Subterranean Rodent Species Research Articles

Assessing spatial learning and working memory in plateau zokors in comparison with plateau pikas and laboratory rats

Spatial learning and memory skills are imperative for the survival and fitness of subterranean rodents because of the harsh underground niche in which they live that necessitates the avoidance of higher energy expenditures or probable conflicts with conspecifics or predators. Our study aims to assess the spatial learning and working memory performance of a subterranean rodent species, plateau zokors (Eospalax baileyi), compared to that of the surface-dwelling plateau pikas (Ochotona curzoniae) and laboratory rats (Rattus norvegicus) which spend a considerable time of their lives above ground. Animals were tested with a spatial delayed alternation task in a T-maze for six consecutive days. Plateau zokors showed less efficient learning and working memory capacity in the T-maze compared to plateau pikas and laboratory rats, which maintained accurate and consistent increased spatial learning rates and working memory performances. The three species did not show bias towards a certain arm of the maze. Additionally, clear sex-specific differences were observed in the laboratory rats regarding spatial learning and working memory functions, while in pikas and zokors, no sex-specific variations were detected. The latency to accomplish the task was significantly lower in rats than in pikas and zokors, but no sex-specific differences were detected in all the species. The inferior performance of plateau zokors, compared to pikas and rats, in the T-maze might imply that although the functional significance of working memory may overlap in diverse taxonomic groups, the adaptive value thereof may differ considerably across taxa on account of the divergence in environmental stability, domestication, habitat structure, behavioural needs and the available sensory cues between species.

Rapid molecular evolution of pain insensitivity in multiple African rodents.

Noxious substances, called algogens, cause pain and are used as defensive weapons by plants and stinging insects. We identified four previously unknown instances of algogen-insensitivity by screening eight African rodent species related to the naked mole-rat with the painful substances capsaicin, acid (hydrogen chloride, pH 3.5), and allyl isothiocyanate (AITC). Using RNA sequencing, we traced the emergence of sequence variants in transduction channels, like transient receptor potential channel TRPA1 and voltage-gated sodium channel Nav1.7, that accompany algogen insensitivity. In addition, the AITC-insensitive highveld mole-rat exhibited overexpression of the leak channel NALCN (sodium leak channel, nonselective), ablating AITC detection by nociceptors. These molecular changes likely rendered highveld mole-rats immune to the stings of the Natal droptail ant. Our study reveals how evolution can be used as a discovery tool to find molecular mechanisms that shut down pain.

How the mole-rat lost its pain

Pain Insensitivity Pain alerts our bodies that something is amiss and typically we stop the pain-causing activity. Numerous species of plants and prey animals take advantage of this response by producing pain-causing substances that are released during predation attempts. In turn, species that encounter these substances often evolve ways of turning off the pain-producing mechanism. Eigenbrod et al. searched RNA transcripts in eight species of subterranean rodents related to pain-resistant naked mole-rats. They found multiple changes to ion channels involved in pain across the different species. Understanding such adaptations could elucidate pain mechanisms and help us develop approaches for pain relief. Science , this issue p. [852][1] [1]: /lookup/doi/10.1126/science.aau0236

Do subterranean mammals use the Earth's magnetic field as a heading indicator to dig straight tunnels?

Subterranean rodents are able to dig long straight tunnels. Keeping the course of such “runways” is important in the context of optimal foraging strategies and natal or mating dispersal. These tunnels are built in the course of a long time, and in social species, by several animals. Although the ability to keep the course of digging has already been described in the 1950s, its proximate mechanism could still not be satisfactorily explained. Here, we analyzed the directional orientation of 68 burrow systems in five subterranean rodent species (Fukomys anselli, F. mechowii, Heliophobius argenteocinereus, Spalax galili, and Ctenomys talarum) on the base of detailed maps of burrow systems charted within the framework of other studies and provided to us. The directional orientation of the vast majority of all evaluated burrow systems on the individual level (94%) showed a significant deviation from a random distribution. The second order statistics (averaging mean vectors of all the studied burrow systems of a respective species) revealed significant deviations from random distribution with a prevalence of north–south (H. argenteocinereus), NNW–SSE (C. talarum), and NE–SW (Fukomys mole-rats) oriented tunnels. Burrow systems of S. galili were randomly oriented. We suggest that the Earth’s magnetic field acts as a common heading indicator, facilitating to keep the course of digging. This study provides a field test and further evidence for magnetoreception and its biological meaning in subterranean mammals. Furthermore, it lays the foundation for future field experiments.

Gender difference in unconditioned and conditioned predator fear responses in Smith's zokors (Eospalax smithii)

Risk taking is imperative for the survival and fitness of animals since they constantly face innumerable threats from various sources. Indeed, the ability of the individual to balance between the costs and benefits of various options and adopt a wise decision is critical for the well-being of the animal. In the current study, we investigated gender differences in risk taking and decision making in male and female Smith's zokors (Eospalax smithii), a subterranean rodent species, in the defensive withdrawal apparatus (DWA) under novel, predator and conditioned contexts. Under novel context, males showed more exploratory and less hiding behavior than females especially during the first half of the testing session. However, under predator and conditioned contexts, non-significant sexually dimorphic behavioral differences were observed. Nevertheless, analysis of the performance of each gender separately across the three contexts revealed that males showed strong aversion to the predator and conditioned contexts. By contrast, females did not significantly vary their behavioral responses when exposed to the predator and conditioned cues. Our results suggest that males are more inclined to indulge in riskier exploratory activities while females may be regarded as risk-aversive. The current findings highlighted the functional significance of the trade-off between risk and exploration in the natural environment such that male and female zokors differed in how they gather and process information during risky confrontations that ultimately elicit significant variations in their decision-making and coping strategies to dangerous events.

Evolution of circadian genes PER and CRY in subterranean rodents

There is considerable interest in examining how circadian rhythms function and evolve in subterranean rodents that spend its entire life in underground, darkness environments. Here, we investigated the evolution of PER and CRY genes that are important for mammalian biological clocks in the subterranean rodents. We performed phylogenetic analyses using newly sequenced PER and CRY from the subterranean rodent Lasiopodomys mandarinus, the related aboveground rodent Lasiopodomys brandtii, sequences from other rodents available in public databases. The constructed phylogenetic tree revealed no convergence among subterranean rodents. Phylogenetic and selection-pressure analyses revealed the effect of purifying selection (ω < 1) on PER and CRY in subterranean rodents. Additionally, evidence of positive selection on the CRY1 and PER3 genes in several subterranean rodent species suggests adaptations to a dark habitat. Most of the positively selected sites in CRY1 and PER3 were on the C-terminus. Our findings suggest that PER and CRY are highly conserved during evolution as subterranean rodents adapted to the darkness environment, and that the C-terminal domain of CRY1 and PER3 may be the core regulatory structure of circadian rhythms. The study advances our understanding of how major circadian genes evolved in subterranean rodents.

Prenatal predatory stress in a wild species of subterranean rodent: Do ecological stressors always have a negative effect on the offspring?

In pregnant females, a failed predatory event not only induces individual responses but also represents a significant change in the developmental environment of the offspring, which may lead to modifications in their phenotype that may persist at different stages of life. We evaluate whether prenatal exposure to predatory cues affects anxiety behavior, behavioral response to predator cues, stress response to immobilization, and immune response to sheep red blood cells (SRBC) and phytohemagglutinin (PHA) in juveniles of the subterranean rodent Ctenomys talarum. We found that prenatal predator stress (PPS) (1) increased juvenile anxiety-like behaviors and the appearance of antipredator behaviors, (2) did not affect the response of offspring to predatory stressors, and (3) did not influence the physiological response of juveniles to stressors (immobilization) nor the immunological responses to SRBC and PHA challenges. This work shows the influence of PPS on the development of behavioral responses in the offspring, whom displayed a state of anxiety and behavioral changes associated with decreased locomotor activity and avoidance behaviors. Thus, these individuals prenatally exposed to predatory cues show behavioral adaptations that may contribute to avoid predators in the adult life.

Interspecific interactions may not influence home range size in subterranean rodents: a case study of two tuco-tuco species (Rodentia: Ctenomyidae)

Coexistence between species with similar niche requirements is often facilitated by displacement of morphological, behavioral, or physiological characteristics. Experiments comparing treatments with and without the presence of potential competitors are ideal for testing hypotheses of interspecific competition. Here, we investigate a fundamental aspect in the natural history of a species: the home range. We determined whether co-occurrence can influence the home range size of 2 subterranean rodent species, Ctenomys flamarioni and C. minutus. We evaluated home range size in populations of both species in allopatry and sympatry along the coastal plain of southern Brazil. Animals were radiotracked, and the home range size of each individual was estimated using grid cells and minimum convex polygon methods. We found no significant differences in home range size between sites or species, and the interaction was nonsignificant. We also found no relationship between home range size and body mass or sex. Our results suggest that co-occurrence may not influence home range size in these species, perhaps due to environmental adaptations that facilitate coexistence (e.g., microhabitat segregation and dietary modifications). Further, the characteristics of the sandy dune habitat may act as environmental filters, favoring similar home range sizes for both species. A coexistência entre espécies com requerimento similares de nicho é normalmente facilitada por deslocamento de caractere morfológico, comportamental ou fisiológico. Experimentos comparando tratamentos com e sem a presença de competidores potenciais são ideais para testar hipóteses sobre competição interespecífica. Neste estudo nós investigamos um aspecto fundamental da história natural de uma espécie: a área de vida. Nós determinamos se a co-ocorrência pode influenciar no tamanho da área de vida de dois roedores subterrâneos, C. flamarioni e C. minutus. Para isso foi avaliado o tamanho da área de vida em populações das duas espécies em locais onde se distribuem de forma alopátrica e simpátrica, ao longo da planície costeira do extremo sul do Brasil. O tamanho da área de vida de cada animal foi estimado utilizando os métodos de grid de células e mínimo polígono convexo, por meio da utilização de rádios colares fixados em cada indivíduo. Os resultados não apontaram nenhuma diferença significativa no tamanho da área de vida entre os sítios ou espécies, e as interações entre eles também não foi significativa. Além disso, não foi encontrado relação entre tamanho da área de vida com massa corporal ou sexo. Nossos resultados sugerem que a co-ocorrência pode não influenciar o tamanho da área de vida das espécies, isto pode se dá devido a adaptações ambientais que facilitam a coexistência (por exemplo, segregação de microhabitat e modificações na dieta). Além disso, as características do habitat de dunas arenosas podem atuar como filtro ambiental, favorecendo tamanhos semelhantes de área de vida em ambas as espécies.

Selection on MHC in a Context of Historical Demographic Change in 2 Closely Distributed Species of Tuco-tucos (Ctenomys australis and C. talarum).

Selection necessarily acts within the same current and historical demographic framework as neutral evolutionary processes, and the outcome of the interplay between these forces may vary according to their relative strength. In this study, we compare the variation at a major histocompatibility complex (MHC) locus (DRB exon 2), typically subject to strong diversifying selection, and mitochondrial diversity (D-loop) across populations encompassing the entire distribution of 2 species of South American subterranean rodents: Ctenomys australis and C. talarum (tuco-tucos). Although these species are parapatric along most of their distribution, historically they have followed distinct demographic trajectories associated with sea level changes during the Quaternary. We surveyed 8 populations of C. australis and 15 of C. talarum, from which we analyzed 70 and 212 D-loop haplotypes and 91 and 346 DRB genotypes, respectively. Both species have gone through a recent demographic expansion; however, the signal of this process only encompasses the entire distribution of one of the species: C. australis. While balancing selection on MHC in C. talarum-enhanced DRB diversity at the local level compared to D-loop, although not promoting divergence among populations, in C. australis local diversifying selection may have driven higher population differentiation at DRB than at D-loop. Our findings reinforce the idea that the relative strength of selection acting on MHC genes varies spatially and temporally within and among species, even between species using the same macrohabitat and exposed to similar immune challenges.

Understanding evolutionary variation in basal metabolic rate: An analysis in subterranean rodents

Understanding how evolutionary variation in energetic metabolism arises is central to several theories in animal biology. Basal metabolic rate (BMR) –i.e., the minimum rate of energy necessary to maintain thermal homeostasis in endotherms– is a highly informative measure to increase our understanding, because it is determined under highly standardized conditions. In this study we evaluate the relationship between taxa- and mass-independent (residual) BMR and ten environmental factors for 34 subterranean rodent species. Both conventional and phylogenetically informed analyses indicate that ambient temperature is the major determinant of residual BMR, with both variables inversely correlated. By contrast, other environmental factors that have been shown to affect residual BMR in endotherms, such as habitat productivity and rainfall, were not significant predictors of residual BMR in this group of species. Then, the results for subterranean rodents appear to support a central prediction of the obligatory heat model (OHM), which is a mechanistic model aimed to explain the evolution of residual BMR. Specifically, OHM proposes that during the colonization of colder environments, individuals with greater masses of metabolically expensive tissues (and thus with greater BMR) are favored by natural selection due to the link between greater masses of metabolically expensive tissues and physiological capacities. This way, natural selection should establishes a negative correlation between ambient temperature and both internal organ size and residual BMR.

Selective binocular vision loss in two subterranean caviomorph rodents: Spalacopus cyanus and Ctenomys talarum

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.

Audiograms of three subterranean rodent species (genus Fukomys) determined by auditory brainstem responses reveal extremely poor high-frequency hearing.

Life underground has shaped the auditory sense of subterranean mammals, shifting their hearing range to low frequencies. Mole-rats of the genus Fukomys have, however, been suggested to hear at frequencies up to 18.5 kHz, unusually high for a subterranean rodent. We present audiograms of three mole-rat species, Fukomys anselli, Fukomys micklemi and the giant mole-rat Fukomys mechowii, based on evoked auditory brainstem potentials. All species showed low sensitivity and restricted hearing ranges at 60 dB SPL extending from 125 Hz to 4 kHz (5 octaves) with most-sensitive hearing between 0.8 kHz and 1.4 kHz. The high-frequency cut-offs are the lowest found in mammals to date. In contrast to predictions from middle ear morphology, F. mechowii did not show higher sensitivity than F. anselli in the low-frequency range. These data suggest that the hearing range of Fukomys mole-rats is highly restricted to low frequencies and similar to that of other subterranean mammals.

Correction: Audiograms of three subterranean rodent species (genus Fukomys) determined by auditory brainstem responses reveal extremely poor high-frequency cut-offs.

ABSTRACT Life underground has shaped the auditory sense of subterranean mammals, shifting their hearing range to low frequencies. Mole-rats of the genus Fukomys have, however, been suggested to hear at frequencies up to 18.5 kHz, unusually high for a subterranean rodent. We present audiograms of three mole-rat species, Fukomys anselli, Fukomys micklemi and the giant mole-rat Fukomys mechowii, based on evoked auditory brainstem potentials. All species showed low sensitivity and restricted hearing ranges at 60 dB SPL extending from 125 Hz to 4 kHz (5 octaves) with most-sensitive hearing between 0.8 kHz and 1.4 kHz. The high-frequency cut-offs are the lowest found in mammals to date. In contrast to predictions from middle ear morphology, F. mechowii did not show higher sensitivity than F. anselli in the low-frequency range. These data suggest that the hearing range of Fukomys mole-rats is highly restricted to low frequencies and similar to that of other subterranean mammals.

Complete mitochondrial genome of Lasiopodomys mandarinus mandarinus (Arvicolinae, Rodentia)

Mandarin voles (Lasiopodomys mandarinus) is a subterranean rodent species that are often used as a model for studying subterranean hypoxic stress in mammals. Its subspecies L. m. mandarinus span in cropland in most area of north China and is regarded as an agricultural pest. In this paper, the complete mitochondrial genome of L. m. mandarinus has been determined. Our results showed that the mitochondrial genome of L. m. mandarinus is a circular molecule of 16 367 bp, which contents 13 protein-coding, 22 tRNAs and 2 rRNAs genes. The overall base composition of the heavy strand is 32.47% A, 27.04% T, 27.01% C, and 13.47% G. with an AT content of 59.51%.

Sharing the space: distribution, habitat segregation and delimitation of a new sympatric area of subterranean rodents.

Subterranean rodents of the genus Ctenomys usually present an allopatric or parapatric distribution. Currently, two cases of sympatry have been recognized for the genus in the coastal dunes of southern Argentina and southern Brazil. In this context, they are ideal models to test hypotheses about the factors that delimit the patterns of space use and to understand interspecific interactions in small mammals. We investigated the vegetation structure, plant biomass and soil hardness selected by two species of subterranean rodents (Ctenomys flamarioni and C. minutus) when distributed in sympatry and allopatry from nine different areas along the line of coastal dunes in southern Brazil. In addition, our work presents a new record of a third area of sympatry for the genus Ctenomys. Ctenomys flamarioni and C. minutus show habitat segregation in the area where they occur in sympatry. These species show segregation in their selection of microhabitats, differing in relation to soil hardness, plant biomass, and plant cover. Ctenomys flamarioni showed a distinction in habitat selection when occurring in allopatry and sympatry, whereas C. minutus selected the same habitat characteristics under both conditions. A possible explanation to the observed pattern is that these species have acquired different adaptations over time which allows them the ability to exploit different resources and thus avoid competitive interactions all together.

A re-assessment of Rensch's rule in tuco-tucos (Rodentia: Ctenomyidae: Ctenomys) using a phylogenetic approach

Sexual size dimorphism (SSD) is affected by a large number of factors, mating system being one of the most relevant. Almost 70 species of subterranean rodents of the genus Ctenomys are considered highly polygynic, and polygyny jointly with absence of paternal care of the young, favours high SSD. In this respect, Rensch's rule predicts that SSD scales with body size so that when males are larger than females SSD tends to increase with body size. We studied SSD and Rensch's rule in 28 taxa of Ctenomys using a phylogenetic approach employing the method of phylogenetic reduced major axis (pRMA) to perform reduced major axis (RMA) model II regression in the form of log10(male mass) on log10(female mass). The RMA regression slope (β) was statistically tested to accept or reject the null hypothesis that βpRMA=1.0. A slope significantly >1.0 would signal concordance with Rensch's rule. Our results showed that despite a high degree of male-biased SSD as expected from polygynic species, Rensch's rule is not verified in this rodent group. The causes of the non-concordance with Rensch's rule as well as its taxonomic level of application are discussed in terms of current models of SSD.

Rhythmic 24 h variation of core body temperature and locomotor activity in a subterranean rodent (Ctenomys aff. knighti), the tuco-tuco.

The tuco-tuco Ctenomys aff. knighti is a subterranean rodent which inhabits a semi-arid area in Northwestern Argentina. Although they live in underground burrows where environmental cycles are attenuated, they display robust, 24 h locomotor activity rhythms that are synchronized by light/dark cycles, both in laboratory and field conditions. The underground environment also poses energetic challenges (e.g. high-energy demands of digging, hypoxia, high humidity, low food availability) that have motivated thermoregulation studies in several subterranean rodent species. By using chronobiological protocols, the present work aims to contribute towards these studies by exploring day-night variations of thermoregulatory functions in tuco-tucos, starting with body temperature and its temporal relationship to locomotor activity. Animals showed daily, 24 h body temperature rhythms that persisted even in constant darkness and temperature, synchronizing to a daily light/dark cycle, with highest values occurring during darkness hours. The range of oscillation of body temperature was slightly lower than those reported for similar-sized and dark-active rodents. Most rhythmic parameters, such as period and phase, did not change upon removal of the running wheel. Body temperature and locomotor activity rhythms were robustly associated in time. The former persisted even after removal of the acute effects of intense activity on body temperature by a statistical method. Finally, regression gradients between body temperature and activity were higher in the beginning of the night, suggesting day-night variation in thermal conductance and heat production. Consideration of these day-night variations in thermoregulatory processes is beneficial for further studies on thermoregulation and energetics of subterranean rodents.

Evolutionary association between subterranean lifestyle and female sociality in rodents

Subterranean rodents are a good model system to examine adaptive evolution of social organization. Life underground has been proposed either to favor solitariness or, to the contrary, to promote sociality. In concordance with the first idea, most specialized diggers are solitary. However, group-living in several unrelated subterranean rodent species and especially eusociality in two genera of African mole-rats, the Bathyergidae, seem to support the second hypothesis. Thus, none of the two models is fully consistent with empirical data. Here we apply the comparative phylogenetic method to test an evolutionary correlation between fossoriality and female social strategy (solitary breeding vs breeding in group). Both characters show very strong phylogenetic signal, and we found a significant correlation between them. Subterranean lifestyle is readily acquired under female sociality. By contrast, the transition to life underground is extremely unlikely under female solitariness. Thus, not only social behavior may be affected by ecological specialization as it is widely assumed, but it can itself restrain the range of possible specializations. The rates of transition from sociality to solitariness are equal under subterranean and surface-dwelling lifestyle. Sociality loss is irreversible in subterranean lineages, unlike surface-dwelling lineages. Based on the revealed transition rates we suggest that all lineages of subterranean rodents have gone through the stage of cooperation at the beginning of their evolutionary track, whereas group-living is selected against in highly specialized diggers. An odd pattern of distribution of sociality across and within truly subterranean taxa probably derives from the influence of extrinsic factors in combination with phylogenetic inertia.

The social brain: transcriptome assembly and characterization of the hippocampus from a social subterranean rodent, the colonial tuco-tuco (Ctenomys sociabilis).

Elucidating the genetic mechanisms that underlie complex adaptive phenotypes is a central problem in evolutionary biology. For behavioral biologists, the ability to link variation in gene expression to the occurrence of specific behavioral traits has long been a largely unobtainable goal. Social interactions with conspecifics represent a fundamental component of the behavior of most animal species. Although several studies of mammals have attempted to uncover the genetic bases for social relationships using a candidate gene approach, none have attempted more comprehensive, transcriptome-based analyses using high throughout sequencing. As a first step toward improved understanding of the genetic underpinnings of mammalian sociality, we generated a reference transcriptome for the colonial tuco-tuco (Ctenomys sociabilis), a social species of subterranean rodent that is endemic to southwestern Argentina. Specifically, we analyzed over 500 million Illumina sequencing reads derived from the hippocampi of 10 colonial tuco-tucos housed in captivity under a variety of social conditions. The resulting reference transcriptome provides a critical tool for future studies aimed at exploring relationships between social environment and gene expression in this non-model species of social mammal.

Ctenomys brasiliensis Blainville (Rodentia: Ctenomyidae): clarifying the geographic placement of the type species of the genus Ctenomys

The genus Ctenomys (Rodentia: Ctenomyidae) comprises more than 60 species of subterranean rodents. Despite the widedistribution of the genus in southern America, the type locality of the type species—Ctenomys brasiliensisBlainville—was long thought to be the State of Minas Gerais in southeastern Brazil, well outside the presently knowndistributional area of the genus. Since it has never been collected again in that State, the type locality of this species is stilla matter for investigation. In order to elucidate this question, we investigated the skull of the type specimens of C.brasiliensis. From geometric morphometrics comparisons with other species of the genus, and taking into account thelabel information, it was possible to rediscover the type locality of this species. There is no doubt that the specimen wascollected in Minas, in the department of Lavalleja, Uruguay. Nowadays in this area on the southern coast of Uruguay, onlypopulations of Ctenomys pearsoni Lessa and Langguth were recognized. We suggest that more studies must be done tobetter understand the taxonomic relation between C. pearsoni complex and the C. brasiliensis, the type species for the genus that was collected in Uruguay and never occurred in southeastern Brazil.