Most cited article - PubMed ID 20676369
Light perception in two strictly subterranean rodents: life in the dark or blue?
African mole-rats (Bathyergidae, Rodentia) are subterranean rodents that live in extensive dark underground tunnel systems and rarely emerge aboveground. They can discriminate between light and dark but show no overt visually driven behaviours except for light-avoidance responses. Their eyes and central visual system are strongly reduced but not degenerated. Here, we focus on retinal ganglion cells (RGCs). Sighted mammals have numerous RGC types with distinct morphological and functional properties that encode different aspects of a visual scene. We analysed the morphological diversity of 216 intracellularly dye-injected RGCs in the giant mole-rat (Fukomys mechowii) and 48 RGCs in Ansell's mole-rat (Fukomys anselli). Using a hierarchical cluster analysis on 11 morphological parameters, we show that both species possess at least five RGC types with distinct dendritic field sizes and branching patterns. These resemble some RGC types of the mouse and rat, but mole-rat RGCs feature overall sparser and more asymmetric branching patterns. The dendritic trees of most RGCs in all clusters are monostratified in the inner plexiform layer, but bistratified and multistratified/diffuse cells also exist. Thus, although RGC morphologies have become disorganized, the basic retinal organization principle of parallel information processing by distinct RGC types is retained.
- Keywords
- Fukomys, microphthalmia, mole-rats, ocular regression, retinal ganglion cells, subterranean mammals,
- MeSH
- Dendrites MeSH
- Mole Rats * anatomy & histology physiology MeSH
- Retinal Ganglion Cells * cytology classification physiology MeSH
- Cluster Analysis MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Subterranean common mole-rats of the genus Fukomys (family Bathyergidae) live in large, cooperatively-breeding families. Odor cues have been hypothesized to play an important role in mediating social behaviors in the underground ecotope, but only little is known about the role of olfactory signaling in burrowing mammals. Here we characterize the so far neglected perioral glands of Fukomys and other African mole-rats as an important source of olfactory social information. Histology demonstrates these structures to be derived sebaceous glands that are developed regardless of sex and reproductive status. However, gland activity is higher in Fukomys males, leading to sexually dimorphic patterns of stain and clotting of the facial pelage. Behavioral assays revealed that conspecifics prefer male but not female perioral swabs over scent samples from the back fur and that male sebum causes similar attraction as anogenital scent, a known source of social information in Fukomys. Finally, we assessed volatile compounds in the perioral sebum of the giant mole-rat (Fukomys mechowii) via GCxGC-MS-based metabolomic profiling. Volatiles display pronounced sex-specific signatures but also allow to differentiate between intrasexual reproductive status groups. These different lines of evidence suggest that mole-rat perioral glands provide complex odor signals which play a crucial role in social communication.
- MeSH
- African People MeSH
- Humans MeSH
- Mole Rats * MeSH
- Reproduction MeSH
- Social Behavior MeSH
- Spalax * MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Several groups of mammals use the Earth's magnetic field for orientation, but their magnetosensory organ remains unknown. The Ansell's mole-rat (Fukomys anselli, Bathyergidae, Rodentia) is a microphthalmic subterranean rodent with innate magnetic orientation behaviour. Previous studies on this species proposed that its magnetoreceptors are located in the eye. To test this hypothesis, we assessed magnetic orientation in mole-rats after the surgical removal of their eyes compared to untreated controls. Initially, we demonstrate that this enucleation does not lead to changes in routine behaviours, including locomotion, feeding and socializing. We then studied magnetic compass orientation by employing a well-established nest-building assay under four magnetic field alignments. In line with previous studies, control animals exhibited a significant preference to build nests in magnetic southeast. By contrast, enucleated mole-rats built nests in random magnetic orientations, suggesting an impairment of their magnetic sense. The results provide robust support for the hypothesis that mole-rats perceive magnetic fields with their minute eyes, probably relying on magnetite-based receptors in the cornea.
- Keywords
- animal orientation, magnetic sense, magnetite, mole-rat, sensory biology,
- MeSH
- Locomotion MeSH
- Magnetic Fields MeSH
- Magnetics MeSH
- Mole Rats * MeSH
- Orientation * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
African mole-rats are subterranean rodents that spend their whole life in underground burrow systems. They show a range of morphological and physiological adaptations to their ecotope, for instance severely reduced eyes and specialized somatosensory, olfactory, and auditory systems. These adaptations are also reflected in the accessory sensory pathways in the brain that process the input coming from the sensory organs. So far, a brain atlas was available only for the naked mole-rat (Heterocephalus glaber). The Ansell's mole-rat (Fukomys anselli) has been the subject of many investigations in various disciplines (ethology, sensory physiology, and anatomy) including magnetic orientation. It is therefore surprising that an atlas of the brain of this species was not available so far. Here, we present a comprehensive atlas of the Ansell's mole-rat brain based on Nissl and Klüver-Barrera stained sections. We identify and label 375 brain regions and discuss selected differences from the brain of the closely related naked mole-rat as well as from epigeic mammals (rat), with a particular focus on the auditory brainstem. This atlas can serve as a reference for future neuroanatomical investigations of subterranean mammals.
- Keywords
- Nissl, RRID:SCR_005910, RRID:SCR_014199, auditory system, magnetoreception, nervous system, neuroanatomy, rodent, subterranean mammal,
- MeSH
- Anatomy, Artistic * MeSH
- Atlases as Topic * MeSH
- Mole Rats anatomy & histology MeSH
- Brain anatomy & histology MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
Mammals usually possess a majority of medium-wavelength sensitive (M-) and a minority of short-wavelength sensitive (S-) opsins in the retina, enabling dichromatic vision. Unexpectedly, subterranean rodents from the genus Fukomys exhibit an S-opsin majority, which is exceptional among mammals, albeit with no apparent adaptive value. Because thyroid hormones (THs) are pivotal for M-opsin expression and metabolic rate regulation, we have, for the first time, manipulated TH levels in the Ansell's mole-rat (Fukomys anselli) using osmotic pumps. In Ansell's mole-rats, the TH thyroxine (T4) is naturally low, likely as an adaptation to the harsh subterranean ecological conditions by keeping resting metabolic rate (RMR) low. We measured gene expression levels in the eye, RMR, and body mass (BM) in TH-treated animals. T4 treatment increased both, S- and M-opsin expression, albeit M-opsin expression at a higher degree. However, this plasticity was only given in animals up to approximately 2.5 years. Mass-specific RMR was not affected following T4 treatment, although BM decreased. Furthermore, the T4 inactivation rate is naturally higher in F. anselli compared to laboratory rodents. This is the first experimental evidence that the S-opsin majority in Ansell's mole-rats is a side effect of low T4, which is downregulated to keep RMR low.
- MeSH
- Basal Metabolism drug effects MeSH
- Cone Opsins genetics metabolism MeSH
- Mole Rats blood metabolism MeSH
- Retina metabolism MeSH
- Thyroxine blood deficiency MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Cone Opsins MeSH
- Thyroxine MeSH
To what extent can the mammalian visual system be shaped by visual behavior? Here we analyze the shape of the visual fields, the densities and distribution of cells in the retinal ganglion-cell layer and the organization of the visual projections in two species of facultative non-strictly subterranean rodents, Spalacopus cyanus and Ctenomys talarum, aiming to compare these traits with those of phylogenetically closely related species possessing contrasting diurnal/nocturnal visual habits. S. cyanus shows a definite zone of frontal binocular overlap and a corresponding area centralis, but a highly reduced amount of ipsilateral retinal projections. The situation in C. talarum is more extreme as it lacks of a fronto-ventral area of binocular superposition, has no recognizable area centralis and shows no ipsilateral retinal projections except to the suprachiasmatic nucleus. In both species, the extension of the monocular visual field and of the dorsal region of binocular overlap as well as the whole set of contralateral visual projections, appear well-developed. We conclude that these subterranean rodents exhibit, paradoxically, diurnal instead of nocturnal visual specializations, but at the same time suffer a specific regression of the anatomical substrate for stereopsis. We discuss these findings in light of the visual ecology of subterranean lifestyles.
- MeSH
- Superior Colliculi metabolism pathology MeSH
- Rodentia * MeSH
- Vision Disorders diagnosis etiology MeSH
- Retina metabolism pathology MeSH
- Retinal Ganglion Cells metabolism pathology MeSH
- Blindness diagnosis etiology MeSH
- Organ Size MeSH
- Vision, Binocular * MeSH
- Visual Fields MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
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.
- MeSH
- Actins genetics MeSH
- Pain genetics MeSH
- Longevity * MeSH
- Ecosystem * MeSH
- Adaptation, Physiological genetics MeSH
- Genome * MeSH
- Globins genetics MeSH
- Insulin genetics MeSH
- Melatonin genetics MeSH
- Mole Rats genetics MeSH
- Molecular Sequence Data MeSH
- RNA, Ribosomal, 28S genetics MeSH
- Amino Acid Sequence MeSH
- Thermogenesis genetics MeSH
- Transcriptome MeSH
- Genetic Speciation MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Actins MeSH
- Globins MeSH
- Insulin MeSH
- Melatonin MeSH
- RNA, Ribosomal, 28S MeSH