A heterochronic interpretation of the origin of digging adaptations in the northern water vole, Arvicola terrestris (Rodentia: Arvicolidae)

The Palaearctic genus Arvicola includes two species: the south‐western water vole A. sapidus, and the northern water vole A. terrestris. The latter has semiaquatic and/or subterranean populations, while populations of A. sapidus are always semiaquatic. According to the current phylogenetic and palaeontological data, adaptation to semiaquatic life is plesiomorphic for the genus Arvicola. We studied the ontogenetic allometry of skull and long bones of the semiaquatic A. sapidus, a semiaquatic population of A. terrestris (A. t. italicus), and two fossorial populations of A. terrestris (A. t. scherman and A. t. monticola). Animals from fossorial populations were smaller than were those from semiaquatic populations. We found that most of the ontogenetic allometric exponents of characters linked to digging in the skull and in the long bones were significantly higher in A. t. monticola, a fossorial clade, than they were in the semiaquatic populations. On the other hand, there may have been an evolutionary lag between invasion of the hypogeic habitat and the acquisition of fossorial adaptations in A. t. scherman. We showed statistically that the morphological differences linked to the invasion of a hypogeic habitat are already present in juvenile animals and, according to these results, suggest that these morphological differences are the direct expression of genetic changes rather than the outcome of epigenetic factors of mechanical origin. Moreover, we tried to ascertain whether the apomorphic shape of the skull and long bones in the fossorial populations of A. terrestris (compared with the primitive condition that would have been retained by the semiaquatic A. sapidus) are the outcome of a heterochronic process. Optimization by squared change parsimony supported the hypothesis of an apomorphic reduction of body size linked to the invasion of the subterranean habitat. The comparison of the ontogenetic trajectories of both skull shape and long bone shape suggested that a heterochronic process was involved in this morphological transformation. By using the ‘clock model’ method, this mechanism was identified as ‘accelerated dwarfism’ affecting both the skull and long bones. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87 , 381–391.     

Life in Burrows Channelled the Morphological Evolution of the Skull in Rodents: the Case of African Mole-Rats (Bathyergidae,Rodentia)

African mole-rats are fossorial rodents that consist of five chisel-tooth digging genera (Heterocephalus, Heliophobius, Georychus, Fukomys, and Cryptomys) and one scratch digger (Bathyergus). They are characterized by striking physiological, morphological, and behavioral adaptations intimately related to their subterranean life. The influence of their mode of life in shaping the cranial morphology has yet to be evaluated in comparison to other Ctenohystrica, especially fossorial genera, which include the subterranean genera Spalacopus and Ctenomys. In our study, we seek to determine to what extent subterranean life affects the morpho-functional properties of the skull among fossorial ctenohystricans. 3D geometric morphometric analyses were performed on 277 skulls, encompassing 63 genera of Ctenohystrica, and complemented by biomechanical studies. African mole-rats and other subterranean Ctenohystrica, especially chisel-tooth diggers, have a short snout, a wide cranium with enlarged zygomatic arches, and a strongly hystricognathous mandible. Even if convergences are also manifest between most fossorial Ctenohystrica, subterranean rodents departed from the main ctenohystrican allometric trends in having a skull shape less size-dependent, but under stronger directional selection with intense digging activity as a major constraint. African mole-rats, notably chisel-tooth diggers, show important mechanical advantage for the temporalis muscles favoring higher forces at the bite point, while mechanical advantage of the superficial masseter muscles is lower compared to other Ctenohystrica. If subterranean species can be clearly discriminated based on their skull morphology, the intrinsic mosaic of anatomical characters of each genus (e.g., skull, teeth, and muscles) can be understood only in the light of their ecology and evolutionary history.     

Moringua edwardsi (Moringuidae: Anguilliformes): Cranial specialization for head‐first burrowing?

The order Anguilliformes forms a natural group of eel-like species. Moringua edwardsi (Moringuidae) is of special interest because of its peculiar fossorial lifestyle: this species burrows head-first. Externally pronounced morphological specializations for a fossorial lifestyle include: reduced eyes, lack of color, low or absent paired vertical fins, elongated, cylindrical body, reduced head pores of the lateral line system, etc. Many fossorial amphibians, reptiles, and even mammals have evolved similar external specializations related to burrowing. The present study focuses on osteological and myological features of M. edwardsi in order to evaluate the structural modifications that may have evolved as adaptations to burrowing. Convergent evolutionary structures and possible relations with head-first burrowing, miniaturization, feeding habits, etc., were investigated. Body elongation, reduction of the eyes, modified cranial lateral line system, and modified skull shape (pointed though firm) can be considered specializations for head-first burrowing. Hyperossification can probably be regarded more as a specialization to both head-first burrowing and feeding, even though an impact of miniaturization cannot be excluded. Hypertrophied adductor mandibulae muscles and the enlarged coronoid process can be associated with both feeding requirements (it enhances bite forces necessary for their predatory behavior) and with a burrowing lifestyle, as well as miniaturization.     

Diversification of African tree frogs (genus Leptopelis) in the highlands of Ethiopia

The frog genus Leptopelis is composed of ~50 species that occur across sub‐Saharan Africa. The majority of these frogs are typically arboreal; however, a few species have evolved a fossorial lifestyle. Most species inhabit lowland forests, but a few species have adapted to high elevations. Five species of Leptopelis occupy the Ethiopian highlands and provide a good opportunity to study the evolutionary transition from an arboreal to a fossorial lifestyle, as well as the diversification in this biodiversity hot spot. We sequenced 14 nuclear and three mitochondrial genes, and generated thousands of SNPs from ddRAD sequencing to study the evolutionary relationships of Ethiopian Leptopelis. The five species of highland Leptopelis form a monophyletic group, which diversified during the late Miocene and Pliocene. We found strong population structure in the fossorial species L. gramineus, with levels of genetic differentiation between populations similar to those found between arboreal species. This could indicate that L. gramineus is a complex of cryptic species. We propose that after the original colonization of the Ethiopian highlands by the ancestor of the L. gramineus group, episodes of vicariance fragmented the ancestral populations of this group. We also report the re‐evolution of arboreality in L. susanae, which evolved from a fossorial ancestor, a rare ecological switch in frogs that had previously been reported only once.     

Terrestrial adaptations in the postcranial skeletons of guenons

Arboreal and semiterrestrial guenons show similar osteological features of the limbs across a wide range of species, environments, and geography, while the more terrestrially committed guenons exhibit greater morphological divergence. An ecomorphological comparison of two sympatric guenons living in Kibale Forest, Uganda, reveals an array of anatomical adaptations for terrestriality in the limbs of Cercopithecus lhoesti similar to those found in Erythrocebus patas. In contrast, Cercopithecus aethiops, although also frequent users of the terrestrial environment, generally exhibit fewer morphological adaptations characteristic of a terrestrial lifestyle. It appears that significant morphological modification for terrestriality has occurred twice within the diverse radiation of living guenons with C. aethiops perhaps representing a third group in the making. © 1994 Wiley-Liss, Inc.     

From lizard body form to serpentiform morphology: The atlas–axis complex in African cordyliformes and their relatives

The comparative vertebral morphology of the atlas–axis complex in cordyliforms, xantusiid and several skinks is studied here. These lizards are particularly interesting because of their different ecological adaptations and anti‐predation strategies, where conformation ranges from the lizard‐like body to a snake‐like body. This transition to serpentiform morphology shows several evolutionary patterns in the atlas–axis complex: 1) the zygapophyseal articulations are lost in the early stage of the transition. In contrast to mammals, the atlas is more or less locked to the axis in lepidosaurs, but the absence of zygapophyseal articulation releases this locking for rotation. However despite its serpentiform morphology, Chamaesaura is different, in possessing this articulation; 2) the first intercentrum of Chamaesaura and Tetradactylus africanus (serpentiform grass‐swimmers) is fully curved anteriorly, underlying the occipital condyle. While this limits ventral skull rotation beyond a certain angle, it locks the skull, which is a crucial adaptation for a sit‐and‐wait position in grassland habitats that needs to keep the head stabilized; and 3) in Acontias, most of the atlas articular surface with the occipital condyle is formed by the lateral aspect of the articulation area relative to the area located in the dorsal region of the slightly reduced intercentrum. A similar state occurs in amphisbaenians, most likely reflecting a fossorial lifestyle of the limbless lizards. Although Chamaesaura and Tetradactylus live sympatrically in grasslands, Chamaesaura differs in several ways in atlas–axis complex: for example, aforementioned presence of the atlas–axis zygapophyseal articulation, and long posterodorsal processes. Its occipital condyle protrudes further posteriorly, placing the atlas–axis complex further from the endocranium than in Tetradactylus. Hence, adaptation in the same niche, even among sister clades, can lead to different atlas–axis morphology due to different lifestyle strategies, for example, different foraging mode, while similar atlas–axis morphology can evolve in two lineages occupying different niches, as in Ablepharus and Scelotes. J. Morphol. 277:512–536, 2016. © 2016 Wiley Periodicals, Inc.     

Ontogeny and phyletic size change in living and fossil lemurs

Lemurs are notable for encompassing the range of body‐size variation for all primates past and present—close to four orders of magnitude. Benefiting from the phylogenetic proximity of subfossil lemurs to smaller‐bodied living forms, we employ allometric data from the skull to probe the ontogenetic bases of size differentiation and morphological diversity across these clades. Building upon prior pairwise comparisons between sister taxa, we performed the first clade‐wide analyses of craniomandibular growth allometries in 359 specimens from 10 lemuroids and 176 specimens from 8 indrioids. Ontogenetic trajectories for extant forms were used as a criterion of subtraction to evaluate morphological variation, and putative adaptations among sister taxa. In other words, do species‐level differences in skull form result from the differential extension of common patterns of relative growth? In lemuroids, a pervasive pattern of ontogenetic scaling is observed for facial dimensions in all genera, with three genera also sharing relative growth trajectories for jaw proportions (Lemur, Eulemur, Varecia). Differences in masticatory growth and form characterizing Hapalemur and fossil Pachylemur likely reflect dietary factors. Pervasive ontogenetic scaling characterizes the facial skull in extant Indri, Avahi, and Propithecus, as well as their larger, extinct sister taxa Mesopropithecus and Babakotia. Significant interspecific differences are observed in the allometry of indrioid masticatory proportions, with variation in the mechanical advantage of the jaw adductors and stress‐resisting elements correlated with diet. As the growth series and adult data are largely coincidental in each clade, interspecific variation in facial form may result from selection for body‐size differentiation among sister taxa. Those cases where trajectories are discordant identify potential dietary adaptations linked to variation in masticatory forces during chewing and biting. Although such dissociations highlight selection to uncouple shared ancestral growth patterns, they occur largely via transpositions and retention of primitive size‐shape covariation patterns or relative growth coefficients. Am. J. Primatol. 72:161–172, 2010. © 2009 Wiley‐Liss, Inc.     

Embryonic development of the fossorial gymnophthalmid lizards Nothobachia ablephara and Calyptommatus sinebrachiatus

The evolutionary history of the lizard family Gymnophthalmidae is characterized by several independent events of morphological modifications to a snake-like body plan, such as limb reduction, body elongation, loss of external ear openings, and modifications in skull bones, as adaptive responses to a burrowing and fossorial lifestyle. The origins of such morphological modifications from an ancestral lizard-like condition can be traced back to evolutionary changes in the developmental processes that coordinate the building of the organism. Thus, the characterization of the embryonic development of gymnophthalmid lizards is an essential step because it lays the foundation for future studies aiming to understand the exact nature of these changes and the developmental mechanisms that could have been responsible for the evolution of a serpentiform (snake-like) from a lacertiform (lizard-like) body form. Here we describe the post-ovipositional embryonic development of the fossorial species Nothobachia ablephara and Calyptommatus sinebrachiatus, presenting a detailed staging system for each one, with special focus on the development of the reduced limbs, and comparing their development to that of other lizard species. The data provided by the staging series are essential for future experimental studies addressing the genetic basis of the evolutionary and developmental variation of the Gymnophthalmidae.     

A non‐aquatic otter (Mammalia,Carnivora, Mustelidae) from the Late Miocene (Vallesian,MN 10) of La Roma 2 (Alfambra,Teruel, Spain): systematics and functional anatomy

A new genus and species of otter‐like mustelid, Teruelictis riparius, is created on the basis of a partial skeleton from the Late Miocene (Vallesian age, MN 10) locality of La Roma 2 (Teruel, Spain), including several postcranial elements, the skull, and the mandible. The combination of a typically lutrine dentition, similar to that of other fossil otters such as Paralutra jaegeri, with a very slender postcranial skeleton, including a long back and gracile long bones and metacarpals, thus lacking any aquatic adaptations, was previously unknown in the fossil record. This mosaic of features strongly suggests the possibility that the aquatic lifestyle of otters could have appeared after the initial development of the distinctive dental morphology of this specialized group of mustelids. © 2013 The Linnean Society of London     

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.     

Skeletal development in the fossorial gymnophthalmids Calyptommatus sinebrachiatus and Nothobachia ablephara

The development of the cartilaginous and bony elements that form the skull and axial and appendicular skeleton is described in detail for the post-ovipositional embryonic development of the fossorial gymnophthalmid species Calyptommatus sinebrachiatus and Nothobachia ablephara. Both species have a snake-like morphology, showing an elongated body and reduced or absent limbs, as well as modifications in skull bones for burrowing, such as complex articulation surfaces and development of bony extensions that enclose and protect the brain. Similar morphological changes have originated independently in several squamate groups, including the one that led to the snake radiation. This study characterizes the patterns of chondrogenesis and osteogenesis, with special emphasis on the features associated with the burrowing habit, and may be used for future comparative analyses of the developmental patterns involved in the origin of the convergent serpentiform morphologies.     

What can morphology tell us about ecology of four invasive goby species?

This study presents a detailed comparative analysis of external morphology of four of the most invasive goby species in Europe (round goby Neogobius melanostomus, bighead goby Ponticola kessleri, monkey goby Neogobius fluviatilis and racer goby Ponticola gymnotrachelus) and interprets some ecological requirements of these species based on their morphological attributes. The results are evaluated within an ontogenetic context, and the morphological differences between the species are discussed in terms of the question: can special external shape adaptations help to assess the invasive potential of each species? The morphometric analyses demonstrate important differences between the four invasive gobies. Neogobius melanostomus appears to have the least specialized external morphology that may favour its invasive success: little specialization to habitat or diet means reduced restraints on overall ecological requirements. The other three species were found to possess some morphological specializations (P. kessleri to large prey, N. fluviatilis to sandy habitats and P. gymnotrachelus to macrophytes), but none of these gobies have managed to colonize such large areas or to reach such overall abundances as N. melanostomus.     

Genetic structure,ecological versatility,and skull shape differentiation in Arvicola water voles (Rodentia,Cricetidae)

Water voles from the genus Arvicola display an amazing ecological versatility, with aquatic and fossorial populations. The Southern water vole (Arvicola sapidus) is largely accepted as a valid species, as well as the newly described Arvicola persicus. In contrast, the taxonomic status and evolutionary relationships within Arvicola amphibiussensu lato had caused a long-standing debate. The phylogenetic relationships among Arvicola were reconstructed using the mitochondrial cytochrome b gene. Four lineages within A. amphibiuss.l. were identified with good support: Western European, Eurasiatic, Italian, and Turkish lineages. Fossorial and aquatic forms were found together in all well-sampled lineages, evidencing that ecotypes do not correspond to distinct species. However, the Western European lineage mostly includes fossorial forms whereas the Eurasiatic lineage tends to include mostly aquatic forms. A morphometric analysis of skull shape evidenced a convergence of aquatic forms of the Eurasiatic lineage toward the typically aquatic shape of A. sapidus. The fossorial form of the Western European lineage, in contrast, displayed morphological adaptation to tooth-digging behavior, with expanded zygomatic arches and proodont incisors. Fossorial Eurasiatic forms displayed intermediate morphologies. This suggests a plastic component of skull shape variation, combined with a genetic component selected by the dominant ecology in each lineage. Integrating genetic distances and other biological data suggest that the Italian lineage may correspond to an incipient species (Arvicola italicus). The three other lineages most probably correspond to phylogeographic variations of a single species (A. amphibius), encompassing the former A. amphibius, Arvicola terrestris, Arvicola scherman, and Arvicola monticola.     

Comparative skull osteology of Karsenia koreana (Amphibia,Caudata, Plethodontidae)

The recent discovery of a plethodontid salamander, Karsenia koreana, in Korea challenged our understanding of the biogeographic history of the family Plethodontidae, by far the largest family of salamanders, which otherwise is distributed in the New World with a few European species. Molecular studies suggest that Karsenia forms a clade with Hydromantes (sensu lato), which includes among its species the only other Old World plethodontids. We studied the skull of K. koreana and compared it with that of other plethodontid genera, especially members of the subfamily Plethodontinae, which it resembles most closely in general anatomy. The anatomy of its skull corresponds to the most generalized and apparently ancestral condition for plethodontids. No clearly autapomorphic states were detected, and no synapomorphies can be found that would link it to other genera. The Karsenia skull is cylindrical and well ossified, giving an impression of strength. In contrast, the skull of Hydromantes is highly derived; the skull is flattened and the bones are weakly ossified and articulated. Hydromantes and Karsenia share no unique anatomical features; differences between them are especially evident in the hyobranchial skeleton, which is generalized in Karsenia but highly modified in Hydromantes, which is well known for its highly projectile tongue. Plethodon and Plethodon‐like species, including Karsenia and to a lesser degree Ensatina, represent the more generalized and apparently ancestral plethodontid morphology. Specialized morphologies have evolved along only a few morphological axes within the Plethodontidae, resulting in a pattern of rampant homoplasy. Our analysis of the anatomy of the new Asiatic lineage illuminates some potential mechanisms underlying adaptive morphological evolution within the Plethodontidae. J. Morphol. 2010. © 2009 Wiley‐Liss, Inc.     

Taxonomy,skull diversity and evolution in a species complex of Myotis (Chiroptera: Vespertilionidae): a geometric morphometric appraisal

Phylogenetic relationships between taxa are not necessarily reflected by morphological data due to widespread homoplasy and convergence. However, combining morphological and molecular data provides insights into the evolution of biological forms and into the potential factors involved. Here we focus on a complex of three taxa of bats with unclear taxonomic affinities: Myotis myotis, Myotis blythii and Myotis punicus. Traditional morphometric methods failed to separate them, whereas recent molecular‐based studies suggested that they constitute separate biological species. In the present study, landmark‐based geometric morphometrics methods have been used to analyse the skull variability of 218 specimens belonging to this species complex. Patterns of size and shape delimitate three morphological groups that are congruent with the proposed taxonomic assignments, and therefore support species rank for all three major groups. These morphometrics results, however, suggest that M. myotis and M. punicus share shape characteristics in the rostrum and in the posterior part of the skull that differ from M. blythii. Because previous molecular phylogenetic analyses suggested that M. myotis and M. blythii are sister species, we interpret the similitude in skull morphology between M. myotis and M. punicus as a convergence probably related to their similar feeding habits. Within the taxon M. punicus, the skull of Corsican and Sardinian populations significantly differs from that of Maghrebian ones, suggesting the existence of further cryptic taxonomic diversity. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 529–538.     

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.     

Ecological and phenotypic divergence in Iberian shrews (Soricidae)

There are examples of coexisting species with similar morphology and ecology, in apparent contradiction to competition theory. Shrews (Soricidae) are a paradigmatic example of this because members of this group exhibit a conserved body form, relatively low variability in lifestyle, and, in many cases, a sympatric distribution. Here, we combined geometric morphometrics and ecological niche modeling to test whether diversification of soricid species inhabiting the Iberian Peninsula has been driven by niche divergence or, conversely, whether niche conservatism has played a paramount role in this process. We also examined whether pairwise morphological distances increase as the degree of niche overlap between species becomes greater, as would be expected if interspecific competition promotes morphological differentiation. Our results showed that water shrews (Neomys), white‐toothed shrews (Crocidurinae), and red‐toothed shrews (Soricinae) are clearly differentiated in terms of both skull shape and mandible shape. However, we found a lack of phylogenetic signal in most morphological traits, indicating that closely related species are not more similar than expected by random chance. Notably, water shrews show a more “triangular” or sharp skull than white‐toothed and red‐toothed shrews, probably as an adaptation to their semiaquatic lifestyle. In agreement with the phenotypic data, climatic traits (mean annual temperature and annual precipitation) were highly labile and sister taxa showed extensive differentiation in their realized niche space. Finally, we found that phenotypic distances between species tend to increase as the degree of niche overlap increases, suggesting that interspecific competition is an important factor in determining the level of morphological resemblance among relatives. Overall, our results indicate that the existence of limited morphological disparity in a given group does not necessarily imply the existence of a niche conservatism signature.