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Adaptations to a subterranean environment and longevity revealed by the analysis of mole rat genomes.
Cell Rep
PUBLISHED: 08-28-2014
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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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Social and Environmental Influences on Daily Activity Pattern in Free-Living Subterranean Rodents: The Case of a Eusocial Bathyergid.
J. Biol. Rhythms
PUBLISHED: 06-12-2014
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Predictable daily activity patterns have been detected repeatedly even in mammals living in stable environments, as is the case for subterranean rodents. Whereas studies on activity of these rodents under laboratory conditions almost exclusively have concerned themselves with the influence of light, many field studies have revealed signs of an association between the activity pattern and daily fluctuations of temperature under the ground. This would assume that behavioral thermoregulation is probably involved. The only exceptions to the relationship between temperature and activity are 2 eusocial mole-rats of the genus Fukomys (Bathyergidae, Rodentia), which indicates that activity patterns could be affected also by social cues. To better understand how social and environmental factors influence the activity pattern in a eusocial mole-rat, we monitored the outside-nest activity in another species of this genus, the Ansell's mole-rat (Fukomys anselli), which has a relatively small body mass, high conductance, and more superficially situated burrows. Its daily activity had 1 prominent peak (around 1400 h), and it was tightly correlated with the temperature measured at depth of foraging burrows. Since F. anselli has high thermoregulatory requirements to maintain stable body temperature below the lower critical temperature, we conclude that the observed pattern is probably the result of minimizing the cost of thermoregulation. There were no significant differences in the daily activity patterns of breeding males and females and nonbreeders. Members of the same family group tended to have more similar activity patterns, but consistent activity synchronization between individuals was not proven. From the comparison of available data on all subterranean rodents, we assume that social cues in communally nesting mole-rats may disrupt (mask) temperature-related daily activity rhythms but probably only if the additional cost of thermoregulation is not too high, as it likely is in the Ansell's mole-rat.
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Parentage analysis of Ansells mole-rat family groups indicates a high reproductive skew despite relatively relaxed ecological constraints on dispersal.
Mol. Ecol.
PUBLISHED: 03-14-2013
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To better understand evolutionary pathways leading to eusociality, interspecific comparisons are needed, which would use a common axis, such as that of reproductive skew, to array species. African mole-rats (Bathyergidae, Rodentia) provide an outstanding model of social evolution because of a wide range of social organizations within a single family; however, their reproductive skew is difficult to estimate, due to their cryptic lifestyle. A maximum skew could theoretically be reached in groups where reproduction is monopolized by a stable breeding pair, but the value could be decreased by breeding-male and breeding-female turnover, shared reproduction and extra-group mating. The frequency of such events should be higher in species or populations inhabiting mesic environments with relaxed ecological constraints on dispersal. To test this prediction, we studied patterns of parentage and relatedness within 16 groups of Ansells mole-rat (Fukomys anselli) in mesic miombo woodland. Contrary to expectation, there was no shared reproduction (more than one breeder of a particular sex) within the studied groups, and proportion of immigrants and offspring not assigned to current breeding males was low. The within-group parentage and relatedness patterns observed resemble arid populations of eusocial Fukomys damarensis, rather than a mesic population of social Cryptomys hottentotus. As a possible explanation, we propose that the extent ecological conditions affect reproductive skew may be markedly affected by life history and natural history traits of the particular species and genera.
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Spatial and temporal activity patterns of the free-living giant mole-rat (Fukomys mechowii), the largest social bathyergid.
PLoS ONE
PUBLISHED: 01-30-2013
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Despite the considerable attention devoted to the biology of social species of African mole-rats (Bathyergidae, Rodentia), knowledge is lacking about their behaviour under natural conditions. We studied activity of the largest social bathyergid, the giant mole-rat Fukomys mechowii, in its natural habitat in Zambia using radio-telemetry. We radio-tracked six individuals during three continuous 72-h sessions. Five of these individuals, including a breeding male, belonged to a single family group; the remaining female was probably a solitary disperser. The non-breeders of the family were active (i.e. outside the nest) 5.8 hours per 24h-day with the activity split into 6.5 short bouts. The activity was more concentrated in the night hours, when the animals also travelled longer distances from the nest. The breeding male spent only 3.2 hours per day outside the nest, utilizing less than 20% of the whole family home range. The dispersing female displayed a much different activity pattern than the family members. Her 8.0 hours of outside-nest activity per day were split into 4.6 bouts which were twice as long as in the family non-breeders. Her activity peak in the late afternoon coincided with the temperature maximum in the depth of 10 cm (roughly the depth of the foraging tunnels). Our results suggest that the breeding individuals (at least males) contribute very little to the work of the family group. Nevertheless, the amount of an individuals activity and its daily pattern are probably flexible in this species and can be modified in response to actual environmental and social conditions.
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Possible incipient sympatric ecological speciation in blind mole rats (Spalax).
Proc. Natl. Acad. Sci. U.S.A.
PUBLISHED: 01-28-2013
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Sympatric speciation has been controversial since it was first proposed as a mode of speciation. Subterranean blind mole rats (Spalacidae) are considered to speciate allopatrically or peripatrically. Here, we report a possible incipient sympatric adaptive ecological speciation in Spalax galili (2n = 52). The study microsite (0.04 km(2)) is sharply subdivided geologically, edaphically, and ecologically into abutting barrier-free ecologies divergent in rock, soil, and vegetation types. The Pleistocene Alma basalt abuts the Cretaceous Senonian Kerem Ben Zimra chalk. Only 28% of 112 plant species were shared between the soils. We examined mitochondrial DNA in the control region and ATP6 in 28 mole rats from basalt and in 14 from chalk habitats. We also sequenced the complete mtDNA (16,423 bp) of four animals, two from each soil type. Remarkably, the frequency of all major haplotype clusters (HC) was highly soil-biased. HCI and HCII are chalk biased. HC-III was abundant in basalt (36%) but absent in chalk; HC-IV was prevalent in basalt (46.5%) but was low (20%) in chalk. Up to 40% of the mtDNA diversity was edaphically dependent, suggesting constrained gene flow. We identified a homologous recombinant mtDNA in the basalt/chalk studied area. Phenotypically significant divergences differentiate the two populations, inhabiting different soils, in adaptive oxygen consumption and in the amount of outside-nest activity. This identification of a possible incipient sympatric adaptive ecological speciation caused by natural selection indirectly refutes the allopatric alternative. Sympatric ecological speciation may be more prevalent in nature because of abundant and sharply abutting divergent ecologies.
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Continuous dental replacement in a hyper-chisel tooth digging rodent.
Proc. Natl. Acad. Sci. U.S.A.
PUBLISHED: 10-10-2011
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Contrary to their reptilian ancestors, which had numerous dental generations, mammals are known to usually develop only two generations of teeth. However, a few mammal species have acquired the ability to continuously replace their dentition by the constant addition of supernumerary teeth moving secondarily toward the front of the jaw. The resulting treadmill-like replacement is thus horizontal, and differs completely from the vertical dental succession of other mammals and their extinct relatives. Despite the developmental implications and prospects regarding the origin of supernumerary teeth, this striking innovation remains poorly documented. Here we report another case of continuous dental replacement in an African rodent, Heliophobius argenteocinereus, which combines this dental system with the progressive eruption of high-crowned teeth. The escalator-like mechanism of Heliophobius constitutes an original adaptation to hyper-chisel tooth digging involving high dental wear. Comparisons between Heliophobius and the few mammals that convergently acquired continuous dental replacement reveal that shared inherited traits, including dental mesial drift, delayed eruption, and supernumerary molars, comprise essential prerequisites to setting up this dental mechanism. Interestingly, these dental traits are present to a lesser extent in humans but are absent in mouse, the usual biological model. Consequently, Heliophobius represents a suitable model to investigate the molecular processes leading to the development of supernumerary teeth in mammals, and the accurate description of these processes could be a significant advance for further applications in humans, such as the regeneration of dental tissues.
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Extended longevity of reproductives appears to be common in Fukomys mole-rats (Rodentia, Bathyergidae).
PLoS ONE
PUBLISHED: 03-16-2011
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African mole-rats (Bathyergidae, Rodentia) contain several social, cooperatively breeding species with low extrinsic mortality and unusually high longevity. All social bathyergids live in multigenerational families where reproduction is skewed towards a few breeding individuals. Most of their offspring remain as reproductively inactive "helpers" in their natal families, often for several years. This "reproductive subdivision" of mole-rat societies might be of interest for ageing research, as in at least one social bathyergid (Ansells mole-rats Fukomys anselli), breeders have been shown to age significantly slower than non-breeders. These animals thus provide excellent conditions for studying the epigenetics of senescence by comparing divergent longevities within the same genotypes without the inescapable short-comings of inter-species comparisons. It has been claimed that many if not all social mole-rat species may have evolved similar ageing patterns, too. However, this remains unclear on account of the scarcity of reliable datasets on the subject. We therefore analyzed a 20-year breeding record of Giant mole-rats Fukomys mechowii, another social bathyergid species. We found that breeders indeed lived significantly longer than helpers (ca. 1.5-2.2fold depending on the sex), irrespective of social rank or other potentially confounding factors. Considering the phylogenetic positions of F. mechowii and F. anselli and unpublished data on a third Fukomys-species (F. damarensis) showing essentially the same pattern, it seems probable that the reversal of the classic trade-off between somatic maintenance and sexual reproduction is characteristic of the whole genus and hence of the vast majority of social mole-rats.
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Light perception in two strictly subterranean rodents: life in the dark or blue?
PLoS ONE
PUBLISHED: 05-13-2010
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The African mole-rats (Bathyergidae, Rodentia) are strictly subterranean, congenitally microphthalmic rodents that are hardly ever exposed to environmental light. Because of the lack of an overt behavioural reaction to light, they have long been considered to be blind. However, recent anatomical studies have suggested retention of basic visual capabilities. In this study, we employed behavioural tests to find out if two mole-rat species are able to discriminate between light and dark, if they are able to discriminate colours and, finally, if the presence of light in burrows provokes plugging behaviour, which is assumed to have a primarily anti-predatory function.
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A seasonal difference of daily energy expenditure in a free-living subterranean rodent, the silvery mole-rat (Heliophobius argenteocinereus; Bathyergidae).
Comp. Biochem. Physiol., Part A Mol. Integr. Physiol.
PUBLISHED: 02-23-2010
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In seasonal climatic regimes, animals have to deal with changing environmental conditions. It is reasonable to expect that seasonal changes are reflected in animal overall energetics. The relation between daily energy expenditure (DEE) and seasonally variable ecological determinants has been studied in many free-living small mammals; however with inconsistent results. Subterranean mammals, i.e. fossorial (burrowing) mammals which live and forage underground, live in a seasonally and diurnally thermally stable environment and represent a suitable model to test seasonality in DEE in respect to seasonal changes, particularly those in soil characteristics and access to food supply. Both factors are affected by seasonal rainfall and are supposed to fundamentally determine activity of belowground dwellers. These ecological constraints are pronounced in some tropical regions, where two distinct periods, dry and rainy seasons, regularly alternate. To explore how a tropical mammal responds to an abrupt environmental change, we determined DEE, resting metabolic rate (RMR) and sustained metabolic scope (SusMS) in a solitary subterranean rodent, the silvery mole-rat, at the end of dry season and the onset of rainy season. Whereas RMR did not differ between both periods, mole-rats had 1.4 times higher DEE and SusMS after the first heavy rains. These findings suggest that rainfall is an important environmental factor responsible for higher energy expenditure in mole-rats, probably due to increased burrowing activity. SusMS in the silvery mole-rat is comparable to values in other bathyergids and all bathyergid values rank among the lowest SusMS found in endothermic vertebrates.
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Social structure predicts genital morphology in African mole-rats.
PLoS ONE
PUBLISHED: 06-11-2009
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African mole-rats (Bathyergidae, Rodentia) exhibit a wide range of social structures, from solitary to eusocial. We previously found a lack of sex differences in the external genitalia and morphology of the perineal muscles associated with the phallus in the eusocial naked mole-rat. This was quite surprising, as the external genitalia and perineal muscles are sexually dimorphic in all other mammals examined. We hypothesized that the lack of sex differences in naked mole-rats might be related to their unusual social structure.
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