Genetic structure in a solitary rodent (Ctenomys talarum): implications for kinship and dispersal

The genetic structure of a population provides critical insights into patterns of kinship and dispersal. Although genetic evidence of kin structure has been obtained for multiple species of social vertebrates, this aspect of population biology has received considerably less attention among solitary taxa in which spatial and social relationships are unlikely to be influenced by kin selection. Nevertheless, significant kin structure may occur in solitary species, particularly if ecological or life history traits limit individual vagility. To explore relationships between genetic structure, kinship, and dispersal in a solitary vertebrate, we compared patterns of genetic variation in two demographically distinct populations of the talar tuco-tuco (Ctenomys talarum), a solitary species of subterranean rodent from Buenos Aires Province, Argentina. Based on previous field studies of C. talarum at Mar de Cobo (MC) and Necochea (NC), we predicted that natal dispersal in these populations is male biased, with dispersal distances for males and females being greater at NC. Analyses of 12 microsatellite loci revealed that in both populations, kin structure was more apparent among females than among males. Between populations, kinship and genetic substructure were more pronounced at MC. Thus, our findings were consistent with predicted patterns of dispersal for these animals. Collectively, these results indicate that populations of this solitary species are characterized by significant kin structure, suggesting that, even in the absence of sociality and kin selection, the spatial distributions and movements of individuals may significantly impact patterns of genetic diversity among conspecifics.     

Energy and distribution in subterranean rodents: sympatry between two species of the genus Ctenomys

The low basal metabolic rate (BMR) observed in subterranean rodents, compared to that of surface-dwelling species of comparable size, has been proposed to be an adaptation to underground life. Two main hypotheses have been proposed to explain this finding, the cost of burrowing and the thermal stress. The former states that the low BMR is due to the high cost of extending the tunnel system whereas the other relates it to the possibility of overheating in burrows where evaporative and convective heat exchange are restricted. Additionally, both hypotheses related the energetics of subterranean rodent with spatial distribution. The genus Ctenomys is an excellent model to evaluate the cost of burrowing or thermal stress, since they are widely distributed, with members differing markedly in body mass. The aim of this study was to assess digging and basal energetics in two Ctenomys species that live in sympatry in a coastal grassland, but differ in their microspatial distribution by soil preference. We used the obtained energetic data to test both energy-distribution hypotheses. We measured BMR and digging metabolic rate (DMR) through open flow respirometry in two species exposed to soft and hard soils. In brief, DMR in Ctenomys talarum (100-170 g), as in Ctenomys australis (250-600 g), was unaffected by soil hardness. Within thermoneutral zone of each species, DMR/RMR quotient was lower in the smaller species. Our data did not support the thermal stress hypothesis, but the cost of burrowing hypothesis was not rejected. Other alternative hypotheses are proposed to explain the distribution of C. talarum and C. australis.     

DNA fingerprinting reveals polygyny in the subterranean rodent Ctenomys talarum

DNA fingerprinting was used to characterize patterns of paternity in two populations of Ctenomys talarum from Buenos Aires Province, Argentina. The multilocus probe PV47-2 was used to detect variation in genomic DNA extracted from 12 females, their 32 offspring, and 14 putative sires. For 11 out of 12 litters examined, a single male capable of providing all nonmaternal bands was identified. Within each study population, individual males sired more than one litter, suggesting that C. talarum is polygynous. No evidence of multiple paternity of litters was found. High band-sharing values among females suggest that further research is needed to assess the population genetic structure of this species.     

Metabolic rate and thermoregulation in two species of tuco-tuco, Ctenomys talarum and Ctenomys australis (Caviomorpha, Octodontidae)

1. Resting metabolic rate and body temperature in function of ambient temperature were determined for two species of Ctenomys. 2. Oxygen consumption was lowest between 25 and 30 degrees C and was 0.946 +/- 0.030 and 0.968 +/- 0.022 in Ctenomys talarum (from Mar de Cobo and Necochea, respectively). Resting metabolic rate was 0.343 +/- 0.053 at 30 C in C. australis. 3. Mean rectal temperature at thermoneutrality was 36.1 +/- 0.13 and 37.3 +/- 0.17 in C. talarum and C. australis, respectively. 4. Limited thermoregulation occurred in C. talarum down to 20 degrees C but C. australis maintained body temperature down to 10 degrees C. 5. Both species of tuco-tucos became hyperthermic at ambient temperatures above thermoneutrality.     

Genetic variation over 10,000 years in Ctenomys: comparative phylochronology provides a temporal perspective on rarity, environmental change and demography

An understanding of how ecological traits influence past species response to environmental change can aid our future predictions of species persistence. We used ancient DNA and serial coalescent modelling in a hypothesis-testing framework to reveal differences in temporal genetic variation over 10,000 years for two species of subterranean rodents that currently differ in rarity (abundance, range size and habitat specificity) and mating system, but that reside in the same volcanically active region. Comparative phylochronologic analyses indicated little genetic change and suggest genetic stability in the solitary widespread Ctenomys haigi over thousands of years. In contrast, we found a pattern of haplotypic turnover in the rare and currently endangered Ctenomys sociabilis. Serial coalescent modelling indicated that the best-fit models of microevolutionary change included gene flow between isolated populations for this species. Although C. haigi and C. sociabilis are congeners that share many life history traits, they have behavioural, habitat-preference and population-size differences that may have resulted in contrasting patterns of temporal variation during periods of environmental change.     

The role of chromosomal rearrangements and geographical barriers in the divergence of lineages in a South American subterranean rodent (Rodentia: Ctenomyidae: Ctenomys minutus)

Identifying factors and the extent of their roles in the differentiation of populations is of great importance for understanding the evolutionary process in which a species is involved. Ctenomys minutus is a highly karyotype–polymorphic subterranean rodent, with diploid numbers ranging from 42 to 50 and autosomal arm numbers (ANs) ranging from 68 to 80, comprising a total of 45 karyotypes described so far. This species inhabits the southern Brazilian coastal plain, which has a complex geological history, with several potential geographical barriers acting on different time scales. We assessed the geographical genetic structure of C. minutus, examining 340 individuals over the entire distributional range and using information from chromosomal rearrangements, mitochondrial DNA (mtDNA) sequences and 14 microsatellite loci. The mtDNA results revealed seven main haplogroups, with the most recent common ancestors dating from the Pleistocene, whereas clustering methods defined 12 populations. Some boundaries of mtDNA haplogroups and population clusters can be associated with potential geographical barriers to gene flow. The isolation-by-distance pattern also has an important role in fine-scale genetic differentiation, which is strengthened by the narrowness of the coastal plain and by common features of subterranean rodents (that is, small fragmented populations and low dispersal rates), which limit gene flow among populations. A step-by-step mechanism of chromosomal evolution can be suggested for this species, mainly associated with the metapopulation structure, genetic drift and the geographical features of the southern Brazilian coastal plain. However, chromosomal variations have no or very little role in the diversification of C. minutus populations.     

Seasonal changes in body composition of Ctenomys talarum (Rodentia: Octodontidae): an herbivore subterranean rodent

Ctenomys talarum is a subterranean herbivorous rodent whose burrow systems exhibit particular characteristics, distinct from other subterranean environments. We studied seasonal variation in body composition of C. talarum in relation to energetic requirements. Body lipid content seasonally changed in C. talarum, related to reproductive cycle and thermorregulatory mechanisms. A decrease in protein body content was found only in spring. Ash content of females was lowest when most of them are in post partum estro. Observed variations in water body content could be associated with plant water content and/or metabolic regulation. Our results show the occurrence of seasonal variations in body composition in C. talarum, which could be related to the high cost of reproduction and the subterranean life style of this species.     

Automatic data recording of circadian rhythms

This paper illustrates a method for automatic data recording using the printer port of personal computer and software designed ad hoc. The system was tested by measuring circadian rhythms of activity in the subterranean rodent Ctenomys talarum. Data is recorded in a text-only comma-delimited file, and displayed on screen.     

Effects of contrasting demographic histories on selection at major histocompatibility complex loci in two sympatric species of tuco‐tucos (Rodentia: Ctenomyidae)

To explore the impact of history on selection and genetic structure at functional loci, we compared patterns of major histocompatibility complex (MHC) variability in two sympatric species of ctenomyid rodents with different demographic backgrounds. Although Ctenomys talarum has experienced a stable demographic history, Ctenomys australis has undergone a recent demographic expansion. Accordingly, we predicted that MHC allele frequency distributions should be more skewed, differences between coding and noncoding regions should be less pronounced, and evidence of current selection on MHC loci should be reduced in C. australis relative to C. talarum. To test these predictions, we compared variation at the MHC class II DRB and DQA genes with that at multiple neutral markers, including DQA intron 2, the mitochondrial control region, and 8–12 microsatellite loci. These analyses supported the first two of our predictions but indicated that estimates of selection (based on ω‐values) were greater for C. australis. Further exploration of these data, however, revealed differences in the time frames over which selection appears to have acted on each species, with evidence of contemporary selection on MHC loci being limited to C. talarum. Collectively, these findings indicate that demographic history can substantially influence genetic structure at functional loci and that the effects of history on selection may be temporally complex and dynamic. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 260–277.     

Nutritional responses to different diet quality in the subterranean rodent Ctenomys talarum (tuco-tucos)

Nutritional response to different diet quality was examined in the subterranean rodent Ctenomys talarum (tuco-tuco). Animals maintained in captive conditions were fed with three plant species that differed in their fibre content. Tuco-tucos showed the ability to perform adjusts in short time lapse in response to diet quality; food ingestion, egestion and feces ingestion changed in animals under different plant species diets. Time budget, mainly time devoted to feeding and activity accompanied such changes. Coprophagy was practiced along the day and night following the arrhythmic activity pattern found for this species. Feces reingestion was not associated to resting. Furthermore, it was observed during fresh food ingestion, being pellets chewed. Soft and hard feces differed in morphological and nutritional characteristics.     

Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates

The purpose of this study was to analyse and describe vocalizations of a solitary subterranean rodent, Ctenomys talarum. In adult C. talarum five different sounds (four true vocalizations and one mechanical sound) were recorded during different behavioural contexts. Using data from the laboratory and literature, we classified these vocalizations as territorial, distress, and mating calls. We found that the vocalization range in C. talarum is shifted towards low frequencies, which transmit better in underground burrows and match well the hearing range described for other species of subterranean rodents. These low-frequency vocalizations, also found in other non-related subterranean rodents, may reflect an adaptation to the acoustic conditions of the habitat. Electronic Publication     

Relationship between helminth parasites and demographic attributes of a population of the subterranean rodent Ctenomys talarum (Rodentla: Octodontidae)

The helminth parasite fauna of a natural population of the octodontid, Ctenomys talarum, was studied. Parasites that were found included the nematodes Heligmostrongylus sp. and Trichuris sp. Total prevalence of parasitism was 92.3%, mean intensity of infection was 22.7 worms, and mean abundance was 21 worms. Prevalence and mean abundance of infection with Heligmostrongylus sp. were higher in C. talarum males relative to females. Ecological and physiological causes, as well as the mating system of the host species, influence the likelihood of sex differences in parasite infection. The low parasite burden and diversity of C. talarum are associated with restrictions imposed by the subterranean habitat and with life-history traits of these rodents. Whether these findings apply to other Ctenomys spp. is unknown.     

Decreased glucose tolerance but normal blood glucose levels in the field in the caviomorph rodent Ctenomys talarum: the role of stress and physical activity

Hystricomorph rodents have a divergent insulin molecule with only 1-10% of the biological activity in comparison to other mammalian species. In this study, we used the subterranean rodent Ctenomys talarum as a model and performed blood glucose tolerance tests (GTTs) with trained and untrained individuals to evaluate blood glucose regulation and the possible role of physical activity as a compensatory mechanism. Additionally, we evaluated the variations in blood glucose during acute and chronic stress and gathered data in the field to evaluate natural-occurring variations in blood glucose levels. The GTTs showed that C. talarum have a diminished capacity of regulating blood glucose levels in comparison to other mammals and suggest that unexplored differences in the compensatory mechanisms, insulin structure and/or glucose transporters exist within species of hystricomorph rodents. However, blood glucose levels in the field stayed within the normal mammalian range. Physical activity did not prove to be a compensatory mechanism for blood glucose regulation. The individuals did not display important increases in blood glucose after acute stressors and managed to adequately regulate blood glucose during chronic stress. We suggest that the species may not face a selective pressure favoring a more tightly, mammalian like, capacity of regulating blood glucose levels.     

Maximal thermogenic capacity and non-shivering thermogenesis in the South American subterranean rodent Ctenomys talarum

Subterranean rodents inhabit closed tunnel systems that are hypoxic and hypercapnic and buffer aboveground ambient temperature. In contrast to other strictly subterranean rodents, Ctenomys talarum exhibits activity on the surface during foraging and dispersion and hence, is exposed also to the aboveground environment. In this context, this species is a valuable model to explore how the interplay between underground and aboveground use affects the relationship among basal metabolic rate (BMR), cold-induced maximum metabolic rate (MMR), shivering (ST), and non-shivering thermogenesis (NST). In this work, we provide the first evidence of the presence of NST, including the expression of uncoupling proteins in brown adipose tissue (BAT), and shivering thermogenesis in Ctenomys talarum, a species belonging to the most numerous subterranean genus, endemic to South America. Our results show no differences in BMR, cold-induced MMR, and NST between cold- (15?°C) and warm- (25?°C) acclimated individuals. Furthermore, thermal acclimation had no effect on the expression of mitochondrial uncoupling protein 1 (UCP1) in BAT. Only cytochrome c oxidase (COX) content and activity increased during cold acclimation. When interscapular BAT was removed, NST decreased more than 30?%, whereas cold-induced MMR remained unchanged. All together, these data suggest that cold-induced MMR reaches a maximum in warm-acclimated individuals and so a probable ceiling in NST and UCP1 expression in BAT. Possible thermogenic mechanisms explaining the increase in the oxidative capacity, mediated by COX in BAT of cold-acclimated individuals and the role of ST in subterranean life habits are proposed.     

Digestive flexibility in females of the subterranean rodent ctenomys talarum in their natural habitat

We studied the occurrence of digestive strategies at different levels in females of the subterranean herbivorous rodent Ctenomys talarum living in their natural habitat. We determined the dimensions of different parts of the gastrointestinal tract and organs along as the activity of key digestive enzymes(sucrase, maltase and N-aminopeptidase) in small intestine in females seasonally caught. Females of C. talarum did not show seasonal variations in the mass of the different parts of the gastrointestinal tract. In nonreproductive females large intestine was longer in autumn, whereas reproductive females did not show seasonal variations in the length of the different parts of the gut. Females of C. talarum exhibited a high sucrose, maltase and N-aminopeptidase activity in small intestine, although these activities were higher in small intestine of females caught in autumn (nonreproductive) than in females caught in winter (reproductive). The results show that C. talarum females exhibit characteristics in the gut at the morphological and biochemical level, which could represent digestive strategies to face the constraints imposed by their costly particular way of life.     

Functional morphology and paleobiology of the pliocene rodent Actenomys (Caviomorpha: Octodontidae): the evolution to a subterranean mode of life

The Pliocene caviomorph rodent Actenomys has long been recognized as an early fossorial representative of the subfamily Ctenomyinae (Octodontidae), which includes one living genus, Ctenomys (tuco-tucos), and several species widely distributed in South America. To assess the de gree of specialization for digging in Actenomys , we performed morphological comparisons with other octodontid genera (Octodon, Spalacopus , and Ctenomys) of known mode of life and behaviour. As a whole, our results indicate that, in terms of morphological specializations for digging, Actenomys occupies an intermediate position between Octodon , a generalized semi-fossorial rodent which forages above ground, and Ctenomys-Spalacopus , two highly specialized subterranean forms. The position of the deltoid process (humerus) and the length of the olecranon process (ulna)–two traits which affect the out-forces exerted by several forelimb muscles–were in Actenomys intermediate between non-subterranean and subterranean taxa. The skull, particularly the rostrum, appears to be strong, and sagittal and nuchal crests are well marked. The zygomatic arches arc as flared as those of the generalized Octodon. Notably, the upper and lower incisors of Actenomys were extremely procumbent, as in many highly-specialized chisel-tooth digging species. Based upon the stratigraphic and sedimentological analysis of the palaeosoils containing its fossil remains, we suggest that Actenomys lived in an environment of moderate to hig primary productivity. The texture of the palaeosoils indicate that theywere hard and highly cohesive. This situation, which contrasts with that observed in living Ctenomyinae, has relevant implications for burrowing cost. The integration of morphological and palaeoenvironmental data allowed testing of hypotheses about the palaeobiological attributes of this ancestral ctenomyine.     

Interactions between environmental factors can hide isolation by distance patterns: a case study of Ctenomys rionegrensis in Uruguay

Identifying the factors responsible for the structuring of genetic diversity is of fundamental importance for biodiversity conservation. However, arriving at such understanding is difficult owing to the many factors involved and the potential interactions between them. Here, we present an example of how such interactions can preclude us from arriving at a complete characterization of the demographic history and genetic structure of a species. Ctenomys rionegrensis is a species with restricted dispersal abilities and, as such, should exhibit an isolation by distance (IBD) pattern, which previous studies were unable to uncover. It was therefore concluded that this species underwent a recent population expansion. Using a novel hierarchical Bayesian method, we show that the inability to detect the IBD pattern is due to the interaction between elevation and geographical distance. We posit that populations in low areas suffer periodic floods that may reduce local population sizes, increasing genetic drift, a process that masks the effect of distance on genetic differentiation. Our results do not refute the possibility that the populations of C. rionegrensis underwent a recent population expansion but they indicate that an alternative scenario described by a metapopulation model at or near migration-drift equilibrium cannot be excluded either.     

Breeding biology of the fossorial rodent Ctenomys talarum (Rodentia: Octodontidae)

The paper describes the breeding biology of the South American herbivorous fossorial rodent Ctenomys talarum (tuco-tuco), covering the following aspects: length of breeding season, prenatal mortality, mean litter size and its correlates, sex ratio and its density-dependence, and late sexual maturity of both sexes. These parameters are compared and contrasted with those of other conspecifics and other subterranean rodents.     

Historical demography and spatial genetic structure of the subterranean rodent Ctenomys magellanicus in Tierra del Fuego (Argentina)

Ctenomys (tuco‐tuco) is the most numerous genus of South American subterranean rodents and one of the most genetically diverse clades of mammals known. In particular, the genus constitutes a very interesting model for evolutionary studies of genetic divergence and conservation. Ctenomys magellanicus is the southernmost species of the group and the only one living in Isla Grande de Tierra del Fuego (Argentina). This species presents two chromosomal forms (Cm34 and Cm36) fragmented into demes distributed from the north region (steppe) to the south region (ecotone) of the island, respectively; no hybrids or overlapping areas were detected. To study the historical demography and the spatial genetic structure of the C. magellanicus population we used mitochondrial DNA (mtDNA) (D‐loop and cytochrome b) and microsatellite loci. Nine mtDNA haplotypes were identified, three of them belonging to the north and the other six to the south. Shared haplotypes between regions were not detected. mtDNA and microsatellite genotypes showed a marked pattern of population structure with low values of genetic flow between regions. The south is made up of small populations or isolated demes making up an endogamic metapopulation with unique alleles and haplotypes. Also, the results suggest a northward expansion process starting from an ancestral haplotype from the south. That population might have lived at a refuge through the adverse Pleistocene environmental conditions that took place at Tierra del Fuego. Results of this study are relevant to the conservation of C. magellanicus, suggesting that each region (north and south) might be considered as an Evolutionarily Significant Unit. © 2013 The Linnean Society of London