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Evolution Towards Fossoriality and Morphological Convergence in the Skull of Spalacidae and Bathyergidae (Rodentia)

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Journal of Mammalian Evolution
Authors:
Morgane Fournier at Universität Bern
Morgane Fournier
Lionel Hautier at French National Centre for Scientific Research
Lionel Hautier
Helder Gomes Rodrigues at Muséum National d'Histoire Naturelle
Helder Gomes Rodrigues
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Abstract and Figures

Rodents show a wide range of anatomical, physiological, and behavioral adaptations to life underground. Cranial and postcranial bone morphologies are deeply impacted by the modes of digging, which can involve either incisors or claws. However, the morphological variation of these elements still needs to be accurately quantified to assess the degree of specializations of the fossorial rodent families in regards to their respective evolution. Here, we focus on the morpho-functional characteristics of the masticatory apparatus in two families of subterranean rodents, the Spalacidae and Bathyergidae. We quantify skull shape in five spalacid genera using geometric morphometric methods, as well as biomechanical estimates for adductor muscles, which are compared with data previously published on bathyergids. We show that skull shape of spalacids has a greater disparity and lower biomechanical estimates than bathyergids, in which the fossorial activity, notably chisel-tooth digging, more significantly impacted the evolution of the skull. Among spalacids, Spalax shows the most extreme specializations to life underground and displays the highest number of morphological convergences with chisel-tooth digging bathyergids, especially regarding its cranial shape and high biomechanical estimate for the temporalis muscle. Fewer morphological convergences were observed between other spalacids and bathyergids. Different evolutionary histories can potentially explain discrepancies observed between the two families, the first bathyergid morphological adaptations to fossorial life being much older than those of spalacids.
Phylogenetic relationships between the investigated spalacid and bathyergid species, including extinct relatives (in grey) and modes of digging. Phylogenetic trees and stratigraphic ranges were based on previous studies using molecular and paleontological data (Cook 2000; Mein and Pickford 2008; Patterson and Upham 2014; Steppan and Schenck 2017; He et al. 2020)
Phylogenetic relationships between the investigated spalacid and bathyergid species, including extinct relatives (in grey) and modes of digging. Phylogenetic trees and stratigraphic ranges were based on previous studies using molecular and paleontological data (Cook 2000; Mein and Pickford 2008; Patterson and Upham 2014; Steppan and Schenck 2017; He et al. 2020)
… 
Landmarks digitized on the cranium (a, dorsal view; c, ventral view; e, lateral view) and the mandible (with the left incisor partly reconstructed; b, lateral view; d, occlusal view) of Spalax sp. (BMNH.10.3.12.10) imaged by using X-ray conventional microtomographic 3D rendering. f, Measure of inlevers (black lines), and outlevers (grey lines) between landmarks digitized on the mandible of Spalax. T: Temporalis, SM: Superficial Masseter, DM: Deep Masseter, I and I2 Incisor (Gomes Rodrigues et al. 2016)
Landmarks digitized on the cranium (a, dorsal view; c, ventral view; e, lateral view) and the mandible (with the left incisor partly reconstructed; b, lateral view; d, occlusal view) of Spalax sp. (BMNH.10.3.12.10) imaged by using X-ray conventional microtomographic 3D rendering. f, Measure of inlevers (black lines), and outlevers (grey lines) between landmarks digitized on the mandible of Spalax. T: Temporalis, SM: Superficial Masseter, DM: Deep Masseter, I and I2 Incisor (Gomes Rodrigues et al. 2016)
… 
Principal component analyses realized on crania of Spalacidae and associated virtual deformation on the extreme sides of each axis. Symbols used: (◊) Cannomys, (ӿ) Myospalax, (□) Rhizomys, (Δ) Spalax, ( ×) Tachyoryctes. Yellow and violet code for increases and decreases in surface area, respectively
Principal component analyses realized on crania of Spalacidae and associated virtual deformation on the extreme sides of each axis. Symbols used: (◊) Cannomys, (ӿ) Myospalax, (□) Rhizomys, (Δ) Spalax, ( ×) Tachyoryctes. Yellow and violet code for increases and decreases in surface area, respectively
… 
Principal component analyses realized on mandible of Spalacidae and associated virtual deformation on the extreme sides of each axis. Symbols used: (◊) Cannomys, (ӿ) Myospalax, (□) Rhizomys, (Δ) Spalax, ( ×) Tachyoryctes. Yellow and violet code for increases and decreases in surface area, respectively
Principal component analyses realized on mandible of Spalacidae and associated virtual deformation on the extreme sides of each axis. Symbols used: (◊) Cannomys, (ӿ) Myospalax, (□) Rhizomys, (Δ) Spalax, ( ×) Tachyoryctes. Yellow and violet code for increases and decreases in surface area, respectively
… 
Trees illustrating morphological distances between Spalacidae and between Bathyergidae resulting from neighbor joining analyses on coordinates data from the PCAs performed on crania and mandibles. Spalacidae—Ca: Cannomys, My: Myospalax, Rh: Rhizomys, Sp: Spalax, Ta: Tachyoryctes. Bathyergidae—Ba: Bathyergus, Fm: Fukomys mech., Fv: Fukomys vand., Ge: Georychus He: Heliophobius, Ht: Heterocephalus
+2
Trees illustrating morphological distances between Spalacidae and between Bathyergidae resulting from neighbor joining analyses on coordinates data from the PCAs performed on crania and mandibles. Spalacidae—Ca: Cannomys, My: Myospalax, Rh: Rhizomys, Sp: Spalax, Ta: Tachyoryctes. Bathyergidae—Ba: Bathyergus, Fm: Fukomys mech., Fv: Fukomys vand., Ge: Georychus He: Heliophobius, Ht: Heterocephalus
… 
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Vol.:(0123456789)
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https://doi.org/10.1007/s10914-021-09550-z
ORIGINAL PAPER
Evolution Towards Fossoriality andMorphological Convergence
intheSkull ofSpalacidae andBathyergidae (Rodentia)
MorganeFournier1· LionelHautier2· HelderGomesRodrigues1
Accepted: 7 April 2021
© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2021
Abstract
Rodents show a wide range of anatomical, physiological, and behavioral adaptations to life underground. Cranial and
postcranial bone morphologies are deeply impacted by the modes of digging, which can involve either incisors or claws.
However, the morphological variation of these elements still needs to be accurately quantified to assess the degree of spe-
cializations of the fossorial rodent families in regards to their respective evolution. Here, we focus on the morpho-functional
characteristics of the masticatory apparatus in two families of subterranean rodents, the Spalacidae and Bathyergidae. We
quantify skull shape in five spalacid genera using geometric morphometric methods, as well as biomechanical estimates
for adductor muscles, which are compared with data previously published on bathyergids. We show that skull shape of
spalacids has a greater disparity and lower biomechanical estimates than bathyergids, in which the fossorial activity, notably
chisel-tooth digging, more significantly impacted the evolution of the skull. Among spalacids, Spalax shows the most extreme
specializations to life underground and displays the highest number of morphological convergences with chisel-tooth dig-
ging bathyergids, especially regarding its cranial shape and high biomechanical estimate for the temporalis muscle. Fewer
morphological convergences were observed between other spalacids and bathyergids. Different evolutionary histories can
potentially explain discrepancies observed between the two families, the first bathyergid morphological adaptations to fos-
sorial life being much older than those of spalacids.
Keywords Skull shape· Fossorial adaptations· Life underground· Rodents· Geometric morphometrics
Introduction
Fossorial habits are widespread among mammals, but it
is especially the case in rodents, which include ten fami-
lies displaying important specializations to fossorial life:
Aplodontidae, Sciuridae, Bathyergidae, Ctenomyidae,
Octodontidae, Echimyidae, Geomyidae, Spalacidae, Cri-
cetidae, and Muridae (Agrawal 1967; Nevo 1999; Lacey
etal. 2000; Begall etal. 2007). Some species, recognized
as subterranean, live underground to forage for food, repro-
duce, and disperse (Nevo 1979). These rodents show a spe-
cialized digging lifestyle, which is reflected by a number
of physiological (e.g., low basal metabolic rate) and ana-
tomical convergences (e.g., eyes and pinnae reduced, mas-
sive masticatory muscles; Morlok 1983; Stein 2000; Burda
2006). Subterranean species convergently evolved different
modes of digging, from “scratch digging” characterized
by alternate flexing and extension of forearms bearing
enlarged claws to “chisel-tooth digging” involving the use
of procumbent incisors to scrape the ground. Digging with
incisors is also suggested to be combined with shoveling
movements of the head in a few cases (Hildebrand 1985;
Laville etal. 1989; Stein 2000). These different modes of
digging are associated with important morphological vari-
ations of the body (e.g., head and limbs), which remain to
be accurately described, to better understand the different
adaptive events to burrowing life in rodents.
Two phylogenetically distant rodent families, the
Spalacidae and Bathyergidae, display some of the most
extreme specializations to fossorial life. Spalacids belong
to the superfamily Muroidea and comprise at least six
genera from Asia (bamboo rats: Cannomys and Rhizomys;
* Helder Gomes Rodrigues
helder.gomes-rodrigues@mnhn.fr
1 Centre de Recherche en Paléontologie - Paris (CR2P), UMR
CNRS 7207, CP38, Muséum National D’Histoire Naturelle,
Sorbonne Université, 8 rue Buffon, 75005Paris, France
2 Institut Des Sciences de L’Evolution, cc64, Université de
Montpellier, CNRS, IRD, EPHE, 34095Montpellier, France
/ Published online: 10 May 2021
Journal of Mammalian Evolution (2021) 28:979–993
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Subterranean rodents generally show the most extreme cranial specializations due to their more intense activity of chisel-tooth digging (e.g., procumbent incisors and massive masticatory muscles; Fournier et al., 2021;Gomes Rodrigues et al., 2016;Landry, 1957;Lessa & Patton, 1989;Marcy et al., 2016;McIntosh & Cox, 2016) and ...
... Mandibular and cranial forms were quantified using 11 and 62 anatomical landmarks, respectively ( Figure 2; Supporting Information Online Material 2). This landmark data set was based on previous studies (Fournier et al., 2021;Gomes Rodrigues et al., 2016;Hautier et al., 2012) and was adapted to our sample. Landmarks #37 and #55 ...
... In previous studies (Michaux et al., 2008;Zelditch et al., 2015), the definition of the skull shape of Tamias tends to be variable, but generally in-between ground and arboreal squirrels. diggers, but in a markedly more pronounced way (e.g., Echeverría et al., 2017;Fournier et al., 2021;Gomes Rodrigues et al., 2016, in press;Marcy et al., 2016). They show a relatively wide and anteriorly tilted occipital plate for insertion of massive neck muscles necessary for removing earth out of the burrows (Stein, 2000), a distinctive character found in many extant and extinct fossorial rodents (Gomes Rodrigues et al. in press). ...
Incipient morphological specializations associated with fossorial life in the skull of ground squirrels (Sciuridae, Rodentia)
Article
Full-text available
  • Jan 2023
Anatomical and biological specializations have been studied extensively in fossorial rodents, especially in subterranean species, such as mole-rats or pocket-gophers. Sciurids (i.e., squirrels) are mostly known for their diverse locomotory behaviors, and encompass many arboreal species. They also include less specialized fossorial species, such as ground squirrels that are mainly scratch diggers. The skull of ground squirrels remains poorly investigated in a fossorial context, while it may reflect incipient morphological specializations associated with fossorial life, especially due to the putative use of incisors for digging in some taxa. Here, we present the results of a comparative analysis of the skull of five fossorial sciurid species, and compare those to four arboreal sciurids, one arboreal/fossorial sciurid and one specialized fossorial aplodontiid. The quantification of both cranial and mandibular shapes, using three dimensional geometric morphometrics, reveals that fossorial species clearly depart from arboreal species. Fossorial species from the Marmotini tribe, and also Xerini to a lesser extent, show widened zygomatic arches and occipital plate on the cranium, and a wide mandible with reduced condyles. These shared characteristics, which are present in the aplodontiid species, likely represent fossorial specializations rather than relaxed selection on traits related to the ancestral arboreal condition of sciurids. Such cranial and mandibular configurations combined with proodont incisors might also be related to the frequent use of incisors for digging (added to forelimbs), especially in Marmotini evolving in soft to hard soil conditions. This study provides some clues to understand the evolutionary mechanisms shaping the skull of fossorial rodents, in relation to the time spent underground and to the nature of the soil.
View
... The absence of significant differences in relative lobule size between the fossorial rodents and other groups when analyzed in the context of endocranial volume in this analysis may relate to the evolution of digging and fossoriality within Rodentia. Fossoriality has evolved independently several times in different rodent groups (here represented by Bathyergidae, Spalacidae, Aplodontidae) and has produced disparate adaptations in skeletal bone structure (Amson & Bibi, 2021) and skull morphology (Fournier et al., 2021). This disparity is the product of a variety of factors including evolutionary history, soil type, time spent above ground, and significantly, digging behavior (Stein, 2000). ...
... In some species, as in Ellobius, the head itself is used in a shoveling motion to excavate tunnels. The diversity of digging behaviors and disparity in fossorial adaptations (Amson & Bibi, 2021;Fournier et al., 2021) may have influenced subarcuate fossa size and therefore lobule size, especially if modifications have been made to the braincase. While it is most likely that the small lobules of these fossorial species relate to their reduced reliance on vision, a feature that characterizes fossorial groups (Stein, 2000), this result, together with previous analyses (Bertrand et al., , 2021 highlights the need for clade specific, fossil informed analyses of fossorial adaptations. ...
Scaling patterns of cerebellar petrosal lobules in Euarchontoglires: Impacts of ecology and phylogeny
Article
Full-text available
The petrosal lobules (in whole or part homologous with the paraflocculi) of the cerebellum regulate functions associated with vision including smooth pursuit and velocity control of eye movements, suggesting a possible relationship between the petrosal lobules and behavioral adaptation. Previous studies have produced diverging conclusions regarding the lobules' ecological signal. The current study examines lobule scaling within an ecologically diverse but phylogenetically constrained sample of extant mammals to determine whether ecology influences relative petrosal lobule size. Using the endocasts of 140 Euarchontoglires (Primates, Scandentia, Dermoptera, Lagomorpha, Rodentia), petrosal lobule size was evaluated relative to endocranium and body size, accounting for phylogenetic relationships and ecology (locomotor behavior, diet, activity pattern). Results show a strong positive relationship between lobule size and both endocranial volume and body mass. Phylogeny is a major factor in the scaling of the petrosal lobules, with significant differences in relative size identified between orders and suborders. Concerning ecology, fossorial taxa were found to have significantly smaller petrosal lobules relative to body mass compared to other locomotor groups across Euarchontoglires. The small lobules possessed by this group may reflect an adaptation related to reduced visual reliance. In contrast to previous research, no relationship was identified between relative lobule size and any other ecological variables. While variation in relative lobule size may be adaptively significant in some groups (i.e., fossorial species), it is critical to study the evolution of petrosal lobule size within a narrow phylogenetic scope, with inclusion of fossil material to inform our understanding of evolutionary trajectories.
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... bathyergids and heterocephalids; Patterson & Upham, 2014) and hystricomorphs. In both cases, the divergence is related to digging specializations (see also Hiiemae, 1971;Cox et al., 2020;Fournier et al., 2021). In Spalax, the infraorbital part of the zygomaticomandibularis is also well developed, differing from other subterranean rodent groups, such as bathyergoids. ...
Myology of the masticatory apparatus of herbivorous mammals and a novel classification for a better understanding of herbivore diversity
Article
  • Mar 2023
Masticatory muscle features allow for an understanding of how dietary habits and masticatory functions have evolved across mammalian lineages. Herbivorous mammals were traditionally classified as pertaining to either ‘ungulate-grinding’ or ‘rodent-gnawing’ morphotypes, but those classes might not adequately encompass the diversity of past and present herbivores. We compiled data for 104 herbivorous (nine orders, including new data for 31 species) and ten non-herbivorous (five orders) extant species and for four extinct taxa, in order to construct a more comprehensive scheme of masticatory morphotypes. A myological phylomorphospace revealed 15 morphotypes, which were tested statistically and interpreted morphofunctionally. Extant herbivorous morphotypes diversified along two main pathways that did not reflect the traditional types. Additionally, some extinct herbivores adapted along alternative pathways to those of extant forms. Early mammaliaforms and mammals possessed muscle proportions almost identical to those of living carnivores. Several more plesiomorphic herbivorous morphotypes were recognized, with some of them retaining generalized myological proportions. The rodent disparity was remarkable and could not be encompassed by a single category or pathway. Features of some derived euungulates and diprotodonts resembled rodents, but only a few extinct euungulates and extant wombats converged closely with them. Criteria for selecting models for palaeobiological reconstructions are discussed.
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... Several studies of extant bathyergids have focused on the cranial and dental anatomy of a few species (e.g., Berkovitz and Faulkes, 2001;Hart et al., 2007;Barčiová et al., 2009;Van Daele et al., 2009;Gomes Rodrigues et al., 2011;McIntosh and Cox, 2016a;Caspar et al., 2021). Only more recent assessments have incorporated a comparative approach including a larger number of species (Gomes Rodrigues and Šumbera, 2015;Gomes Rodrigues et al., 2016;Mason et al., 2016;McIntosh and Cox, 2016b;Fournier et al., 2021). In general, these studies have found clear differences between chisel-tooth diggers and scratchdiggers, with the former having a more specialized dental and craniomandibular morphology, including more procumbent incisors, shorter snout, relatively wider and taller skulls with enlarged zygomatic arches, strongly hystricognathous mandible, and increased jaw and condyle lengths relative to their size, all features that facilitates higher bite forces and wider gapes to maximize breaking up soils (Gomes Rodrigues et al., 2016;McIntosh and Cox, 2016a,b). ...
Functional anatomy and disparity of the postcranial skeleton of African mole-rats (Bathyergidae)
Article
Full-text available
  • Oct 2022
The burrowing adaptations of the appendicular system of African mole-rats (Bathyergidae) have been comparatively less investigated than their cranial adaptations. Because bathyergids exhibit different digging modes (scratch-digging and chisel-tooth digging) and social systems (from solitary to highly social), they are a unique group to assess the effects of distinct biomechanical regimes and social organization on morphology. We investigated the morphological diversity and intraspecific variation of the appendicular system of a large dataset of mole-rats (n = 244) including seven species and all six bathyergid genera. Seventeen morpho-functional indices from stylopodial (femur, humerus) and zeugopodial (ulna, tibia-fibula) elements were analyzed with multivariate analysis. We hypothesized that scratch-diggers (i.e., Bathyergus) would exhibit a more specialized skeletal phenotype favoring powerful forelimb digging as compared to the chisel-tooth diggers, and that among chisel-tooth diggers, the social taxa will exhibit decreased limb bone specializations as compared to solitary taxa due to colony members sharing the costs of digging. Our results show that most bathyergids have highly specialized fossorial traits, although such specializations were not more developed in Bathyergus (or solitary species), as predicted. Most chisel tooth-diggers are equally, or more specialized than scratch-diggers. Heterocephalus glaber contrasted significantly from other bathyergids, presenting a surprisingly less specialized fossorial morphology. Our data suggests that despite our expectations, chisel-tooth diggers have a suite of appendicular adaptations that have allowed them to maximize different aspects of burrowing, including shoulder and neck support for forward force production, transport and removal of soils out of the burrow, and bidirectional locomotion. It is probably that both postcranial and cranial adaptations in bathyergids have played an important role in the successful colonization of a wide range of habitats and soil conditions within their present distribution.
View
Functional and morphological divergence in the forelimb musculoskeletal system of scratch-digging subterranean mammals (Rodentia: Bathyergidae)
Article
Full-text available
  • May 2024
  • J ANAT
Whether the forelimb‐digging apparatus of tooth‐digging subterranean mammals has similar levels of specialization as compared to scratch‐diggers is still unknown. We assessed the scapular morphology and forelimb musculature of all four solitary African mole rats (Bathyergidae): two scratch‐diggers, Bathyergus suillus and Bathyergus janetta , and two chisel‐tooth diggers, Heliophobius argenteocinereus and Georychus capensis . Remarkable differences were detected: Bathyergus have more robust neck, shoulder, and forearm muscles as compared to the other genera. Some muscles in Bathyergus were also fused and often showing wider attachment areas to bones, which correlate well with its more robust and larger scapula, and its wider and medially oriented olecranon. This suggests that shoulder, elbow, and wrist work in synergy in Bathyergus for generating greater out‐forces and that the scapula and proximal ulna play fundamental roles as pivots to maximize and accommodate specialized muscles for better (i) glenohumeral and scapular stabilization, (ii) powerful shoulder flexion, (iii) extension of the elbow and (iv) flexion of the manus and digits. Moreover, although all bathyergids showed a similar set of muscles, Heliophobius lacked the m. tensor fasciae antebrachii (aiding with elbow extension and humeral retraction), and Heliophobius and Georychus lacked the m. articularis humeri (aiding with humeral adduction), indicating deeper morphogenetic differences among digging groups and suggesting a relatively less specialized scratch‐digging ability. Nevertheless, Heliophobius and Bathyergus shared some similar adaptations allowing scratch‐digging. Our results provide new information about the morphological divergence within this family associated with the specialization to distinct functions and digging behaviors, thus contributing to understand the mosaic of adaptations emerging in phylogenetically and ecologically closer subterranean taxa. This and previous anatomical studies on the Bathyergidae will provide researchers with a substantial basis on the form and function of the musculoskeletal system for future kinematic investigations of digging behavior, as well as to define potential indicators of scratch‐digging ability.
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Digging Up Convergence in Fossorial Rodents: Insights into Burrowing Activity and Morpho-Functional Specializations of the Masticatory Apparatus
Chapter
  • Feb 2023
Fossorial habits are tightly related to digging abilities in vertebrates and the most extreme fossorial specialization is being restricted to conducting the entire life underground. Many mammals, especially rodents, show behavioural, morphological and physiological adaptations to fossorial life, mainly for gaining access to sources of food and escaping predators and extreme climatic fluctuations. Adaptations to fossorial life are found in more than ten families of extant and extinct rodents, on most continents. Examples are Eurasian mole voles (Cricetidae), African mole-rats (Bathyergidae) and root-rats, Asian zokors and bamboo rats (Spalacidae), North American pocket gophers (Geomyidae) and mountain beavers (Aplodontidae), and South American tuco-tucos (Ctenomyidae) and cururos (Octodontidae). The constraints imposed by digging and living underground have led to strong behavioural and morphological convergences, notably involving the functioning of the rodent masticatory apparatus. Whereas most mammals use their claws for digging, rodents are unique in that some species use their ever-growing incisors for this purpose, with most subterranean species having become chisel-tooth diggers. Here, we review examples of convergence found in the main morphological and functional components of the rodent digging apparatus in relation to burrowing activity. We first present the different modes of digging in rodents, focusing on the chisel-tooth digging mechanisms and their associated burrowing behaviours. Following this, several morphological specializations of the skull and the main jaw adductor muscles are described in relation to their associated contribution to biting efficiency. Specialized incisors allow subterranean rodents to dig in hard soil and to consume hard subterranean parts of plants, and their morphological and structural characteristics are considered in the last part of this chapter. Data on incisor bite force of fossorial rodents are also compiled to highlight the enhanced efficacy of the masticatory apparatus of chisel-tooth digging species. Despite the different cranial and muscular morphotypes in rodents, we underscore the fact that multiple modifications of the different components of the masticatory apparatus have led to similar overall morphologies and functions, overcoming phylogenetic inheritance. This remarkable example of convergence needs further scrutiny at both the micro- and macroevolutionary level to more fully understand how different rodent families evolved to deal with such external constraints.
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On the antiquity and status of the Spalacidae, new data from the late Eocene of south-East Serbia
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  • May 2022
A new blind mole-rat species Debruijnia tintinnabulus nov. sp. is described from the late Eocene of south east Serbia. This find is approximately 10 Ma older than the hitherto oldest records of Spalacidae Vetusspalax and Pannoniamys, both from the late Oligocene of Bosnia and Herzegovina and Serbia. The antiquity of the new species (~34 Ma) is in accordance with recent genetically based age estimates of Spalacidae as an early branch of the Supramyomorpha. A review of the fossil record shows that the Spalacidae are probably not closely related to the Rhizomyinae and Myospalacinae. The spalacid finds from the Paleogene of the Balkans and the Neogene of Anatolia suggests that the family underwent a radiation during the Oligocene involving Debruijnia, Vetusspalax , Pannoniamys and Heramys. During the middle and late Miocene Heramys evolved into a large number of species, here all tentatively allocated to Pliospalax.
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Masticatory musculature of the African mole-rats (Rodentia: Bathyergidae)
Article
Full-text available
  • Mar 2020
The Bathyergidae, commonly known as blesmols or African mole-rats, is a family of rodents well-known for their subterranean lifestyle and tunnelling behaviour. Four of the five extant bathyergid genera ( Cryptomys , Fukomys , Georychus and Heliophobius ) are chisel-tooth diggers, that is they dig through soil with their enlarged incisors, whereas the remaining genus ( Bathyergus ) is a scratch-digger, only using its forelimbs for burrowing. Heterocephalus glaber , the naked mole-rat, is also a chisel-tooth digger and was until recently included within the Bathyergidae (as the most basally branching genus), but has now been placed by some researchers into its own family, the Heterocephalidae. Given the importance of the masticatory apparatus in habitat construction in this group, knowledge and understanding of the morphology and arrangement of the jaw-closing muscles in Bathyergidae is vital for future functional analyses. Here, we use diffusible iodine-based contrast-enhanced microCT to reveal and describe the muscles of mastication in representative specimens of each genus of bathyergid mole-rat and to compare them to the previously described musculature of the naked mole-rat. In all bathyergids, as in all rodents, the masseter muscle is the most dominant component of the masticatory musculature. However, the temporalis is also a relatively large muscle, a condition normally associated with sciuromorphous rodents. Unlike their hystricomorphous relatives, the bathyergids do not show an extension of the masseter through the infraorbital foramen on to the rostrum (other than a very slight protrusion in Cryptomys and Fukomys ). Thus, morphologically, bathyergids are protrogomorphous, although this is thought to be secondarily derived rather than retained from ancestral rodents. Overall, the relative proportions of the jaw-closing muscles were found to be fairly consistent between genera except in Bathyergus , which was found to have an enlarged superficial masseter and relatively smaller pterygoid muscles. It is concluded that these differences may be a reflection of the behaviour of Bathyergus which, uniquely in the family, does not use its incisors for digging.
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Phylogeny and biogeography of the African Bathyergidae: a review of patterns and processes
Article
Full-text available
  • Oct 2019
Background We review genealogical relationships, biogeographic patterns and broad historical drivers of speciation within the Bathyergidae, a group of endemic African rodents, as well as identify key taxa which need further research. Methods We sourced comparable cytochrome b sequence data (comparable data available for all members for the Family) and geographic information for all six genera of the African subterranean rodent. This information was combined into the most comprehensive and geographically representative evolutionary study for the Bathyergidae to date. Results Species richness within the Bathyergidae appears to be underestimated, with undescribed taxa in five of the six genera. Biogeographic patterns suggest large historical distributions, which were repeatedly fragmented by major landscape changes (especially rifting, uplift and drainage evolution) since the Miocene. Aside from vicariant events, other factors (ecological specialization, population-level responses and climatic change) may have been instrumental in driving divergences in the Bathyergidae. As such, adaptive differences may exist among both populations and species across their discrete ranges, driving independent evolutionary trajectories among taxa. In addition, highly fragmented distributions of divergent (and often relict) lineages indicates the possibility of narrow endemics restricted to diminishing suitable habitats. From this, it is clear that a systematic revision of the Bathyergidae is necessary; such a revision should include comprehensive sampling of all putative taxa, the addition of genomic information to assess adaptive differences, as well as ecological information.
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Evolutionary history of Spalacidae inferred from fossil occurrences and molecular phylogeny
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Full-text available
  • Sep 2019
1. Spalacidae is a family of strictly subterranean rodents with a long evolutionary history. It is unclear how historical ecological changes have influenced the evolutionary history of these mammals, and the phylogenetic relationship of the subfamilies within Spalacidae is controversial. 2. Through compiling fossil records, reconstructing molecular phylogeny from molecular data, determining the date of divergence, and analyzing their geographical evolution based on molecular data and fossil taxa, this study explores the origin and evolutionary process of Spalacidae in detail. Diversification within Spalacidae dates to the late Oligocene, approximately 25 Mya, based on molecular data. 3. This family originated in South and East Asia in the late Oligocene, and then split into four clades. The first clade includes Rhizomyinae, which was highly diversified in south Asia in the early to middle Miocene. Then Rhizomyinae from Asia migrated to northern Africa in multiple waves through the Afro-Eurasian land bridge. Its range largely contracted in the late Miocene, notably in central Asia. The second clade includes the extinct Tachyoryctoidinae, which was confined to east and central Asia, and survived from the late Oligocene to the late Miocene. The third clade includes Spalacinae, which have remained around the Mediterranean region since the late Oligocene with slight trend of northward expansion. The fourth clade is Myospalacinae. Ancient genera of this subfamily in east Asia dispersed eastward during the late Miocene and reached northern China and southeast Russia. 4. The general distribution pattern of Spalacidae has persisted since the late Miocene. Extinction of Tachyoryctoidinae and clear range contraction of Rhizomyinae in central and east Asia likely resulted from increased aridification, while the slight northward expansion of Myospalacinae and Spalacinae since the Quaternary was likely a response to a similar northward expansion of suitable vegetation for these animals.
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Morphometric models for estimating bite force in Mus and Rattus : mandible shape and size do better than lever-arm ratios
Article
Full-text available
  • May 2019
Morphological traits are frequently used as proxies for functional outputs such as bite force performance. This allows researchers to infer and interpret the impacts of functional variation, notably in adaptive terms. Despite their mechanical bases, the predictive power of these proxies for performance is not always tested. In particular, their accuracy at the intraspecific level is rarely assessed, and they have sometimes been shown to be unreliable. Here, we compared the performance of several morphological proxies in estimating in vivo bite force, across five species of murine rodents, at the interspecific and intraspecific levels. Proxies used included the size and shape of the mandible, as well as individual and combined muscular mechanical advantage (temporalis, superficial masseter and deep masseter). Maximum voluntary bite force was measured in all individuals included. To test the accuracy of predictions allowed by the proxies, we combined linear regressions with a leave-one-out approach, estimating an individual’s bite force based on the rest of the dataset. The correlations between estimated values and the in vivo measurements were tested. At the interspecific and intraspecific levels, size and shape were better estimators than mechanical advantage. Mechanical advantage showed some predictive power at the interspecific level, but generally not within species, except for the deep masseter in Rattus. In a few species, size and shape did not allow us to predict bite force. Extrapolations of performance based on mechanical advantage should therefore be used with care, and are mostly unjustified within species. In the latter case, size and shape are preferable
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Seismic communication in spalacids: signals in the giant root-rat and Gansu zokor
Article
Full-text available
  • Dec 2018
  • HYSTRIX
We analysed seismic signals in two spalacid rodents with a different degree of fossoriality: the giant root-rat (Tachyoryctes macrocephalus) and the Gansu zokor (Eospalax cansus). As all hitherto studied spalacids they also produce seismic signals by head-thumping, which probably evolved as a ritualization of soil tampering. The seismic signal of giant root-rat contains 5.51±1.60 pulses with inter-pulse distance of 0.11±0.01 s. The Gansu zokors produce seismic signals with 6.90±2.33 pulses and inter-pulse distance of 0.13±0.01s. Both studied species produced seismic signals during the peak of activity, most likely as territorial advertisement. No relationship has been found between inter-pulse distance and body mass in studied spalacid species; although this relationship did appear when the giant root-rat, the largest and most fossorial species, was excluded from the analysis. The seismic signals in spalacids can be considered as species specific.
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Differentiation underground: Range-wide multilocus genetic structure of the silvery mole-rat does not support current taxonomy based on mitochondrial sequences
Article
Full-text available
  • Aug 2018
The silvery mole-rat (Heliophobius argenteocinereus) is a solitary subterranean rodent with its distribution centred mainly in miombo woodlands of eastern Africa. This part of the continent was significantly influenced by the formation of the East African Rift System (EARS) during the last 25 Mya and by pronounced climatic changes in the Plio-Pleistocene that have caused genetic differentiation leading even to speciation events in many organisms. Recently, based on analysis of mitochondrial (mt) DNA sequences, it was suggested that H. argenteocinereus is a complex of six to eight species that diverged from the early to middle Miocene. In the present study, we significantly extended the sampling, re-analysed mtDNA datasets and analysed nuclear markers with the aim to assess the evolutionary history of Heliophobius. If we do not consider the old museum samples from south-eastern Democratic Republic of Congo (very divergent short mtDNA sequences obtained from ancient DNA, requiring further study from fresh material), the genus Heliophobius is composed of three major mtDNA lineages with parapatric distribution. The Rukwa Rift (+Mbeya triple junction) at the Zambia-Tanzania border, Lake Malawi, and the Eastern Arc Mountains form the biogeographical divides among these clades. The relatively shallow differences among the mitochondrial clades, divergence dating based on the use of the fossilised birth-death ratio model and a multi-locus dataset, and a very similar pattern of genetic structure to other rodents inhabiting the same area and habitat, suggest that the evolutionary history of the extant silvery mole-rat was predominantly influenced by the climatic fluctuations in the Plio-Pleistocene. Awaiting further studies employing genomic, ecological, morphological or behavioural data, we advocate for using the single name H. argenteocinereus for all evolutionary lineages within this taxon, because (1) comparison of the genetic structure observed in mtDNA and nuclear markers suggest hybridization between at least some mtDNA lineages in the contact zones; and (2) new samples close to the type localities suggest incorrect use of previous names.
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The impact of digging on the evolution of the rodent mandible
Article
  • Nov 2018
  • J MORPHOL
There are two main (but not mutually exclusive) methods by which subterranean rodents construct burrows: chisel‐tooth digging, where large incisors are used to dig through soil; and scratch digging, where forelimbs and claws are used to dig instead of incisors. A previous study by the authors showed that upper incisors of chisel‐tooth diggers were better adapted to dig but the overall cranial morphology within the rodent sample was not significantly different. This study analyzed the lower incisors and mandibles of the specimens used in the previous study to show the impact of chisel‐tooth digging on the rodent mandible. We compared lower incisors and mandibular shape of chisel‐tooth digging rodents with nonchisel‐tooth digging rodents to see if there were morphological differences between the two groups. The shape of incisors was quantified using incisor radius of curvature and second moment of area (SMA). Mandibular shape was quantified using landmark based geometric morphometrics. We found that lower incisor shape was strongly influenced by digging group using a Generalized Phylogenetic ancova (analysis of covariance). A phylogenetic Procrustes anova (analysis of variance) showed that mandibular shape of chisel‐tooth digging rodents was also significantly different from nonchisel‐tooth digging rodents. The phylogenetic signal of incisor radius of curvature was weak, whereas that of incisor SMA and mandibular shape was significant. This is despite the analyses revealing significant differences in the shape of both mandibles and incisors between digging groups. In conclusion, we showed that although the mandible and incisor of rodents are influenced by function, there is also a degree of phylogenetic affinity that shapes the rodent mandibular apparatus.
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ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R
Article
  • Jul 2018
  • BIOINFORMATICS
After more than fifteen years of existence, the R package ape has continuously grown its contents, and has been used by a growing community of users. The release of version 5.0 has marked a leap towards a modern software for evolutionary analyses. Efforts have been put to improve efficiency, flexibility, support for 'big data' (R's long vectors), ease of use, and quality check before a new release. These changes will hopefully make ape a useful software for the study of biodiversity and evolution in a context of increasing data quantity. Availability: ape is distributed through the Comprehensive R Archive Network: http://cran.r-project.org/package=apeFurther information may be found athttp://ape-package.ird.fr/.
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