Title: Functional implications of craniomandibular morphology in African mole-rats (Rodentia: Bathyergidae) Running head: Bathyergid functional morphology Authors



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Title: Functional implications of craniomandibular morphology in African mole-rats (Rodentia: Bathyergidae)
Running head: Bathyergid functional morphology
Authors:

Andrew F. McIntosh1

Philip G. Cox2
Institutional addresses:

1Centre for Anatomical and Human Sciences, Hull York Medical School, University of Hull, Hull, UK

2Centre for Anatomical and Human Sciences, Department of Archaeology, University of York, and Hull York Medical School, York, UK
Corresponding author:

Philip G. Cox

Email address: philip.cox@hyms.ac.uk

Telephone: +44 1904 321744



ABSTRACT

African mole-rats are subterranean rodents from the family Bathyergidae. The family consists of six genera, five of which (Cryptomys, Fukomys, Georychus, Heliophobius and Heterocephalus) are chisel-tooth diggers, meaning they dig underground using procumbent incisors. The remaining genus of mole-rat (Bathyergus) is a scratch digger, which digs using its forelimbs. Chisel-tooth digging is thought to have evolved to enable exploitation of harder soils. It was hypothesised that in order to dig successfully using incisors, chisel-tooth digging mole-rats will have a craniomandibular complex that is better able to achieve a large bite force and wide gape compared to scratch digging mole-rats. Linear measurements of morphological characteristics associated with bite force and gape were measured in a number of chisel-tooth digging and scratch digging mole-rats. It was found that chisel-tooth diggers have increased jaw and condyle lengths relative to their size (characteristics associated with larger gape). They also have relatively wider and taller skulls (characteristics associated with larger bite force). The mechanical advantage of three masticatory muscles of each specimen was also calculated. Mechanical advantage of the temporalis muscle was found to be significantly larger in chisel-tooth digging mole-rats compared to the scratch digging genus. Our results demonstrate that chisel-tooth digging bathyergids have a craniomandibular morphology better able to facilitate high bite force and wide gape than scratch digging mole-rats.


Keywords: Masticatory biomechanics; chisel-tooth digging; scratch digging; Bathyergidae; mole-rats; subterranean rodents


INTRODUCTION

Morphological correlates of digging in subterranean rodents have been well documented (Nevo, 1979) and may be the result of numerous different evolutionary strategies. Lessa and Thaeler (1989) proposed two alternative evolutionary strategies for digging in two genera of pocket gopher: an increase in incisor procumbency to facilitate chisel-tooth digging versus an enlargement of the forearms to enable scratch digging. Scratch digging primarily involves soil removal via enlarged forelimbs, and is used by numerous fossorial mammals, including many rodents (e.g. Dubost, 1968; Hildebrand, 1985; Reichman and Smith, 1990; Nevo, 1999). Chisel-tooth digging, which involves the use of incisors powered by head and jaw muscles to remove compact soil, evolved to allow subterranean species to exploit harder soils (Lessa and Thaeler, 1989) and is associated with many morphological traits such as more procumbent incisors, wider crania, enlarged zygomatic arches, longer rostra and larger temporal fossae (Landry, 1957a; Agrawal, 1967; Lessa, 1990; Samuels and Van Valkenburgh, 2009).


Incisor procumbency, the angle of the incisor protruding from the rostrum or mandible, is a well-studied morphological trait associated with chisel-tooth digging (Lessa, 1990). Stein (2000) notes that, although chisel-tooth digging is accomplished primarily by the lower incisors, with the upper incisors being used to anchor the skull to the soil (Jarvis and Sale, 1971), it is the upper incisors that show greater variability in their procumbency. An example of this exists in the rodent family Bathyergidae (the African mole-rats or blesmols), in which the chisel-tooth diggers Cryptomys and Georychus have been shown to have significantly greater upper incisor procumbency compared with the scratch digger Bathyergus. Lower incisor procumbency however was not significantly different between the three genera (Van der Merwe and Botha, 1998). This association between upper incisor procumbency and chisel-tooth digging is said to allow a more favourable angle of attack for anchoring the head of the rodent to the burrow wall when compared to more recurved upper incisors (Lessa, 1990; Vassallo, 1998; Korth and Rybczynski, 2003). Upper incisor procumbency is influenced by the degree of curvature of the incisor and the position of the incisor in the rostrum (Landry, 1957a; Akersten, 1981). Within the Bathyergidae, the root of the incisor of chisel-tooth diggers extends behind the molar tooth row, a trait unique amongst rodents (Ellerman, 1940). This is in contrast to the scratch digging Bathyergus, whose upper incisor is rooted above the first molar. It has been suggested by Van der Merwe and Botha (1998) that the posterior displacement of the upper incisor root in chisel-tooth digging rodents promotes increased procumbency. In addition, Landry (1957a) suggested that an increase in the length of the incisor located within the rostrum would increase the area of contact between tooth and skull, and so would help dissipate biting forces more effectively, thus protecting the region of odontogenesis at the posterior end of the incisor.
Bite force and gape are limiting factors for animals in the context of their feeding and behavioural ecology. For instance, the force at which an animal can bite will limit the range of hardness of food items that the animal can consume, with previous studies showing a correlation between bite force, food mechanical properties and diet (e.g. Kiltie, 1982; Binder and Van Valkenburgh, 2000). In contrast, gape limits the size of food that an animal can ingest (e.g. Gans, 1961; Herring and Herring 1974; Pough and Groves, 1983; Wheelwright, 1985). Although bite force and gape have been widely studied in the context of dietary inferences (Herrel et al, 2001; Dumont and Herrel, 2003; Vinyard, 2003; Taylor and Vinyard 2004; Williams et al, 2009; Santana et al, 2010), very little research has focused on behaviour such as fossorial activity (Van Daele et al, 2009). Furthermore, despite several studies on morphological predictors of bite force and gape, few have combined morphological predictors with biomechanical modelling to show how morphological traits affect the biomechanics of the system.
The main aims of this study were to highlight key morphological traits in the craniomandibular complex that would improve the performance of bite force and/or gape in a particular family of subterranean rodents, the African mole-rats (Bathyergidae). Bathyergids are especially interesting when investigating the morphological correlates of digging because chisel-tooth digging is seen in five of the six genera of bathyergids (Cryptomys, Fukomys, Georychus, Heliophobius and Heterocephalus), whereas Bathyergus is the only genus to use the scratch digging method (Nowak, 1999; Stein, 2000). Furthermore, recent phylogenies (Figure 1; Faulkes et al, 2004; Seney et al, 2009; Patterson and Upham, 2014) agree that the scratch digging genus Bathyergus is nested deep within the crown of Bathyergidae, indicating that chisel-tooth digging is ancestral for the family and has been lost in Bathyergus. Despite this, previous research has shown that the cranium of Bathyergus is morphologically different from the chisel-tooth digging bathyergids, having more in common with other, more distantly related scratch digging rodents (Samuels and Van Valkenburgh, 2009). Thus, the skull of Bathyergus has changed, either by adaptation to a different selection pressure, or by genetic drift owing to the release of the constraint of chisel-tooth digging.
The objective of this study is to ascertain whether the cranial morphology of chisel-tooth digging bathyergids better facilitates high bite force and wide gape than does the cranial morphology of the scratch digging Bathyergus. We hypothesise that the change in morphology of Bathyergus, whether mediated by selection or drift, will have decreased its tooth digging abilities, which will be manifest in reduced bite force and gape. Based on previous work there are a number of predictions that can be made:
Morphological predictions related to bite force

An increase in bite force has been found to be strongly correlated with an increase in head height in Fukomys mole-rats (Van Daele et al, 2009) and bats (Dumont and Herrel, 2003). We therefore hypothesise that chisel-tooth diggers will have relatively increased head heights compared to scratch diggers.


Chisel-tooth diggers tend to have broader zygomatic arches and larger temporal fossae to accommodate larger, more powerful masticatory muscles (e.g. Hildebrand, 1985; Stein, 2000; Samuels and Van Valkenburgh, 2009) and so it is hypothesised that chisel-tooth diggers will have relatively wider crania compared to scratch diggers.
An increase in upper incisor procumbency has been shown to be associated with chisel-tooth digging in a number of subterranean rodents (Landry, 1957a; Lessa, 1990; Vassallo, 1998; Samuels and Van Valkenburgh, 2009). This increase in procumbency has also been associated with an increase in rostral length (Lessa and Patton, 1989; Mora et al, 2003). It was therefore hypothesised that chisel-tooth digging rodents will have an increased upper incisor procumbency and a longer rostrum compared to scratch diggers.
Morphological predictions related to gape

Gape has been shown to be strongly predicted by jaw length in animals whose masticatory biomechanics have been extensively studied, such as snakes (e.g. Hampton and Moon, 2013). Vinyard and Payseur (2008) also found a significant correlation between maximum gape and jaw length in classical inbred strains of house mice. In addition, the cranium and mandible in rodents strongly co-vary (Hautier et al, 2012). As it has been hypothesised that rostral length increases in chisel-tooth digging rodents, if this covariation occurs in subterranean rodents, then it is also expected that there will be an increase in jaw length combined with that of rostral length in chisel-tooth digging rodents. Thus, it is hypothesised that chisel-tooth diggers will have a relatively longer jaw compared to scratch diggers.


Elongated antero-posterior lengths of articulating joint surfaces are known to increase joint mobility (Ruff, 1988; Hamrick, 1996). An increased antero-posterior length of the condyle articular surface has also been linked to increased gape in primates (Vinyard et al, 2003) and house mice (Vinyard and Payseur, 2008). Gape also increases theoretically in mammals with reduced condyle heights (height of condyle above the molar tooth row) as this reduces stretch in masticatory muscles during gape (Herring and Herring, 1974). Hence, we hypothesise that chisel-tooth digging mole-rats will have lower condyles with longer articulating surfaces than the scratch digging genus Bathyergus.
Biomechanics of a chisel-tooth digger

The performance of the masticatory apparatus is traditionally assessed by modelling the jaw as a static third class lever and calculating mechanical advantage (MA) of each masticatory muscle (Maynard Smith and Savage, 1959). MA is the ratio of the muscle moment arm to the jaw moment arm and is affected if either moment arm is changed within the system. The jaw moment arm is the distance from the pivot (in mammalian masticatory biomechanics this is equivalent to the temporomandibular joint [TMJ]) to the bite force vector, and the muscle moment arm is the perpendicular distance from the TMJ to the muscle force vector. Movement of the bite point towards the TMJ (assuming constant muscle attachments) will result in a higher MA, as the jaw moment arm has been reduced. This biomechanical definition explains why there is a trade-off between gape and bite force. An increase in jaw length is associated with larger gape (e.g. Hampton and Moon, 2013) but will also increase the jaw moment arm, reducing the MA of the masticatory muscle, and therefore reducing bite force. It is clear that craniomandibular traits that facilitate an increase in gape thus decrease bite force capabilities, and vice versa. Due to this trade-off, animals that need both large gapes and large bite forces, e.g. carnivores, may show unique morphological traits. Animals that must produce high bite forces at large gapes normally have larger temporalis muscles compared to animals that produce larger bite forces with smaller gapes, in which case the masseter dominates (Turnbull, 1970). It was therefore hypothesised that in chisel-tooth digging subterranean rodents, the temporalis muscle would have a higher mechanical advantage compared to that of scratch digging subterranean rodents to enable the production of a high bite force at large gape. It was also hypothesised that MA of temporalis would be maintained at larger gapes in chisel-tooth diggers compared to scratch diggers.


MATERIALS AND METHODS

A sample of 47 crania and mandibles from the subterranean rodent family Bathyergidae, representing adult mole-rats of both sexes, were used in this analysis. The sample comprised five species of chisel-tooth digging rodents (Cryptomys hottentotus, Fukomys mechowi, Georychus capensis, Heliophobius argenteocinereus and Heterocephalus glaber) and one species of scratch digging rodent (Bathyergus suillus), representing all six extant genera of bathyergid mole-rats. The specimens were scanned on an X-Tek Metris microCT scanner at the University of Hull (Medical and Biological Engineering Research Group), and the resulting scans had isometric voxels ranging between 0.01-0.07 mm. MicroCT scans were automatically reconstructed in Avizo 8.0 (FEI, Hillsboro, OR) using a predefined grey scale to render a 3D volume of each specimen (Figure 2). From the reconstructions, 3D landmark co-ordinates were recorded to enable the calculation of six linear measurements – three from the cranium (cranial width, head height and rostral length) and three from the mandible (jaw length, condyle length and condyle height). In addition, the procumbency angle of the upper incisor was measured based on the method outlined in Landry (1957a). All measurements taken are detailed in Table 1 and Figure 3. Linear measurements were scaled relative to basilar length (the midline distance along the cranial base from the anterior extremity of the premaxillae to the margin of the foramen magnum). Each linear measurement was also regressed against basilar length to show the effects of allometric scaling. Due to the error contained in the variables and the ambiguity of dependence between variables, a reduced major axis model was fitted (Sokal and Rohlf, 1981). Both variables were logged in order to fit the standard allometric equation, y=axb. The slope, R2 and P values for each allometric equation are given in Table 2. For visualisation purposes the data were displayed as box plots, with each genus shown separately. However, owing to small sample sizes of Cryptomys, Georychus and Heterocephalus, for statistical testing the specimens were grouped by digging method. Between 10 and 11 specimens of the scratch digging Bathyergus, and between 25 and 36 specimens of chisel-tooth digging mole-rats were included in each analysis. Following Ruxton (2006), the unequal variance t-test (Welch’s t-test) was used to test for significant differences between the scratch digging and chisel-tooth digging groups, except where there was evidence of non-normality in the data, in which case the non-parametric Mann-Whitney U test was employed. The normality of the data in each group was tested using the Shapiro-Wilk test. All statistical tests were performed using PAST (Hammer et al, 2001). To check that the over-represented chisel-tooth genera (Fukomys and Heliophobius) were not unduly influencing the results, the tests were rerun using just five randomly-selected specimens of each; however, the results were unchanged.
In addition to the cranial and mandibular measurements outlined above, the performance of three major masticatory muscles (superficial masseter, deep masseter and temporalis) was measured in each specimen for a comparison between chisel-tooth digging and scratch digging systems. These muscles were selected as together they make up over 80% of the masticatory muscles in mole-rats (Bekele, 1983; Cox and Faulkes, 2014). Performance was measured by calculating the MA of each muscle using moment arms (Figure 4; example using temporalis muscle). Muscle moment arms (MMA) were calculated for the selected muscles, along with the jaw moment arm (JMA) for each specimen. Mechanical advantage was calculated as the ratio between these two variables.
The cranium and mandible of each specimen were re-orientated with respect to one another in Avizo 8.0 to simulate incisal occlusion (Figure 4). Incisal occlusion was defined by the tips of the upper and lower incisor being in contact, and each mandibular condyle being in contact with the articular surfaces of the corresponding glenoid fossa. Following this, a bite force vector (BFV) was defined as a line going directly through the incisor bite point (point of contact between incisors), orthogonal to the occlusal plane of the hemi-mandible. JMA was calculated as the perpendicular distance from the fulcrum (condyle tip) to the BFV (see Figure 4). The incisor was the only bite point chosen in this study as chisel-tooth digging is carried out exclusively by the incisors.
The angle between the jaw moment arm and the line from the fulcrum to the bite point (angle θ, Figure 4) was calculated using trigonometry in 3D. The occlusal plane is defined as the plane on the mandible containing points at the posterior edge of the tooth row and points at the medial and lateral sides of the third mandibular molar. The angle between the occlusal plane and the line connecting the fulcrum and bite point (dashed line in Figure 4) was then calculated using the dot product:


Where n is the normal vector to the occlusal plane and m is the vector of the line representing the distance from the fulcrum to the incisor bite point. As the occlusal plane runs parallel to the JMA, θ is equivalent to the angle between JMA and the line representing the distance between fulcrum and incisor bite point. The JMA can then be calculated using standard trigonometry.
MMA is calculated as the perpendicular distance from the fulcrum to the muscle force vector (MFV). MFV was defined by a line going through the centre of the origin and insertion of each muscle (see Figure 2). The origin and insertion of each muscle was defined by placing a curve on the dorsal border of each muscle origin on the cranium and the ventral border of each muscle insertion on the mandible. The curve was placed via a B-spline in Avizo 8.0, and automatically divided into 100 equidistant points. Thus the centre of each origin and insertion could be established to represent the directionality of the muscle force. Note that no curve was placed on the insertion of temporalis or the origin of superficial masseter as these muscle attachment areas were small enough to be represented as a single point. MMA was then calculated using standard trigonometry.
In order to evaluate the effect of gape on mechanical advantage, a rotation matrix was used to rotate the co-ordinates lying on the mandible around an axis running through the landmarks representing the dorsal points on the condylar surfaces on the left and right side of the mandible (thus simulating mandibular rotation):

Where) is the point being rotated about the line through with a direction vector of by angle . The direction vector is defined by the tips of the left and right condyles.
It is also worth noting that the theoretical maximum gape of this model was deemed to be the angle where mechanical advantage was a minimum. This assumption originates from the fact that beyond a certain angle of rotation, the mandibular insertion of the muscle will move posterior to the fulcrum, and therefore from that point would operate to open the jaw, not close it. Limitations of this model will also be discussed below.
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