Functional and morphological divergence in the forelimb musculoskeletal system of scratch-digging subterranean mammals (Rodentia: Bathyergidae)

DATA AVAILABILITY STATEMENT : All data supporting our findings are available in the present study in the form of tables and figures.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.Open access publishing facilitated by Jihoceska Univerzita v Ceskych Budejovicich, as part of the Wiley - CzechELib agreement.http://www.wileyonlinelibrary.com/journal/joahj2024Mammal Research InstituteZoology and EntomologySDG-15:Life on lan

Functional anatomy and disparity of the postcranial skeleton of African mole-rats (Bathyergidae)

DATA AVAILABILITY STATEMENT : The original contributions presented in this study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author.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 (scratchdigging 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 scratchdiggers (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.The Becas Chile, Government of Chile, the National Research Foundation, the SARChI Chair of Mammalian Behavioral Ecology and Physiology and Czech Science Foundation Project GACR.http://frontiersin.org/Ecology_and_Evolutionam2023Mammal Research InstituteZoology and Entomolog

Fossorial adaptations in African mole-rats (Bathyergidae) and the unique appendicular phenotype of naked mole-rats

DATA AVAILABILITY: All the data generated and analysed in this study are included in this published article and its supplementary information files.CODE AVAILABILITY: The code for all analyses is available at: https://github.com/gabrielsaffa/african_mole_rats.Life underground has constrained the evolution of subterranean mammals to maximize digging performance. However, the mechanisms modulating morphological change and development of fossorial adaptations in such taxa are still poorly known. We assessed the morpho-functional diversity and early postnatal development of fossorial adaptations (bone superstructures) in the appendicular system of the African mole-rats (Bathyergidae), a highly specialized subterranean rodent family. Although bathyergids can use claws or incisors for digging, all genera presented highly specialized bone superstructures associated with scratch-digging behavior. Surprisingly, Heterocephalus glaber differed substantially from other bathyergids, and from fossorial mammals by possessing a less specialized humerus, tibia and fibula. Our data suggest strong functional and developmental constraints driving the selection of limb specializations in most bathyergids, but more relaxed pressures acting on the limbs of H. glaber. A combination of historical, developmental and ecological factors in Heterocephalus are hypothesized to have played important roles in shaping its appendicular phenotype.Financial support for the research trip to Kenya of J.U.M.J. was provided by The National Geographic Society, whereas funding support for the maintenance of the original NMR colonies was provided by the University of Cape Town and the South African National Research Foundation (NRF). DST-NRF is acknowledged for the financial support to establish the MIXRAD micro-focus X-ray tomography facility at Necsa.https://www.nature.com/commsbioam2023Mammal Research InstituteZoology and Entomolog

Bone remodeling in the longest living rodent, the naked mole-rat : interelement variation and the effects of reproduction

The pattern of bone remodeling of one of the most peculiar mammals in the world, the naked mole-rat (NMR), was assessed. NMRs are known for their long lifespans among rodents and for having low metabolic rates. We assessed long-term in vivo bone labeling of subordinate individuals, as well as the patterns of bone resorption and bone remodeling in a large sample including reproductive and non-reproductive individuals (n = 70). Over 268 undecalcified thin cross-sections from the midshaft of humerus, ulna, femur and tibia were analyzed with confocal fluorescence and polarized light microscopy. Fluorochrome analysis revealed low osteogenesis, scarce bone resorption and infrequent formation of secondary osteons (Haversian systems) (i.e., slow bone turnover), thus most likely reflecting the low metabolic rates of this species. Secondary osteons occurred regardless of reproductive status. However, considerable differences in the degree of bone remodeling were found between breeders and non-breeders. Pre-reproductive stages (subordinates) exhibited quite stable skeletal homeostasis and bone structure, although the attainment of sexual maturity and beginning of reproductive cycles in female breeders triggered a series of anabolic and catabolic processes that up-regulate bone turnover, most likely associated with the increased metabolic rates of reproduction. Furthermore, bone remodeling was more frequently found in stylopodial elements compared to zeugopodial elements. Despite the limited bone remodeling observed in NMRs, the variation in the pattern of skeletal homeostasis (interelement variation) reported here represents an important aspect to understand the skeletal dynamics of a small mammal with low metabolic rates. Given the relevance of the remodeling process among mammals, this study also permitted the comparison of such process with the well-documented histomorphology of extinct therapsids (i.e., mammalian precursors), thus evidencing that bone remodeling and its endocortical compartmentalization represent ancestral features among the lineage that gave rise to mammals. It is concluded that other factors associated with development (and not uniquely related to biomechanical loading) can also have an important role in the development of bone remodeling.CONICYT; National Research Foundation and DST-NRF.http://www.wileyonlinelibrary.com/journal/joahj2022Mammal Research InstituteZoology and Entomolog

Late early Miocene caviomorph rodents from Laguna del Laja (~37° S), Cura-Mallín Formation, south-central Chile

Despite recent efforts, the paleodiversity of the Neogene mammals in Chile remains poorly known, with several putative new species awaiting description. For example, previous studies suggest that the early to late Miocene mammalian assemblages from the Laguna del Laja fossiliferous locality (Cura-Mallín and Trapa-Trapa formations), which crop out in the Andean Cordillera of Chile (~37°), comprise dozens of undescribed taxa. A better understanding of the taxonomic affinities of the Laguna del Laja faunas is needed, as it represents one of the few faunas known from the early to late? Miocene of the south-central Andean main range. Several specimens of caviomorphs recently recovered in late early Miocene beds of the Cura-Mallín Formation at Laguna del Laja are here described in detail, and a brief discussion of their chronological, biogeographical, and paleoenvironmental significance is also provided. Based on fragments of mandible, maxilla and isolated teeth five taxa were recognized, Phanomys mixtus Ameghino, Prolagostomus sp., Neoreomys sp., Maruchito nov. sp.?, and Luantus sompallwei nov. sp. The radiometric ages of the fossil-bearing horizons, constrained between 17.7 and 16.4 Ma, as well as the common species (P. mixtus) and genera (Prolagostomus and Neoreomys) indicate that the fauna here reported belongs to the Santacrucian SALMA. Finally, our finding preliminary suggests the predominance of rather open habitats in the Cura-Mallín Formation during this time, but also a widely distributed late Early Miocene caviomorph fauna along the southern Andes, in both intra-arc and foreland basins.Fil: Solorzano, Andres. Universidad de Concepción; ChileFil: Encinas, Alfonso. Universidad de Concepción; ChileFil: Kramarz, Alejandro Gustavo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Museo Argentino de Ciencias Naturales "Bernardino Rivadavia"; ArgentinaFil: Carrasco, Gabrial. Servicios Científicos Educativos y Turismo Científico; ChileFil: Montoya Sanhueza, German. University of Cape Town; SudáfricaFil: Bobe, Rene. University of Oxford; Reino Unid

Long bone histomorphogenesis of the naked mole-rat : histodiversity and intraspecific variation

Lacking fur, living in eusocial colonies and having the longest lifespan of any rodent, makes naked mole-rats (NMRs) rather peculiar mammals. Although they exhibit a high degree of polymorphism, skeletal plasticity and are considered a novel model to assess the effects of delayed puberty on the skeletal system, scarce information on their morphogenesis exists. Here, we examined a large ontogenetic sample (n = 76) of subordinate individuals to assess the pattern of bone growth and bone microstructure of fore- and hindlimb bones by using histomorphological techniques. Over 290 undecalcified thin cross-sections from the midshaft of the humerus, ulna, femur, and tibia from pups, juveniles and adults were analyzed with polarized light microscopy. Similar to other fossorial mammals, NMRs exhibited a systematic cortical thickening of their long bones, which clearly indicates a conserved functional adaptation to withstand the mechanical strains imposed during digging, regardless of their chisel-tooth predominance. We describe a high histodiversity of bone matrices and the formation of secondary osteons in NMRs. The bones of pups are extremely thin-walled and grow by periosteal bone formation coupled with considerable expansion of the medullary cavity, a process probably tightly regulated and adapted to optimize the amount of minerals destined for skeletal development, to thus allow the female breeder to produce a higher number of pups, as well as several litters. Subsequent cortical thickening in juveniles involves high amounts of endosteal bone apposition, which contrasts with the bone modeling of other mammals where a periosteal predominance exists. Adults have bone matrices predominantly consisting of parallel-fibered bone and lamellar bone, which indicate intermediate to slow rates of osteogenesis, as well as the development of poorly vascularized lamellar-zonal tissues separated by lines of arrested growth (LAGs) and annuli. These features reflect the low metabolism, low body temperature and slow growth rates reported for this species, as well as indicate a cyclical pattern of osteogenesis. The presence of LAGs in captive individuals was striking and indicates that postnatal osteogenesis and its consequent cortical stratification most likely represents a plesiomorphic thermometabolic strategy among endotherms which has been suggested to be regulated by endogenous rhythms. However, the generalized presence of LAGs in this and other subterranean taxa in the wild, as well as recent investigations on variability of environmental conditions in burrow systems, supports the hypothesis that underground environments experience seasonal fluctuations that may influence the postnatal osteogenesis of animals by limiting the extension of burrow systems during the unfavorable dry seasons and therefore the finding of food resources. Additionally, the intraspecific variation found in the formation of bone tissue matrices and vascularization suggested a high degree of developmental plasticity in NMRs, which may help explaining the polymorphism reported for this species. The results obtained here represent a valuable contribution to understanding the relationship of several aspects involved in the morphogenesis of the skeletal system of a mammal with extraordinary adaptations.CONICYT; National Research Foundation and DST-NRF.http://www.wileyonlinelibrary.com/journal/joahj2022Mammal Research InstituteZoology and Entomolog