Colonial Tuco-tuco Research Articles

Stable isotopes reveal differential patterns of Holocene environmental change among tuco-tucos (Rodentia: Ctenomyidae, Ctenomys) from Patagonia

To explore the role of past environmental changes in shaping interspecific differences in genetic structure among tuco-tucos (Rodentia: Ctenomyidae, Ctenomys) from the Limay Valley of northern Patagonia, we compared δ13C and δ18O values for modern and historical tooth enamel from the colonial tuco-tuco (C. sociabilis) and the parapatric Patagonian tuco-tuco (C. haigi). Specifically, we sought to test the hypothesis that a mid-Holocene loss of genetic variation in C. sociabilis was associated with environmental change. For both species, the δ13C composition of tooth enamel differed significantly (~ 5.1‰ difference in mean δ13C values) between modern and Holocene (0.5–12 kyr B.P.) samples, suggesting marked temporal changes in the vegetation consumed. For C. sociabilis, no statistically significant differences in the δ13C composition of teeth were found among individuals from the early, middle, and late Holocene. In contrast, significant differences in δ13C values were found between middle and late Holocene samples from C. haigi. None of our analyses revealed statistically significant differences in δ18O values. Thus, although the diets of both study species have changed from the Holocene to the present, only C. haigi experienced significant dietary changes during the Holocene. We suggest that the ecologically more specialized C. sociabilis continued to consume the same food resources even as changing Holocene conditions caused preferred habitats to disappear. In contrast, the more generalized C. haigi altered its diet, allowing populations of this species to remain widespread despite changing Holocene environments.

Identifying drivers of historical genetic decline in an endemic Patagonian rodent, the colonial tuco-tuco, Ctenomys sociabilis (Rodentia: Ctenomyidae)

Identifying drivers of historical genetic decline in an endemic Patagonian rodent, the colonial tuco-tuco, Ctenomys sociabilis (Rodentia: Ctenomyidae)

Genomic data reveal a loss of diversity in two species of tuco-tucos (genus Ctenomys) following a volcanic eruption

Marked reductions in population size can trigger corresponding declines in genetic variation. Understanding the precise genetic consequences of such reductions, however, is often challenging due to the absence of robust pre- and post-reduction datasets. Here, we use heterochronous genomic data from samples obtained before and immediately after the 2011 eruption of the Puyehue-Cordón Caulle volcanic complex in Patagonia to explore the genetic impacts of this event on two parapatric species of rodents, the colonial tuco-tuco (Ctenomys sociabilis) and the Patagonian tuco-tuco (C. haigi). Previous analyses using microsatellites revealed no post-eruption changes in genetic variation in C. haigi, but an unexpected increase in variation in C. sociabilis. To explore this outcome further, we used targeted gene capture to sequence over 2,000 putatively neutral regions for both species. Our data revealed that, contrary to the microsatellite analyses, the eruption was associated with a small but significant decrease in genetic variation in both species. We suggest that genome-level analyses provide greater power than traditional molecular markers to detect the genetic consequences of population size changes, particularly changes that are recent, short-term, or modest in size. Consequently, genomic analyses promise to generate important new insights into the effects of specific environmental events on demography and genetic variation.

Rapid increase in genetic diversity in an endemic Patagonian tuco-tuco following a recent volcanic eruption

Catastrophic natural events can have profound impacts on patterns of genetic diversity. Due to the typically unpredictable nature of such phenomena, however, few studies have been able to directly compare patterns of diversity before and after natural catastrophic events. Here, we examine the impacts of a recent volcanic eruption in southern Chile on genetic variation in the colonial tuco-tuco (Ctenomys sociabilis), a subterranean species of rodent endemic to the area most affected by the June 2011 eruption of the Puyehue-Cordon Caulle volcanic complex. To provide a comparative context for interpreting changes in genetic variation in this species, we also analyze the effects of this eruption on genetic variation in the geographically proximate but more widely distributed Patagonian tuco-tuco (C. haigi). Our analyses indicate that while both C. sociabilis and C. haigi displayed significant post-eruption decreases in population density, the apparent impacts of the eruption on genetic diversity differed between species. In particular, genetic diversity at multiple microsatellite loci increased in C. sociabilis after the eruption while no comparable post-eruption increase in C. haigi was observed at these loci. No changes in post-eruption diversity at the mitochondrial cytochrome b locus were detected for either species. To place these findings in a larger spatiotemporal context, we compared our results for C. sociabilis to genetic data from additional modern and ancient populations of this species. These comparisons, combined with Bayesian serial coalescent modeling, suggest that post-eruption gene flow from nearby populations represents the most probable explanation for the apparent increase in post-eruption microsatellite diversity in C. sociabilis. Thus, detailed comparisons of pre- and post-eruption populations provide important insights into not only the genetic consequences of a natural catastrophic event, but also the demographic processes by which these changes in genetic diversity likely occurred.

Post-extinction discovery of a population of the highly endemic colonial tuco-tuco (Ctenomys sociabilis)

Comparisons of a species’ modern and historic geographic distributions can yield important insights into patterns of biodiversity, including faunal responses to environmental change. Using morphological and genetic analyses of museum specimens and samples recently collected in the field, we document the historical occurrence of a population of colonial tuco-tucos ( Ctenomys sociabilis ) from Laguna Nahuelquir in Chubut Province, Argentina. This locality represents a significant increase in the geographic distribution of this species, which had been thought to be endemic to the Sierra de Cuyin Manzano located ~130 km to the north in Neuquen Province. Field surveys of the Laguna Nahuelquir locality failed to reveal extant populations of C. sociabilis ; although the habitat at this location is generally consistent with areas occupied by C. sociabilis in the Cuyin Manzano, the Laguna Nahuelquir site is now occupied by the Patagonian tuco-tuco, C. haigi . This apparent replacement of ctenomyid species is consistent with patterns of faunal turnover revealed by analyses of late Pleistocene–early Holocene cave deposits near the Sierra de Cuyin Manzano and supports the hypothesis that changes in local environmental conditions have contributed to the loss of C. sociabilis from these localities. Thus, comparisons of historical and modern specimens of ctenomyids provide evidence of range retractions by colonial tuco-tucos over multiple time scales and add to a growing body of evidence regarding the apparent effects of environmental change on the small mammal fauna of northern Patagonia. Comparar la distribucion geografica actual y pasada de una especie puede revelar importantes conocimientos sobre los patrones de la biodiversidad, incluyendo su respuesta a los cambios ambientales. Mediante analisis morfologicos y geneticos de especimenes de museo y muestras recientemente recolectadas en el campo, documentamos la ocurrencia historica de una poblacion de tuco-tuco colonial ( Ctenomys sociabilis ) en Laguna Nahuelquir, provincia del Chubut, Argentina. La confirmacion de la poblacion de C. sociabilis en la provincia del Chubut representa una expansion significativa del rango geografico de esta especie, que se creia endemica de la Sierra de Cuyin Manzano en la provincia del Neuquen, ~130 km al norte de la Laguna Nahuelquir. Los estudios de campo en la localidad de Laguna Nahuelquir no revelaron la presencia de poblaciones existentes de C. sociabilis ; aunque el habitat en este lugar es generalmente consistente con las areas ocupadas por C. sociabilis en el Cuyin Manzano, el sitio Laguna Nahuelquir esta ahora ocupado por el tuco-tuco patagonico, C. haigi . Este cambio en las especies de Ctenomys es consistente con los patrones de cambio de fauna revelados por el analisis de depositos de finales del Pleistoceno y Holoceno temprano en la Sierra de Cuyin Manzano y apoya la hipotesis de que los cambios en las condiciones ambientales locales han contribuido a la perdida de C. sociabilis en estas localidades. Por lo tanto, la comparacion de las muestras actuales e historicas de Ctenomys proporciona evidencias de retraccion del rango geografico del tuco-tuco colonial a traves de diferentes escalas temporales y se suman a un creciente cuerpo de evidencia sobre los efectos aparentes de los cambios ambientales en la fauna pequenos mamiferos del norte de la Patagonia.

Effects of social environment on baseline glucocorticoid levels in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis)

The social environment in which an animal lives can profoundly impact its physiology, including glucocorticoid (GC) responses to external stressors. In social, group-living species, individuals may face stressors arising from regular interactions with conspecifics as well as those associated with basic life history needs such as acquiring food or shelter. To explore the relative contributions of these two types of stressors on glucocorticoid physiology in a communally breeding mammal, we characterized baseline GC levels in female colonial tuco-tucos (Ctenomys sociabilis), which are subterranean rodents endemic to southwestern Argentina. Long-term field studies have revealed that while about half of all yearling female C. sociabilis live and breed alone, the remainder live and breed within their natal group. We assessed the effects of this intraspecific variation in social environment on GC physiology by comparing concentrations of baseline fecal corticosterone metabolite (fCM) for (1) lone and group-living yearling females in a free-living population of C. sociabilis and (2) captive yearling female C. sociabilis that had been experimentally assigned to live alone or with conspecifics. In both cases, lone females displayed significantly higher mean baseline fCM concentrations. Data from free-living animals indicated that this outcome arose from differences in circadian patterns of GC production. fCM concentrations for group-living animals declined in the afternoon while fCM in lone individuals did not. These findings suggest that for C. sociabilis, stressors associated with basic life history functions present greater challenges than those arising from interactions with conspecifics. Our study is one of the first to examine GC levels in a plural-breeding mammal in which the effects of group-living are not confounded by differences in reproductive or dominance status, thereby generating important insights into the endocrine consequences of group-living.

Habitat use by colonial tuco-tucos (Ctenomys sociabilis): specialization, variation, and sociality

Understanding habitat requirements has implications for numerous aspects of a species' biology, including where individuals live and how they behave. Specialization for mesic, resource-rich habitats known as mallines is thought to have favored group living in the colonial tuco-tuco (Ctenomys sociabilis), a subterranean rodent that is endemic to NeuquProvince in southwestern Argentina. To explore the proposed relationship between mallines and sociality in this species in greater detail, we characterized the habitats occupied by C. sociabilis at 3 locations representing the extremes of this species' geographic range. Specifically, plant composition and vegetative structure were characterized for 57 occupied burrow systems distributed across the 3 sampling localities. Our data indicate that C. sociabilis is not restricted to mallines. Although significant variation in vegetation was detected among the 3 study sites, the majority of active burrow systems surveyed at each site occurred in nonmallhabitats. In addition to providing the first species-wide survey of habitat use by C. sociabilis, our data yield new insights into the role of habitat specialization in promoting sociality in this behaviorally unusual species of ctenomyid rodent.

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.

Contrasting fecal corticosterone metabolite levels in captive and free‐living colonial tuco‐tucos (Ctenomys sociabilis)

The environment in which an animal lives can profoundly influence its biology, including physiological responses to external stressors. To examine the effects of environmental conditions on physiological stress reactions in colonial tuco-tucos (Ctenomys sociabilis), we measured glucocorticoid (GC) levels in captive and free-living members of this species of social, subterranean rodent. Analyses of plasma and fecal samples revealed immunoreactive corticosterone (metabolites) to be the most prevalent GC in this species. An adrenocorticotropic hormone challenge confirmed that fecal corticosterone metabolites are responsive to exogenous stressors and provided validation of the commercial enzyme immunoassay kit used to detect these metabolites. Comparisons of adult female C. sociabilis from natural and captive environments revealed significantly higher baseline concentrations of corticosterone metabolites and significantly greater individual variation in metabolite concentrations among free-living animals. These findings suggest that the natural environment in which these animals occur is more challenging and more variable than the captive housing conditions employed. In addition to providing the first evaluation of GC levels in captive and wild colonial tuco-tucos, our findings indicate that the influence of environmental conditions on stress physiology may have important implications for understanding the social behavior of this species in the laboratory and the field.

Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco‐tuco (Ctenomys haigi and Ctenomys sociabilis)

The neuropeptides oxytocin and vasopressin and their receptors have been implicated in elements of mammalian social behavior such as attachment to mates and offspring, but their potential role in mediating other types of social relationships remains largely unknown. We performed receptor autoradiography to assess whether forebrain oxytocin receptor (OTR) or vasopressin V1a receptor (V1aR) distributions differed with social structure in two closely related and ecologically similar species of South American rodents, the colonial tuco-tuco (Ctenomys sociabilis) and the Patagonian tuco-tuco (Ctenomys haigi). Long-term field studies have revealed that C. haigi is solitary, whereas C. sociabilis is social and provides a model of female-based group living. Our analyses revealed marked differences in OTR and V1aR distributions between these species. For example, only C. sociabilis had OTR binding in the piriform cortex and thalamus and V1aR binding in the olfactory bulbs. In contrast, C. haigi exhibited dramatically higher levels of OTR binding throughout the lateral septum and hippocampus. More generally, the group-living C. sociabilis exhibited a pattern of nucleus accumbens OTR and ventral pallidum V1aR binding different from that associated with the formation of opposite-sex pair bonds in microtine rodents. Higher binding in the central nucleus of the amygdala of C. sociabilis was consistent with the hypothesis that formation of social groups in C. sociabilis may be facilitated by reduced social anxiety. Low OTR binding in the lateral septum might also be a permissive factor for group living in C. sociabilis. Future studies will expand on these analyses to explore interspecific differences in ctenomyid receptor binding patterns in a phylogenetic context.

Effects of group size on nest attendance in the communally breeding colonial tuco-tuco

Communal nesting is generally assumed to be adaptive, meaning that it confers a fitness advantage on the individuals that share a nest site. This advantage may accrue directly to adults, or it may affect adult fitness through gains in offspring survival. In particular, survival of juveniles reared in communal groups may be greater because adults are present in the nest more often to provide care to young. To test the hypothesis that communal nesting is associated with increased adult presence in the nest, we used radiotelemetry to examine patterns of adult nest attendance as a function of group size for free-living colonial tuco-tucos ( Ctenomys sociabilis). Burrow systems of this social, subterranean rodent are inhabited by 1–6 adult females and, in some cases, a single adult male. Data obtained from residents of 26 burrow systems monitored during 1996–2000 indicated that the percentage of time that the nest was unattended (no adult present) did not vary predictably with date or time of day during the period between the birth and weaning of young. The percentage of time that the nest was unattended, however, decreased significantly as the number of adults per burrow system increased. This difference was most evident when the percentage of time that the nest was unattended was compared for lone females versus multi-adult groups. We suggest that increased nest attendance has important implications for the survival of juveniles reared in multi-adult burrow systems but that this effect may be confounded by the fitness consequences of other costs and benefits associated with communal nesting in this species.

Ancient DNA reveals Holocene loss of genetic diversity in a South American rodent.

Understanding how animal populations have evolved in response to palaeoenvironmental conditions is essential for predicting the impact of future environmental change on current biodiversity. Analyses of ancient DNA provide a unique opportunity to track population responses to prehistoric environments. We explored the effects of palaeoenvironmental change on the colonial tuco-tuco (Ctenomys sociabilis), a highly endemic species of Patagonian rodent that is currently listed as threatened by the IUCN. By combining surveys of modern genetic variation from throughout this species' current geographic range with analyses of DNA samples from fossil material dating back to 10,000 ybp, we demonstrate a striking decline in genetic diversity that is concordant with environmental events in the study region. Our results highlight the importance of non-anthropogenic factors in loss of diversity, including reductions in smaller mammals such as rodents.

Kinship in colonial tuco-tucos: evidence from group composition and population structure

Kinship plays a significant role in shaping the social and genetic structures of many vertebrate populations. Evidence of kinship, however, may be substantially influenced by the spatial and temporal scales over which co-ancestry is monitored. For example, while data on social group composition may yield little indication of relatedness among reproductive partners, data on the demographic structure of a population may reveal considerable shared ancestry among mates. We explored relationships among social group composition, individual movements, and population-level patterns of kinship using data from a 7-year field study of the colonial tuco-tuco (Ctenomys sociabilis), a group-living subterranean rodent that is endemic to southwestern Argentina. Our analyses indicate that social groups are composed of 1–4 generations of closely related females and a single, immigrant male, suggesting that reproductive partners are not related to one another. Monitoring individual movements, however, revealed that (1) most male dispersal occurs within the local population and (2) most new social groups are founded by females born in the study population, indicating that individuals reared in different burrow systems may share considerable co-ancestry. Simulation analyses revealed that up to 67% of reproductive partnerships consist of animals that share co-ancestry within the last 5–7 generations. Thus, while analyses of social group composition provide little evidence of kinship among reproductive partners, population-level analyses of dispersal and group formation suggest that co-ancestry among mates is common. These findings have important implications for interpreting social interactions and genetic structure in this species.

Sociality reduces individual direct fitness in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis)

In many social vertebrates, remaining in the natal group leads to at least short-term reductions in the direct fitness of philopatric animals. Among communally breeding rodents, the direct fitness costs of philopatry appear to increase as the frequency of successful natal dispersal decreases, suggesting a functional link between constraints on natal dispersal and the reproductive consequences of sociality. To explore this relationship empirically, I documented patterns of direct fitness among female colonial tuco-tucos (Ctenomys sociabilis), which are group-living subterranean rodents from southwestern Argentina. Demographic data suggest that successful natal dispersal is rare in this species, leading to the prediction that natal philopatry in C. sociabilis is associated with significant reductions in individual direct fitness. Using data obtained during 1996–2001, I compared the direct fitness of females that dispersed from their natal group and bred alone as yearlings to that of females that lived and bred in their natal group as yearlings. Philopatric yearlings reared significantly fewer young to weaning than did disperser (lone) yearlings. Although neither survival to a second breeding season nor the estimated lifetime number of pups reared to weaning differed between dispersal strategies, the annual direct fitness of group-living females was 23–40% less than expected, suggesting that philopatric animals experienced a substantial direct fitness cost by remaining in their natal group. These data yield important insights into the adaptive bases for group living in C. sociabilis and suggest that constraints on natal dispersal are an important factor favoring group living in this species.

ECOLOGY OF SOCIALITY IN RODENTS: A CTENOMYID PERSPECTIVE

Group living is an important component of the social biology of numerous rodent species. For the past 2 decades, efforts to understand the ecological factors associated with group living in rodents have focused on subterranean taxa, in particular African mole-rats of the family Bathyergidae. Comparative analyses of the habitats occupied by solitary and social bathyergids suggest that group living occurs when the combined effects of sporadic rainfall, hard soils, and patchily distributed food resources render energetic costs of burrow excavation prohibitive for lone individuals. To determine whether these variables were associated with group living in other subterranean taxa, we characterized ecological differences between a solitary and a social member of a phylogenetically independent lineage of subterranean rodents, the Ctenomyidae. Specifically, we quantified soil conditions and spatial distributions of food resources for 1 population each of the solitary Patagonian tuco-tuco (Ctenomys haigi) and the group-living colonial tuco-tuco (C. sociabilis), both of which occur in the Limay Valley of southwestern Argentina. Our analyses revealed that while members of both species occurred in relatively mesic mallin habitats, only C. haigi also occurred in arid steppe habitat. No differences in spatial distributions of food resources were found between study sites. Significant differences in soil conditions, however, were detected; soils from steppe habitat were significantly harder to penetrate than soils from mallin areas, suggesting that costs of burrow excavation may be higher for the solitary C. haigi. Thus, data from ctenomyids in the Limay Valley are not consistent with explanations for group living developed for bathyergid mole-rats. Although ecological comparisons of ctenomyids over larger spatial scales are required, our data suggest that interactions between ecology and group living in subterranean rodents may be more diverse than previously realized.

Olfactory discrimination of gender by colonial tuco-tucos (Ctenomys sociabilis)

Olfactory discrimination of gender by colonial tuco-tucos (Ctenomys sociabilis)

Microsatellite variation in solitary and social tuco-tucos: molecular properties and population dynamics.

Variation at 15 microsatellite loci was characterized for a population of the solitary Patagonian tuco-tuco (Ctenomys haigi) and a population of group-living colonial tuco-tuco (C. sociabilis), both of which were located in the Limay River Valley of south western Argentina. All loci examined were characterized by uninterrupted di- or trinucleotide repeats in both species; seven of these loci had been isolated from C. haigi and eight had been isolated from C. sociabilis. Across all loci, there was a significant tendency for both number of alleles and heterozygosity to be greater in C. haigi than in C. sociabilis. Cloning and sequencing of multiple PCR products per locus per population revealed no significant biases in allele length, suggesting that this difference in variability was not due to ascertainment bias or to population-wide differences in rates of microsatellite evolution. Instead, differences in microsatellite variation between C. haigi and C. sociabilis were more consistent with current demographic and suspected historical differences between these populations. In particular, interpopulation differences in the distribution of microsatellite allele sizes and allele frequencies suggested that C. sociabilis has been more subject to historical reductions in population size (e.g. population bottlenecks) than has C. haigi. These findings indicate that analyses of microsatellite structure can yield important insights into the population-level phenomena that contribute to diversity at these markers, including differences in population history that continue to influence levels of genetic variability.

Solitary Burrow Use by Adult Patagonian tuco-tucos (Ctenomys haigi)

Although >100 Patagonian tuco-tucos (Ctenomys haigi) were live-trapped in the Limay River Valley, Rio Negro Province, Argentina, during January 1994, December 1994, and January 1996, no more than one adult was captured per burrow system. Radiotelemetry studies of nine adults revealed that areas occupied by different individuals did not overlap. This pattern of burrow use differed markedly from that reported for the colonial tuco-tuco (C. sociabilis), which also occurs in the Limay Valley. We suggest that comparative studies of C. haigi and C. sociabilis will yield important new insights into factors associated with interspecific differences in the social systems of subterranean rodents.

Burrow Sharing by Colonial Tuco-Tucos (Ctenomys sociabilis)

Preliminary studies indicate that the recently described colonial tuco-tuco (Ctenomys sociabilis) is social. As part of efforts to characterize the behavioral ecology of this species, we examined patterns of use of burrows by members of a free-living population of C. sociabilis located in southern Neuquen Province, Argentina. As many as five adults (one male, four females) were captured within a single colony (spatially distinct cluster of burrow entrances). Spatial relationships among eight adults from three colonies were monitored using radiotelemetry. Each animal was active in only a single colony. Within each colony, the areas used by different adults overlapped extensively (X̄ ≥ 68%) and all animals shared a single nest site. Collectively, these data indicate that a colony of C. sociabilis consists of a single burrow system that may be inhabited by multiple adults. We suggest that comparative analyses of C. sociabilis and other colonial taxa (e.g., colonial African mole-rats; Bathyergidae) will significantly improve our understanding of the factors favoring sociality among subterranean rodents.