Eileen A. Lacey

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. J. Comp. Neurol. 507:1847–1859, 2008.

An evolutionary framework for studying mechanisms of social behavior

Social interactions are central to most animals and have a fundamental impact upon the phenotype of an individual. Social behavior (social interactions among conspecifics) represents a central challenge to the integration of the functional and mechanistic bases of complex behavior. Traditionally, studies of proximate and ultimate elements of social behavior have been conducted by distinct groups of researchers, with little communication across perceived disciplinary boundaries. However, recent technological advances, coupled with increased recognition of the substantial variation in mechanisms underlying social interactions, should compel investigators from divergent disciplines to pursue more integrative analyses of social behavior. We propose an integrative conceptual framework intended to guide researchers towards a comprehensive understanding of the evolution and maintenance of mechanisms governing variation in sociality.

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 ( X ≥ 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.

Bateman's Principle in Cooperatively Breeding Vertebrates: The Effects of Non-breeding Alloparents on Variability in Female and Male Reproductive Success

Abstract The sex-specific slopes of Batemans gradients have important implications for understanding animal mating systems, including patterns of sexual selection and reproductive competition. Intersexual differences in the fitness benefits derived from mating with multiple partners are expected to yield distinct patterns of reproductive success for males and females, with variance in direct fitness predicted to be greater among males. These analyses assume that typically all adults are reproductive and that failure to produce offspring is non-adaptive. Among some species of cooperatively breeding birds and mammals, however, non-breeding adult alloparents are common and may comprise the majority of individuals in social groups. The presence of a large number of non-breeding adults, particularly when coupled with greater social suppression of reproduction among females, may alter the relative variance in direct fitness between the sexes, thereby generating an apparent contradiction to Batemans Paradigm. To explore quantitatively the effects of non-breeding alloparents on variance in reproductive success, we used genetic estimates of parentage and reproductive success drawn from the literature to calculate the relative variability in direct fitness for females and males in alloparental and “other” societies of birds and mammals. Our analyses indicate that in mammals and, to a lesser extent, in birds, variability in direct fitness is greater among females in species characterized by the presence of non-breeding alloparents. These data suggest that social interactions, including social suppression of reproduction, are powerful determinants of individual direct fitness that may modify sex-specific patterns of reproductive variance from those described by Bateman.

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.

ECOLOGY OF SOCIALITY IN RODENTS: A CTENOMYID PERSPECTIVE

Abstract 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.

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.

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.

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.

Toward an integrative understanding of social behavior: New models and new opportunities

Social interactions among conspecifics are a fundamental and adaptively significant component of the biology of numerous species. Such interactions give rise to group living as well as many of the complex forms of cooperation and conflict that occur within animal groups. Although previous conceptual models have focused on the ecological causes and fitness consequences of variation in social interactions, recent developments in endocrinology, neuroscience, and molecular genetics offer exciting opportunities to develop more integrated research programs that will facilitate new insights into the physiological causes and consequences of social variation. Here, we propose an integrative framework of social behavior that emphasizes relationships between ultimate-level function and proximate-level mechanism, thereby providing a foundation for exploring the full diversity of factors that underlie variation in social interactions, and ultimately sociality. In addition to identifying new model systems for the study of human psychopathologies, this framework provides a mechanistic basis for predicting how social behavior will change in response to environmental variation. We argue that the study of non-model organisms is essential for implementing this integrative model of social behavior because such species can be studied simultaneously in the lab and field, thereby allowing integration of rigorously controlled experimental manipulations with detailed observations of the ecological contexts in which interactions among conspecifics occur.