African mole-rats are subterranean rodents, which rarely if ever leave the safety of their burrow systems. The environment of the burrows is humid, with relatively stable temperatures, and may have a ...hypoxic and hypercapnic atmosphere. One of crucial problems related to the subterranean way of life in mammals is avoidance of overheating, because traditional mammalian cooling mechanisms are not effective under high humidity. In African mole-rats, a variety of adaptations have evolved in response to this and other challenges of the underground ecotope. Traditionally, attention has been devoted mainly to the naked mole-rat Heterocephalus glaber, which became popular as a result of its eusociality and absence of fur, both being unique phenomena in small mammals. Despite more recent research, information on other species is still relatively limited and patchy. I review the results of studies on African mole-rats that are relevant for the understanding of their energetics and thermal biology. Attention is paid to the parameters of the burrow environment, which represent the main selection pressures shaping their physiology. In addition, an overview is given of the morphological, physiological and behavioural adaptations helping mole-rats to face temperature extremes, mechanisms by which they deal with a surplus of metabolic heat and how changes in ambient temperature influence their daily activity. The naked mole-rat is compared to its furred relatives to determine whether this species is really exceptional from the point of thermal biology. An ordination analysis was conducted using published data on mole-rat body temperature, thermoneutral zone, resting metabolic rate and thermal conductance. Most of the variability in these characteristics was found to be explained by body mass, followed by temperature characteristics of climate, but not precipitation, of the species distributional ranges. This analysis shows that the naked mole-rat is comparable to the other mole-rat species in these physiological characteristics.
•African mole-rats face thermally challenging environment in their burrow systems.•Various adaptations which evolved to thrive in such conditions are reviewed here.•Body mass explains most of the variability in mole-rat energetics.•Temperature characteristics of climate have also significant influence.•More than an outlier, H. glaber is on the gradient of mole-rat thermoregulation.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPUK, ZAGLJ, ZRSKP
The evolution of endothermy in vertebrates is a major research topic in recent decades that has been tackled by a myriad of research disciplines including paleontology, anatomy, physiology, ...evolutionary and developmental biology. The ability of most mammals to maintain a relatively constant and high body temperature is considered a key adaptation, enabling them to successfully colonize new habitats and harsh environments. It has been proposed that in mammals the anterior nasal cavity, which houses the maxilloturbinal, plays a pivotal role in body temperature maintenance, via a bony system supporting an epithelium involved in heat and moisture conservation. The presence and the relative size of the maxilloturbinal has been proposed to reflect the endothermic conditions and basal metabolic rate in extinct vertebrates. We show that there is no evidence to relate the origin of endothermy and the development of some turbinal bones by using a comprehensive dataset of µCT-derived maxilloturbinals spanning most mammalian orders. Indeed, we demonstrate that neither corrected basal metabolic rate nor body temperature significantly correlate with the relative surface area of the maxilloturbinal. Instead, we identify important variations in the relative surface area, morpho-anatomy, and complexity of the maxilloturbinal across the mammalian phylogeny and species ecology.
ABSTRACT
Naked mole‐rats express many unusual traits for such a small rodent. Their morphology, social behaviour, physiology, and ageing have been well studied over the past half‐century. Many early ...findings and speculations about this subterranean species persist in the literature, although some have been repeatedly questioned or refuted. While the popularity of this species as a natural‐history curiosity, and oversimplified story‐telling in science journalism, might have fuelled the perpetuation of such misconceptions, an accurate understanding of their biology is especially important for this new biomedical model organism. We review 28 of these persistent myths about naked mole‐rat sensory abilities, ecophysiology, social behaviour, development and ageing, and where possible we explain how these misunderstandings came about.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
We provide an annotated checklist of rodents of Ethiopia. For each species we show a distributional map based on critically revised data from: (1) published literature; (2) museum collections, ...including records in the Global Biodiversity Information Facility (GBIF); and (3) recent field surveys performed in the last three decades as part of the Joint Ethio-Russian Biological Expedition (JERBE) and Ethio-Czech Research Projects. In most cases recent material was analysed in detail using genetic and/or morphometric approaches. In total, the Ethiopian rodent fauna consists of 104 species (40 genera, 10 families). Compared to previous studies we were not able to confirm the presence of 12 species, probably due to a lack of data from arid lowland areas, though some of these species may be extinct. We report the occurrence of > 40 species not previously included in a checklist published in 1996 (with many species still requiring formal description). Of the total number of species recorded, a high proportion are endemics of Ethiopian Highlands (43 species = 41.3 %), followed by those living in Somali-Masai (27) and Sudanian (13) savanna. The checklist confirms an unusually high level of Ethiopian rodent biodiversity, which should serve as a basis for conservation.
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IZUM, KILJ, NUK, PILJ, PNG, SAZU, UL, UM, UPUK
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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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
It is supposed that the subterranean lifestyle in mammals is reflected in ear morphology and tuning of hearing to low frequencies. We studied two root-rat species to see if their ear morphology ...reflects the difference in the amount of their surface activity. Whereas the more subterranean
Tachyoryctes splendens
possesses shorter pinnae as expected, it has smaller bullae compared to the more epigeic
Tachyoryctes macrocephalus
. The ratio between the eardrum and the stapedial footplate area and the ratio between the mallear and the incudal lever were lower in
T. splendens
(19.3 ± 0.3 and 1.9 ± 0.0, respectively) than in
T. macrocephalus
(21.8 ± 0.6 and 2.1 ± 0.1), probably reflecting the latter’s higher surface activity. The cochlea in both species has 3.5 coils, yet the basilar membrane is longer in the smaller
T. splendens
(13.0 ± 0.5 versus 11.4 ± 0.7 mm), which indicates its wider hearing range and/or higher sensitivity (to some frequencies). In both root-rat species, the highest density of outer hair cells (OHC) was in the apical part of the cochlea, while the highest density of inner hair cells (IHC) was in its middle part. This OHC density pattern corresponds with good low-frequency hearing, whereas the IHC pattern suggests sensitivity to higher frequencies.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Aim: Grammomys are mostly arboreal rodents occurring in forests, woodlands and thickets throughout sub-Saharan Africa. We investigated whether the divergence events within the genus follow the ...existing evolutionary scenario for the development of African forests since the late Miocene. Location: Sub-Saharan African forests and woodlands. Methods: We inferred the molecular phylogeny of Grammomys using Bayesian and maximum likelihood methods and DNA sequences of 351 specimens collected from across the distribution of the genus. We mapped the genetic diversity, estimated the divergence times by a relaxed clock model and compared evolution of the genus with forest history. Results: Phylogenetic analysis confirms the monophyly of Grammomys and reveals five main Grammomys lineages with mainly parapatric distributions: (1) the poensis group in Guineo-Congolese forests; (2) the selousi group with a distribution mainly in coastal forests of southern and eastern Africa; (3) the dolichurus group restricted to the easternmost part of South Africa; (4) the macmillani group in the northern part of eastern and Central Africa with one isolated species in Guiñean forests; and (5) the surdaster group, widely distributed in eastern Africa south of the equator. Every group contains well supported sublineages suggesting the existence of undescribed species. The earliest split within the genus (groups 1 vs. 2-5) occurred in the late Miocene and coincides with the formation of the Rift Valley which resulted in the east-west division of the initially pan-African forest. The subsequent separation between groups (2 vs. 3-5) also dates to the end of the Miocene and suggests the split between Grammomys from coastal to upland forests in eastern Africa followed by a single dispersal event into western Africa during the Pleistocene. Conclusions: The evolutionary history of the genus Grammomys closely reflects the accepted scenario of major historical changes in the distribution of tropical African forests since the late Miocene.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
The evolution of species is governed by complex phenomena in which biological and environmental features may interact dynamically. Subterranean mammals dig tunnels whose diameter minimizes energetic ...costs during excavations and display anatomical adaptations in order to burrow structurally stable tunnels according to specific features of the soil. These animals weight from less than 50 g up to 1-2 kg, and dig tunnels with diameters from 3 to 15 cm. The use of allometric laws has enabled these data to be correlated. However, since tunnels need to be stable with respect to the geomechanical characteristics of the resident soils, a mathematical treatment linking the admissible dimensions of tunnels to the environment here suggests a mechanically grounded correlation between the body mass of subterranean mammals and the maximum dimensions of tunnels. Remarkably, such theoretical findings reflect very well the empirical allometric relationship and contribute to explain the wide differences observed in body sizes of subterranean mammals. In this respect, a far from ancillary role of environmental mechanics on the morphological evolution of subterranean mammals can be hypothesized.
Subterranean mammals spend their lives in dark, unventilated environments that are rich in carbon dioxide and ammonia and low in oxygen. Many of these animals are also long-lived and exhibit reduced ...aging-associated diseases, such as neurodegenerative disorders and cancer. We sequenced the genome of the Damaraland mole rat (DMR, Fukomys damarensis) and improved the genome assembly of the naked mole rat (NMR, Heterocephalus glaber). Comparative genome analyses, along with the transcriptomes of related subterranean rodents, revealed candidate molecular adaptations for subterranean life and longevity, including a divergent insulin peptide, expression of oxygen-carrying globins in the brain, prevention of high CO2-induced pain perception, and enhanced ammonia detoxification. Juxtaposition of the genomes of DMR and other more conventional animals with the genome of NMR revealed several truly exceptional NMR features: unusual thermogenesis, an aberrant melatonin system, pain insensitivity, and unique processing of 28S rRNA. Together, these genomes and transcriptomes extend our understanding of subterranean adaptations, stress resistance, and longevity.
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•Genome of the Damaraland mole rat and improved genome assembly of the naked mole rat•Transcriptomes of subterranean rodents and comparative genome analyses•Common adaptations for subterranean life: arginase, globins, and Na(V)1.7•Unique NMR adaptations: UCP1, 28S rRNA processing, melatonin, actin, and pain systems
Subterranean rodents thrive in harsh underground environments. Many are long-lived and hold promise as animal models of successful aging and sustained good health. Here, Fang et al. sequence the genome of the Damaraland mole rat (Fukomys damarensis), improve the genome assembly of the naked mole rat (Heterocephalus glaber), and compare the transcriptomes of subterranean rodents. Comparative analyses reveal candidate molecular adaptations for subterranean life and longevity, as well as traits unique to the naked mole rat, including unusual thermogenesis and novel processing of 28S rRNA.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPUK, ZAGLJ, ZRSKP
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•Most comprehensive phylogenetic analysis of the endemic Ethiopian rodent genus.•Complex reticulate evolution affected by Pleistocene climate changes.•Secondary contacts resulted in ...mito-nuclear discordance.•Great Rift Valley is not absolute barrier to gene flow for Afroalpine species.•Repeated ecological speciation at elevation gradient is supposed.
The Ethiopian highlands are the most extensive complex of mountainous habitats in Africa. The presence of the Great Rift Valley (GRV) and the striking elevational ecological gradients inhabited by recently radiated Ethiopian endemics, provide a wide spectrum of model situations for evolutionary studies. The extant species of endemic rodents, often markedly phenotypically differentiated, are expected to possess complex genetic features which evolved asa consequence of the interplay between geomorphology and past climatic changes. In this study, we used the largest available multi-locus genetic dataset of the murid genus Stenocephalemys (347 specimens from ca 40 localities across the known distributional area of all taxa) to investigate the relative importance of disruptive selection, temporary geographic isolation and introgression in their adaptive radiations in the Pleistocene. We confirmed the four main highly supported mitochondrial (mtDNA) clades that were proposed as four species in a previous pilot study: S. albipes is a sister species of S. griseicauda (both lineages are present on both sides of the GRV), while the second clade is formed by two Afro-alpine species, S. albocaudata (east of GRV) and the undescribed Stenocephalemys sp. A (west of GRV). There is a clear elevational gradient in the distribution of the Stenocephalemys taxa with two to three species present at different elevations of the same mountain range. Surprisingly, the nuclear species tree corresponded only a little to the mtDNA tree. Multispecies coalescent models based on six nuclear markers revealed the presence of six separate gene pools (i.e. candidate species), with different topology. Phylogenetic analysis, together with the geographic distribution of the genetic groups, suggests a complex reticulate evolution. We propose a scenario that involves (besides classical allopatric speciation) two cases of disruptive selection along the elevational ecological gradient, multiple crosses of GRV in dry and cold periods of the Pleistocene, followed by hybridization and mtDNA introgression on imperfect reproductive barriers. Spatial expansion of the currently most widespread “albipes” mtDNA clade was followed by population fragmentation, lineage sorting and again by hybridization and mtDNA introgression. Comparison of this genetic structure to other Ethiopian endemic taxa highlight the geographical areas of special conservation concern, where more detailed biodiversity studies should be carried out to prevent many endemic taxa from going extinct even before they are recognized.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPUK, ZRSKP
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