. Squalus bassi can be distinguished from all its congeners by a combination of body and fin colouration, external morphometrics, vertebral counts and shape of dermal denticles. Similar long‐snouted congeners from the Indo‐Pacific region, including S. montalbani, S. edmundsi and S. lalannei are compared in detail with the new species. This new species has been misidentified as the Japanese S. mitsukurii and the Mediterranean S. blainvillei due to the lack of comparative morphological analyses. The validity of the nominal species S. mitsukurii in the south‐eastern Atlantic Ocean and western Indian Ocean is also clarified herein, indicating it has a more restricted geographical distribution in the North Pacific Ocean.     

Skull morphology and functionality of extant Felidae (Mammalia: Carnivora): a phylogenetic and evolutionary perspective

Felids morphology and ecological role as hypercarnivores are quite constant, despite considerable body size variation among species. Skull morphological and functional features of 34 extant cat species were evaluated under a phylogenetic framework of the Felidae. Twenty skull measurements were analysed through Principal Component Analysis to assess the species morphofunctional spaces. Force indexes were obtained from static equilibrium equations to infer jaw mechanics. Correlations between morphological, functional, and ecological traits were tested by phylogenetically independent contrasts. In spite of the general cat‐like pattern, specific features on the skulls allowed differentiation among groups. Acinonyx jubatus, for instance, showed a shorter and shallower temporal fossa than other big cats, and their bite functionality is marked by an increased contribution of the masseteric system. A morphofunctional dichotomy between Neotropical and Eurasian/African small cats was detected, and is associated with the major transversal axes of the skulls. According to the contrast analyses, the skull size is correlated with the bite force and prey size, but it is uncorrelated with the variations on jaw mechanics (from temporalis or masseter muscle optimizations). Also, there was no correlation between functional differences on jaw muscles and the ratio of prey weight to cat weight. The efficiency of the jaw apparatus among cats is quite consistent; therefore, the different evolutionary trends of jaw mechanics seem to be caused by the casuistic fixation of phenotypical variations, rather than by specific adaptative selections. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161 , 414–462.     

A NEW METRIORHYNCHID CROCODILIAN (MESOEUCROCODYLIA: THALATTOSUCHIA) FROM THE KIMMERIDGIAN (UPPER JURASSIC) OF WILTSHIRE,UK

Abstract: Recent revision of the marine metriorhynchid crocodilians indicates that a partial skull previously assigned to the species Metriorhynchus superciliosus and newly discovered postcranial elements from the Kimmeridge Clay of Westbury, Wiltshire belong to a new species of metriorhynchid. This material is herein described and referred to a new species of the genus Dakosaurus, characterised by four apomorphies: the size and shape of the enlarged supratemporal fossae; relatively large teeth, and half the number in relatives; the robust and unornamented cranium; and the angle that the prefrontal makes with the long axis of the skull. In a new phylogenetic analysis, Dakosaurus carpenteri sp. nov. is the basal member of a clade containing also D. maximus and D. andiniensis: it is not so short‐snouted and its teeth are not so few and large as in the other two species, but the new form illustrates the ecological transition among metriorhynchids from a piscivorous diet to high‐order carnivory.     

Cranial morphology of the California vole (Microtus californicus,Cricetidae) in a contact zone

Zones of contact between divergent biological forms within or between species are critical to the study of speciation. How characters flow across contact zones can be informative of the speciation process. To better understand this phenomenon in a mammal, we investigated cranial shape change in a contact zone between northern and southern phylogeographical groups of California voles (Microtus californicus). We took 12 linear measurements of skulls, one measurement of the mandible, and coded the presence and absence of two skull foramina for 427 specimens. In multivariate analyses, skulls within parental regions were correctly assigned more than 90% of the time. In the contact zone, 49% were classified as northern and 51% as southern, with a bimodal distribution of posterior probability values. Foraminal patterns in the contact zone were intermediate between northern and southern regions. A cline analysis for coastal populations suggested a similar centre for mitochondrial and nuclear markers, although a centre for the morphological data was offset. Cranial morphology indicates an intermediate area with overlap between the two regions, as suggested by the molecular data, with a pattern distinct from mitochondrial DNA or nuclear DNA markers. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 264–283.     

The genus Teliocrinus (Crinoidea,Echinodermata): a key taxon among pentacrinid stalked crinoids

The main characters of the stalked crinoids of the family Pentacrinitidae attributed to the genus Teliocrinus are re‐evaluated from a quantitative study of phenotype variation, new observations on arm and stalk articulations, and observation of ontogenetic trends. All of the specimens collected in the northern Indian Ocean belong to the same species, i.e. Teliocrinus springeri (Clark, 1909). However, two phenotypes living at different depths remain valid as subspecies: Teliocrinus springeri springeri (Clark, 1909) and Teliocrinus springeri liliaceus (Clark, 1909). Teliocrinus shares several ontogenetic trends with Endoxocrinus, especially in nonfunctional brachial articulations and stalk symplexies. Its assignment to the Diplocrininae is confirmed. A discussion of its affinities with pentacrinid fossil genera in which the crown is well preserved suggests that Diplocrininae could have first appeared during the Lower Cretaceous. A shortening of brachitaxes and a paedomorphic trend of stalk symplexies are the main other evolutionary traits. Nonfunctional articulations are frequently found at the paedomorphic pole of the heterochronic gradient, without clear derived characters. Classification of pentacrinids mainly based on such symplesiomorphy or paedomorphic characters must be definitively abandoned. However, in post‐Palaeozoic stalked crinoids the scarcity of well‐preserved fossils, the high frequency of paedomorphy, and convergent adaptive characters makes phylogenetic reconstruction only based on morphological characters very difficult and speculative. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 22–39.     

Pollination systems in pioneer trees of the genus Macaranga (Euphorbiaceae) in Malaysian rainforests

Many species of Macaranga (Euphorbiacae) are fast‐growing pioneer trees with an important role in early succession in south‐east Asian rainforests. Within the genus, diverse types of ant–plant associations exist and it has therefore been a model system for studying mutualistic interactions. Little information existed up to now, however, on its reproductive biology. Our comparative study in the genus Macaranga in Sundaland revealed specific flower characteristics and uncommon brood‐site pollination systems: enclosed inflorescence morphologies with narrow entrances strongly restrict the set of flower visitors in many species. Thysanoptera were the most abundant insects in 20 of the 26 investigated Macaranga species and, in three species, heteropteran adults and larvae were dominant. Both insect groups used the flower chambers as breeding sites and fed on nectar‐producing trichomes inside the bracteoles. Thrips as well as heteropterans are assumed to contribute to pollination. Different Macaranga sections were associated with different flower visitors, suggesting isolation by different pollinators. Thrips pollination and myrmecophyty often occurred in the same sections. The development of enclosed flowers might have facilitated tight ant–plant interactions and prevent ant–pollinator conflicts. However, the complex ecosystems in which the mutualistic systems evolved are rapidly changed with unknown consequences for these specific interactions. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 935–953.     

The influence of environmental factors on the morphology of red‐backed voles Myodes gapperi (Rodentia,Arvicolinae) in Québec and western Labrador

Geographical patterns of morphological variation in small mammals are often associated with environmental factors. The southern red‐backed vole Myodes gapperi is a widespread and abundant small mammal in Canada, occurring in environments as diverse as mixed‐wood forests and taiga. First upper molars and skulls from nine populations of southern red‐backed voles distributed across three ecozones and approximately 10° of latitude were analysed by means of geometric morphometric techniques, and their relationships with environmental variables were examined. A weak, non‐linear trend of size increase towards higher latitudes was observed in voles' skulls. Environmental variables appeared to be important drivers of shape differentiation among populations from the three distinct ecozones analysed. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 204–218.     

The impact of population bottlenecks on fluctuating asymmetry and morphological variance in two separate populations of reindeer on the island of South Georgia

In the early part of the 20^th century, whalers on South Georgia in the South Atlantic transported reindeer from Norway to establish a population from which they could cull animals for food. This happened twice, with reindeer obtained from the same source in each case, and with independent founder populations being established on separate parts of the island. As the exact number of founding males and females are known in each case, and as it was possible to obtain materials from the source population, this provided an unusually clear test of expectations about the impact of population bottlenecks on morphological and genetic diversity. In this study, we focus on the impact on morphological variation and on the relationship between genomic stress and indirect measures of fitness. We find that fluctuating asymmetry and morphological variation increased in each bottlenecked population and that the impact was somewhat stronger for the founder group that began with fewer females. Based on several skull measurements, there was also a significant trend for the reindeer in the bottlenecked populations to have smaller skulls. There were consistent correlations between individual genetic diversity and indirect measures of fitness, but these were weak and non‐significant after correction for type 1 error. Taken together, these data support the expectation that genomic stress has the potential to impact the expression of morphological phenotype in a large mammal and provide an opportunity to directly compare two parallel events. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 798–811.     

Sexual dimorphism in head structures of the weevil Rhopalapion longirostre (Olivier 1807) (Coleoptera: Curculionoidea): a response to ecological demands of egg deposition

Extreme sexually dimorphic phenotypes are frequently attributed to strong sexual selection but they can also arise as a consequence of different ecological demands. The evolutionary emergence of elongated rostra was a key event in the adaptive radiation of weevils. Exaggerated female rostra evolved in numerous weevil taxa, enabling females to bore long channels for egg deposition into various parts of host plants. The investigated ecological scenario involves three species of brentid weevils, all associated with the same host plant, Alcea rosea. The present study reveals that: (1) Rhopalapion longirostre bores egg channels into the buds, and the female rostrum is twice as long and its surface is smoother than in the male; (2) Alocentron curvirostre and Aspidapion validum live on the same host plant but use the stems for egg deposition; in these species, female rostra are not exaggerated; (3) the females of all three species possess a stronger mandible musculature than males; (4) the elongated female snout of R. longirostre is a response to the requirements of boring egg channels of maximal depth into the buds of the host plant; and (5) female muscle strength is an adaptation to boring into hard plant tissues, irrespective of rostrum length. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 642–660.     

Cranial shape variation and molecular phylogenetic structure of crested newts (Triturus cristatus superspecies: Caudata,Salamandridae) in the Balkans

In the present study, we investigated the degree of congruence between phylogeny, as inferred from mitochondrial (mt)DNA sequences, and cranium shape variation of crested newts (Triturus cristatus superspecies) in the Balkans. These newts belong to four phylogenetic clades defined by mtDNA analysis, and significantly differed in cranial shape. Allometry explained a high percentage of shape variation in crested newts. The clade‐specific allometric slopes significantly diverged for both the ventral cranium and dorsal cranium, indicating that differences in shape between clades could not be a simple consequence of their difference in size. The analysis of hierarchical and spatial variation showed similarity in the patterns of global and spatially localized hierarchical variation of cranial shape. We also found significant congruence between the pattern of cranial shape variation and molecular phylogeny. The differences in morphology of Triturus dobrogicus in comparison to other crested newt clades, including marked differences in cranium shape, is discussed in the context of the evolution and ecology of crested newts. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 348–360.     

A new primitive alligatorine from the Eocene of Thailand: relevance of Asiatic members to the radiation of the group

Despite the report of fragmentary remains from China, the fossil record of primitive Alligatorinae is unbalanced with most of its members reported from North America and Europe. Here, we describe cranial, mandibular, and some postcranial elements of a new alligatorine taxon from the Late Eocene of Krabi Basin, southern Thailand. Krabisuchus siamogallicus gen. et sp. nov. was a small animal probably not surpassing 2 m in total length. Despite deformation, the remains show a dorsally elevated cranium similar to Arambourgia gaudryi and Osteolaemus tetraspis. The new alligatorine is characterized by a very short snout and a blunt dentition in the posterior region. Krabisuchus siamogallicus is the first fossil alligatorine from Asia to be incorporated into cladistic analysis. Results indicate a close relationship of the newtaxon to Procaimanoidea, Arambourgia gaudryi, and Allognathosuchus polyodon, all of them being sister groups to the Alligator clade. Alligatorine were widespread as early as the Late Eocene across the northern hemisphere. Scenarios of alligatorine dispersal during the Palaeogene are discussed in comparison with the European and North American alligatorine fossil record. Basal alligatorines were probably land‐dwelling animals contrary to modern‐day crocodylians. Such a mode of life may have allowed this group to colonize vast territories, especially during periods of global warm climates. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158 , 608–628.     

A clan of Late Pleistocene hyenas,Crocuta crocuta spelaea (Goldfuss 1823), from the Rösenbeck Cave (Germany) and a contribution to cranial shape variability

The remains of a large population of Late Pleistocene Ice Age spotted hyenas (Crocuta crocuta spelaea Goldfuss 1823) are described from the Rösenbeck Cave in the Sauerland Karst of Germany. They include four skulls and 79 other skeletal parts, mainly from adult to senile animals, making this an important Late Pleistocene hyena cave‐den site in Europe. The skulls have been compared with 30 other hyena skull specimens from open air and cave‐den sites in central Europe (Germany, Austria, the Czech Republic and Romania) in order to achieve an understanding of sexual dimorphism in the crania of Ice Age spotted hyenas from the Upper Pleistocene cold period (Weichselian/Wuermian), and the types of injuries that they acquired during their lifetimes. Three different types of cranial shape have been distinguished, one of which appears to have been a consequence of pathologies that developed in response to injuries caused by bites received during the animal's lifetime, as a result of either intraspecies fights or fights with lions. Although cave bears penetrated to great depths within the Rösenbeck Cave for hibernation purposes, hyenas appear to have utilized only a short section of the cave that branched off directly from the entrance area. Hyena cub material is scarce, suggesting that this area was used as a communal den rather than for cub rearing. Bones exhibiting gnaw marks, representing prey imported by hyenas, are also rare but include horse (Equus caballus przewalskii) and reindeer (Rangifer tarandus) remains. The scarcity of bones from hyena prey suggests that this cave was not used as a food storage site. Some Ursus spelaeus cave bear remains, including skulls, show evidence of having been gnawed, chewed and cracked by hyenas, indicating that the hyenas periodically fed on cave bear carcasses in a specialization response to the mammoth steppe megafauna absence of the boreal mountain forest regions. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 191–220.     

Sexual differences in head form and diet in a population of Mexican lance‐headed rattlesnakes,Crotalus polystictus

Sexual dimorphism of phenotypic traits associated with resource use is common in animals, and may result from niche divergence between sexes. Snakes have become widely used in studies of the ecological basis of sexual dimorphism because they are gape‐limited predators and their head morphology is likely to be a direct indicator of the size and shape of prey consumed. We examined sexual dimorphism of body size and head morphology, as well as sexual differences in diet, in a population of Mexican lance‐headed rattlesnakes, Crotalus polystictus, from the State of México, Mexico. The maximum snout–vent length of males was greater than that of females by 21%. Males had relatively larger heads, and differed from females in head shape after removing the effects of head size. In addition, male rattlesnakes showed positive allometry in head shape: head width was amplified, whereas snout length was truncated with increased head size. By contrast, our data did not provide clear evidence of allometry in head shape of females. Adults of both males and females ate predominately mice and voles; however, males also consumed a greater proportion of larger mammalian species, and fewer small prey species. The differences in diet correspond with dimorphism in head morphology, and provide evidence of intersexual niche divergence in the study population. However, because the sexes overlapped greatly in diet, we hypothesize that diet and head dimorphisms in C. polystictus are likely related to different selection pressures in each sex arising from pre‐existing body size differences rather than from character displacement for reducing intersexual competition. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 633–640.