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

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.

The role of ambient temperature and light as cues in the control of circadian rhythms of Damaraland mole-rat.

Light is considered the primary entrainer for mammalian biological rhythms, including locomotor activity (LA). However, mammals experience different environmental and light conditions, which include those predominantly devoid of light stimuli, such as those experienced in subterranean environments. In this study, we investigated what environmental cue (light or ambient temperature (Ta)) is the strongest modulator of circadian rhythms, by using LA as a proxy, in mammals that experience a lifestyle devoid of light stimuli. To address this question, this study exposed a subterranean African mole-rat species, the Damaraland mole-rat (Fukomys damarensis), to six light and Ta cycles in different combinations. Contrary to previous literature, when provided with a reliable light cue, Damaraland mole rats exhibited nocturnal, diurnal, or arrhythmic LA patterns under constant Ta. While under constant darkness and a 24-hour Ta cycle mimicking the burrow environment, all mole-rats were most active during the coolest 12-hour period. This finding suggests that in a subterranean environment, which receives no reliable photic cue, the limited heat dissipation and energy constraints during digging activity experienced by Damaraland mole-rats make Ta a reliable and consistent "time-keeping" variable. More so, when providing a reliable light cue (12 light: 12 dark) to Damaraland mole-rats under a 24-hour Ta cycle, this study presents the first evidence that cycles of Ta affect the LA rhythm of a subterranean mammal more strongly than cycles of light and darkness. Once again, Damaraland mole-rats were more active during the coolest 12-hour period regardless of whether this fell during the light or dark phase. However, conclusive differentiation of entrainment to Ta from that of masking was not achieved in this study, and as such, we have recommended future research avenues to do so.

Sleep in the East African root rat, Tachyoryctes splendens.

The present study reports the results of an electrophysiological analysis of sleep in the East African root rat, Tachyoryctes splendens, belonging to the rodent subfamily Spalacinae. Telemetric electroencephalographic (EEG) and electromyographic recordings, with associated video recording, on three root rats over a continuous 72 h period (12 h light/12 h dark cycle) were analyzed. The analysis revealed that the East African root rat has a total sleep time (TST) of 8.9 h per day. Despite this relatively short total sleep time in comparison to fossorial rodents, nonrapid eye movement (non-REM) sleep and rapid eye movement (REM) sleep states showed similar physiological signatures to that observed in other rodents and no unusual sleep states were observed. REM occupied 19.7% of TST, which is within the range observed in other rodents. The root rats were extremely active during the dark period, and appeared to spend much of the light period in quiet wake while maintaining vigilance (as determined from both EEG recordings and behavioral observation). These recordings were made under normocapnic environmental conditions, which contrasts with the hypercapnic environment of their natural burrows.

Lovers, not fighters: docility influences reproductive fitness, but not survival, in male Cape ground squirrels, Xerus inauris.

Over their lifetime, individuals may use different behavioural strategies to maximize their fitness. Some behavioural traits may be consistent among individuals over time (i.e., 'personality' traits) resulting in an individual behavioural phenotype with different associated costs and benefits. Understanding how behavioural traits are linked to lifetime fitness requires tracking individuals over their lifetime. Here, we leverage a long-term study on a multi-year living species (maximum lifespan ~ 10 years) to examine how docility (an individual's reaction to trapping and handling) may contribute to how males are able to maximize their lifetime fitness. Cape ground squirrels are burrowing mammals that live in social groups, and although males lack physical aggression and territoriality, they vary in docility. Males face high predation risk and high reproductive competition and employ either of two reproductive tactics ('natal' or 'band') which are not associated with different docility personalities. We found that although more docile individuals sired more offspring on an annual basis, docility did not affect an individual's long-term (lifetime) reproductive output. Survival was not associated with docility or body condition, but annual survival was influenced by rainfall. Our findings suggest that although docility may represent a behavioural strategy to maximize fitness by possibly playing a role in female-male associations or female mate-choice, variations in docility within our study population is likely maintained by other environmental drivers. However, individual variations in behaviours may still contribute as part of the 'tool kit' individuals use to maximize their lifetime fitness. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-023-03421-8.

Patterns of Genetic Diversity and Gene Flow Associated With an Aridity Gradient in Populations of Common Mole-rats, Cryptomys hottentotus hottentotus.

Genetic adaptation is the change of a population toward a phenotype that best fits the present ecological conditions of the environment it inhabits. As environmental conditions change, allele frequencies shift, resulting in different populations of the same species possessing genetic variation and divergent phenotypes. Cooperatively breeding common mole-rats (Cryptomys hottentotus hottentotus) inhabit environments along an aridity gradient in South Africa, which provides an opportunity for local genetic adaptations to occur. Using one mitochondrial gene (cytochrome b) and 3,540 SNP loci across the whole genome, we determined the phylogenetic relationship, population structure and genetic diversity of five populations of C. h. hottentotus located along an aridity gradient. Mitochondrial data identified population-specific clades that were less distinct in the two mesic populations, potentially indicating historical or recent gene flow, or the retention of ancestral haplotypes. Arid and semi-arid populations formed a distinct cluster from the non-arid populations. Genetic diversity and gene flow were higher in arid-dwelling individuals, suggesting greater connectivity and interactions between colonies in arid regions in comparison to mesic ones. Using an Aridity Index, we determined that isolation by environment, rather than isolation by geographical distance, best explains the genetic distance between the populations. Further analyses using target loci may determine if there are differing underlying genetic adaptations among populations of C. h. hottentotus. These analyses could help unravel population differences in response to environmental factors within a subspecies of bathyergid mole-rat and determine the adaptive capacity of this small nonmigratory subterranean rodent species in response to aridification in the face of climate change.

New insights into morphological adaptation in common mole-rats (Cryptomys hottentotus hottentotus) along an aridity gradient.

Morphological adaptation is the change in the form of an organism that benefits the individual in its current habitat. Mole-rats (family Bathyergidae), despite being subterranean, are impacted by both local and broad-scale environmental conditions that occur above ground. Common mole-rats (Cryptomys hottentotus hottentotus) present an ideal mammalian model system for the study of morphological variation in response to ecology, as this species is found along an aridity gradient and thus can be sampled from geographically non-overlapping populations of the same species along an environmental longitudinal cline. Using the mass of five internal organs, ten skeletal measurements and 3D morphometric analyses of skulls, we assessed the morphology of wild non-breeding individuals from five common mole-rat populations in South Africa. We found that the body mass and mean relative mass of the spleen and kidneys in arid populations was larger, and individuals from arid regions possessed shorter legs and larger inter-shoulder widths compared to individuals from mesic regions. Additionally, arid populations demonstrated greater skull depth, and shape change of features such as angular processes of the lower jaw than mesic individuals, indicating that these distinct geographic populations show differences corresponding to the aridity gradient, potentially in response to environmental factors such as the variation in food sources found between different habitats, in addition to different soil compositions found in the different regions. Arid populations potentially require a stronger jaw and neck musculature associated with mastication to chew xeric-adapted plants and to dig through hard soil types, whereas mesic populations excavate through soft, looser soil and may make use of their front limbs to aid the movement of soils when digging. Aridity influences the morphology of this species and could indicate the impact of environmental changes on speciation and mammalian skull morphology.

Naked mole-rats have distinctive cardiometabolic and genetic adaptations to their underground low-oxygen lifestyles.

The naked mole-rat Heterocephalus glaber is a eusocial mammal exhibiting extreme longevity (37-year lifespan), extraordinary resistance to hypoxia and absence of cardiovascular disease. To identify the mechanisms behind these exceptional traits, metabolomics and RNAseq of cardiac tissue from naked mole-rats was compared to other African mole-rat genera (Cape, Cape dune, Common, Natal, Mahali, Highveld and Damaraland mole-rats) and evolutionarily divergent mammals (Hottentot golden mole and C57/BL6 mouse). We identify metabolic and genetic adaptations unique to naked mole-rats including elevated glycogen, thus enabling glycolytic ATP generation during cardiac ischemia. Elevated normoxic expression of HIF-1α is observed while downstream hypoxia responsive-genes are down-regulated, suggesting adaptation to low oxygen environments. Naked mole-rat hearts show reduced succinate levels during ischemia compared to C57/BL6 mouse and negligible tissue damage following ischemia-reperfusion injury. These evolutionary traits reflect adaptation to a unique hypoxic and eusocial lifestyle that collectively may contribute to their longevity and health span.

Where Do Core Thalamocortical Axons Terminate in Mammalian Neocortex When There Is No Cytoarchitecturally Distinct Layer 4?

Although the mammalian cerebral cortex is most often described as a hexalaminar structure, there are cortical areas (primary motor cortex) and species (elephants, cetaceans, and hippopotami), where a cytoarchitecturally indistinct, or absent, layer 4 is noted. Thalamocortical projections from the core, or first order, thalamic system terminate primarily in layers 4/inner 3. We explored the termination sites of core thalamocortical projections in cortical areas and in species where there is no cytoarchitecturally distinct layer 4 using the immunolocalization of vesicular glutamate transporter 2, a known marker of core thalamocortical axon terminals, in 31 mammal species spanning the eutherian radiation. Several variations from the canonical cortical column outline of layer 4 and core thalamocortical inputs were noted. In shrews/microchiropterans, layer 4 was present, but many core thalamocortical projections terminated in layer 1 in addition to layers 4 and inner 3. In primate primary visual cortex, the sublaminated layer 4 was associated with a specialized core thalamocortical projection pattern. In primate primary motor cortex, no cytoarchitecturally distinct layer 4 was evident and the core thalamocortical projections terminated throughout layer 3. In the African elephant, cetaceans, and river hippopotamus, no cytoarchitecturally distinct layer 4 was observed and core thalamocortical projections terminated primarily in inner layer 3 and less densely in outer layer 3. These findings are contextualized in terms of cortical processing, perception, and the evolutionary trajectory leading to an indistinct or absent cortical layer 4.

Adult stem cell activity in naked mole rats for long-term tissue maintenance.

The naked mole rat (NMR), Heterocephalus glaber, the longest-living rodent, provides a unique opportunity to explore how evolution has shaped adult stem cell (ASC) activity and tissue function with increasing lifespan. Using cumulative BrdU labelling and a quantitative imaging approach to track intestinal ASCs (Lgr5+) in their native in vivo state, we find an expanded pool of Lgr5+ cells in NMRs, and these cells specifically at the crypt base (Lgr5+CBC) exhibit slower division rates compared to those in short-lived mice but have a similar turnover as human LGR5+CBC cells. Instead of entering quiescence (G0), NMR Lgr5+CBC cells reduce their division rates by prolonging arrest in the G1 and/or G2 phases of the cell cycle. Moreover, we also observe a higher proportion of differentiated cells in NMRs that confer enhanced protection and function to the intestinal mucosa which is able to detect any chemical imbalance in the luminal environment efficiently, triggering a robust pro-apoptotic, anti-proliferative response within the stem/progenitor cell zone.