Ontogenetic skull variation in a shovel-headed amphisbaenian species.

Leposternon microcephalum is a species belonging to the Amphisbaenia, a group of burrowing reptiles. Amphisbaenia present various morphological and physiological adaptations that allow them to penetrate the ground and live underground, through a system of galleries and permanent chambers that they build themselves. Among the morphological adaptations in this group, those of the skull stand out as it serves as the main excavation tool. Four basic skull shapes are recognized: rounded, keeled, shovel-shaped, and spade-shaped. The skull of L. microcephalum belongs to this last type, which is considered the most specialized. The species inhabits soils that are highly compacted and difficult to penetrate. Among the species of Leposternon present in South America, L. microcephalum has the widest distribution, being found in all Brazilian biomes and neighboring countries such as Bolivia, Argentina, Paraguay, and Uruguay. The analysis of the skull of this species was carried out using three-dimensional geometric morphometrics (3D-GMM), a technique that allows comparative analysis, through robust statistical methods, of shape and its variations, using Cartesian coordinate data from a configuration of homologous landmarks. The technique allows the size and shape components of a structure to be analyzed separately. From an ontogenetic point of view, this methodology had also been used to investigate variations in Cynisca leucura, a member of the Amphisbaenidae with a rounded head. Our hypothesis is that the patterns of morphological differentiation in the skull, mainly in the intermediate and occipital regions, are similar in different Amphisbaenia species. Therefore, the objective of this study was to analyze cranial morphological variations in an ontogenetic series of L. microcephalum using 3D-GMM. Computed Tomographic scans of 13 specimens were analyzed: juveniles (N = 8) and adults (N = 5), based on 20 landmarks that characterize the skull. Principal components and regression analyses between shape (dependent variable) and size (independent variable) showed a clear difference between the cranial morphological pattern of juvenile individuals and that of adults. For instance, young specimens tend to have a dorsoventrally tall neurocranium, with the tip of the snout more anteriorly oriented and its dorsal border subtly curved. Dorsally, the parietal region is thicker and smoothly dome-shaped in juveniles. As in C. leucura, the variation was strongly correlated with the size change from juvenile to adult, indicating a dominant role for ontogenetic allometry in determining skull shape.

Shape analysis of the preorbital bar in caviomorph rodents.

The highly specialised masticatory apparatus of rodents raises interesting questions about how their skull withstands the intensive and sustained forces produced by biting on hard items. In these mammals, major systematics were explored for a long time based on the adductor muscles' architecture and the related bony structures. The infraorbital foramen stands out, where a hypertrophied head of the zygomaticomandibular muscle passes through-in hystricomorphous rodents-as a direct consequence of the lateral and posterior shift of the preorbital bar. Interestingly, this bar moved laterally and backwards-enlarging the foramen-but it never disappeared throughout evolution, even showing morphological convergence among rodents. Previous research proposed this bar as behaving mechanically similar to the postorbital bar in ungulates, i.e., a safety structure against torsion stress while chewing. We analysed its morphology by mathematically modelling it under bending and torsion scenarios (linearly and elliptically shaped, respectively), and as for biting load propagation (catenary curve). Although the preorbital bar primarily seems to be shaped for withstanding torsional stress (as the postorbital bar in ungulates) and as an escaping point for force propagation, these forces are not a consequence of chewing and grinding foods, but preventing the zygomatic arch from failing when the powerful laterally-displaced jaw adductor muscles are pulling the dentary upwards at biting.

Mandible strength and geometry in relation to bite force: a study in three caviomorph rodents.

The monophyletic group Caviomorpha constitutes the most diverse rodent clade in terms of locomotion, ecology and diet. Caviomorph species show considerable variation in cranio-mandibular morphology that has been linked to the differences in toughness of dietary items and other behaviors, such as chisel-tooth digging. This work assesses the structural strength of the mandible of three caviomorph species that show remarkable differences in ecology, behavior and bite force: Chinchilla lanigera (a surface-dwelling species), Octodon degus (a semi-fossorial species) and Ctenomys talarum (a subterranean species). Finite element (FE) models of the mandibles are used to predict the stresses they withstand during incisor biting; the results are related to in vivo bite forces and interspecific variations in the mandibular geometries. The study concludes that the mandible of C. talarum is better able to withstand strong incisor bites. Its powerful adducting musculature is consistent with the notorious lateral expansion of the angular process and the masseteric crest, and the enhanced cortical bone thickness. Although it has a relatively low bite force, the mandible of O. degus also shows a good performance for mid-to-strong incisor biting, in contrast to that of C. lanigera, which exhibits, from a mechanical point of view, the worst performance. The mandibles of C. talarum and O. degus appear to be better suited to withstand stronger reaction forces from incisor biting, which is consistent with their closer phylogenetic affinity and shared digging behaviors. The contrast between the low in vivo bite force of C. lanigera and the relatively high estimations that result from the models suggests that its adductor musculature could play significant roles in functions other than incisor biting.

Bite it forward bite it better? Incisor procumbency and mechanical advantage in the chisel-tooth and scratch-digger genus Ctenomys (Caviomorpha, Rodentia).

The subterranean genus Ctenomys (∼60 species, ∼100-1000g) constructs its burrows by using both forefeet and teeth throughout a wide range of habitats in South America. They show a high variation in the incisors' angle of attack (procumbency) and a mostly conserved skull morphology, not only amongst their congeners, but within the caviomorph rodents. Traditionally, procumbency has been largely related to tooth-digging. Looking for the possible influence of incisor procumbency on the mechanical advantage (MA) of each of the seven jaw adductor muscles in the genus, we examined 165 skulls representing 24 species. We also evaluated the role of two other relevant traits - i.e. mandibular width and diastema length - in jaw biomechanics and the existence of a relationship between procumbency angle and soil hardness. The in- and out-lever arms (Li and Lo) of the involve muscles were determined based on their insertion's 3D-coordinates and integrated to calculate their MA. Interspecific scaling relationships for skull and muscle measurements were analyzed through reduced major axis regression performed with phylogenetically independent standardized contrasts. Although the procumbency angle ranged between ∼92.5° (C. mendocinus) and ∼107.2 (C. occultus), we found that it was not significantly correlated with the MA of any jaw adductor muscle. This study also showed that the incisor procumbency variation was not associated with the relative rostral length or soil hardness. This result contradicts previous generalizations about a correlation between habitat conditions and the procumbency of the incisors in subterranean rodents. In sum, our results suggest that, within Ctenomys, possessing more procumbent incisors may not represent a biomechanical advantage, but might be beneficial in other aspects related to chisel-tooth digging or food processing behaviors.

Sexual selection in a polygynous rodent (Ctenomys talarum): an analysis of fighting capacity.

The South American subterranean rodent genus Ctenomys (Caviomorpha: Octodontoidea), which uses both claws and teeth to dig, shows striking morphological adaptations to its specialized mode of life. Among other traits, the genus has evolved a powerful jaw musculature and procumbent incisors that are used for dento-excavation. Behavioral observations indicate that these traits are also used during male aggressive encounters, which characterize the polygynous mating system of one of the species of the genus, Ctenomys talarum. A question emerges about sexual selection: could it have induced further changes in traits primarily evolved as adaptations for digging? To address this issue, we studied functional and morphological attributes of the jaw and incisors in specimens of C. talarum. Incisor bite forces were measured on wild females and males from a local population (Mar de Cobo; Buenos Aires Province) by means of a strain gauge load cell force transducer. Museum specimens coming from the same population were studied to assess anatomical attributes of both sexes. Since this species exhibits dimorphism in body size, the possible effect of body mass on the studied traits was analyzed. Males and females showed significant differences in biting performance and mandibular width, but when size was taken into account these differences disappeared. However, other dimorphic traits can vary with a certain independence with respect to size, particularly the 2nd moment of area of the incisors and, to a lesser extent, incisor procumbency. The former geometrical parameter, which is proportional to the bending strength, was highly dimorphic. This fact suggests that, during aggressive encounters between males, biting would place large bending loads on the incisors.

Scaling and adaptations of incisors and cheek teeth in caviomorph rodents (Rodentia, Hystricognathi).

The South American hystricognath rodents are one of the most diverse mammalian clades considering their occupied habitats, locomotor modes and body sizes. This might have been partly evolved by diversification of their masticatory apparatus' structure and its ecological commitment, for example, chisel-tooth digging. In this phylogeny-based comparative study, we test the relationship between ecological behavior and mechanical features of their incisors and molariforms. In 33 species of nine families of caviomorph rodents, we analyze incisor attributes related to structural stress resistance and molar features related with grinding capacity, for example, second moment of inertia and enamel index (EI) (enamel band length/occlusal surface area), respectively. Most of these variables scaled isometrically to body mass, with a strong phylogenetic effect. A principal component analysis discrimination on the EI clustered the species according to their geographic distribution. We presume that selective pressures in Andean-Patagonian regions, on particular feeding habits and chisel-tooth digging behaviors, have modeled the morphological characteristics of the teeth. Subterranean/burrower ctenomyids, coruros, and plains viscachas showed the highest bending/torsion strength and anchorage values for incisors; a simplified enamel pattern in molariforms would be associated with a better grinding of the more abrasive vegetation present in more open and drier biomes.

Phylogeographical structure in the subterranean tuco-tuco Ctenomys talarum (Rodentia: Ctenomyidae): contrasting the demographic consequences of regional and habitat-specific histories.

In this work we examined the phylogeography of the South American subterranean herbivorous rodent Ctenomys talarum (Talas tuco-tuco) using mitochondrial DNA (mtDNA) control region (D-loop) sequences, and we assessed the geographical genetic structure of this species in comparison with that of subterranean Ctenomys australis, which we have shown previously to be parapatric to C. talarum and to also live in a coastal sand dune habitat. A significant apportionment of the genetic variance among regional groups indicated that putative geographical barriers, such as rivers, substantially affected the pattern of genetic structure in C. talarum. Furthermore, genetic differentiation is consistent with a simple model of isolation by distance, possibly evidencing equilibrium between gene flow and local genetic drift. In contrast, C. australis showed limited hierarchical partitioning of genetic variation and departed from an isolation-by-distance pattern. Mismatch distributions and tests of neutrality suggest contrasting histories of these two species: C. talarum appears to be characterized by demographic stability and no significant departures from neutrality, whereas C. australis has undergone a recent demographic expansion and/or departures from strict neutrality in its mtDNA.