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Bedford, N. L.

Publications and source records attributed to Bedford, N. L..

7 recordsLinked to original sources

Social hierarchy assays measure independent features of competitive ability

Social hierarchies are a nearly universal feature of animal groups, but whether dominance reflects a single generalized trait or a collection of context-specific competitive abilities remains unclear. Here, we assess social hierarchy in three strains of laboratory mice (BALB/c, C57BL/6, and Shank3B knockouts) of both sexes using three established paradigms: the tube test, the warm spot assay, and the void spot assay. Hierarchies emerged in all strains and both sexes across all three assays, but how animals established rank differed markedly by strain and sex. In the tube test, Shank3b-/- knockout females, but not males, lacked the winner effects seen in wild-type mice, indicating that the ability to build a winning streak depends on social recognition in a sex-specific manner. In the warm spot assay, females formed stronger hierarchies than males, particularly among mice on a C57BL/6 background, with high-ranking females actively displacing others from the warm platform. In the void spot assay, BALB/c mice of both sexes frequently displayed territory-marking behavior, a pattern that was less common in the other strains. Overall, individual rank rarely generalized across domains, despite high trial-to-trial repeatability for individuals within each assay. Together, these findings indicate that mice behave as dominance specialists rather than generalists, with strain- and sex-specific strategies for establishing rank in different competitive contexts, suggesting that distinct neural circuits likely underlie these separable components of competitive ability.

animal behavior and cognition↗

Diurnal Regulation of Urinary Behavior and Gene Expression in Aged Mice

Nocturia, defined as waking one or more times per night to urinate, is a prevalent and burdensome condition with few effective treatments. While the primary risk factor for nocturia is advanced age, few preclinical studies have addressed the pathophysiological mechanisms of nocturia in older subjects. Here, we develop a translational model of nocturia using aging mice and a behavioral paradigm that enables circadian assessment of voluntary urination in group-housed animals. We discovered dampened diurnal regulation of urinary behavior in aged mice compared to adult controls. Molecular analyses revealed disrupted diurnal expression of canonical circadian genes in aged mouse kidney and bladder tissues. Notably, we identified age-related loss of diurnal regulation of the bladder mechanosensory ion channel, Piezo1, suggesting a potential mechanism linking circadian disruption to altered bladder sensitivity. Our results reveal a role for circadian dysfunction in age-related nocturia and identify Piezo1 as a promising therapeutic target for chronobiological intervention.

physiology↗

Oxytocin neurons signal state-dependent transitions to thermogenesis and behavioral arousal in social and non-social settings.

Core body temperature (Tb) is defended within narrow limits through thermoregulatory behaviors like huddling, nesting, and physical activity as well as autonomic responses like brown fat thermogenesis. While Tb displays regulated fluctuations across different behavioral states and rest/arousal cycles, the neural control of these transitions is poorly understood. Here, we investigate the relationship between oxytocin neurons of the paraventricular hypothalamus (PVNOT) and behavioral and autonomic thermoeffector pathways across physiological states in mice. First, we show that PVNOT neurons are activated during social thermoregulation. We then demonstrate that in vivo PVNOT calcium dynamics align with transitions from rest to thermogenesis and behavioral arousal. Counter to our initial hypothesis, these dynamics were observed in both social and non-social contexts. Using a computer vision model to track thermoeffector pathways, we demonstrate that precisely timed stimulation of PVNOT neurons during low-Tb resting states increases thermogenesis followed by behavioral arousal. We therefore suggest a model in which PVNOT neurons facilitate homeostatic state-dependent transitions in thermo-behavioral states.

neuroscience↗

Evolution of gene expression across brain regions in behaviorally divergent deer mice

The evolution of innate behaviors is ultimately due to genetic variation likely acting in the nervous system. Gene regulation may be particularly important because it can evolve in a modular brain-region specific fashion through the concerted action of cis- and trans-regulatory changes. Here, to investigate transcriptional variation and its regulatory basis across the brain, we perform RNA sequencing (RNA-Seq) on ten brain subregions in two sister species of deer mice (Peromyscus maniculatus and P. polionotus) - which differ in a range of innate behaviors, including their social system - and their F1 hybrids. We find that most of the variation in gene expression distinguishes subregions, followed by species. Interspecific differential expression (DE) is pervasive (52-59% of expressed genes), whereas the number of DE genes between sexes is modest overall ([~]3%). Interestingly, the identity of DE genes varies considerably across brain regions. Much of this modularity is due to cis-regulatory divergence, and while 43% of genes were consistently assigned to the same gene regulatory class across subregions (e.g., conserved, cis-, or trans-regulatory divergence), a similar number were assigned to two or more different gene regulatory classes. Together, these results highlight the modularity of gene expression differences and divergence in the brain, which may be key to explain how the evolution of brain gene expression can contribute to the astonishing diversity of animal behaviors.

evolutionary biology↗

Automated tracking reveals the social network of beach mice and their burrows

Evolutionary biologists have long sought to understand the selective pressures driving phenotypic evolution. While most experimental data come from the study of morphological evolution, we know much less about the ultimate drivers of behavioral variation. Among the most striking examples of behavioral evolution are the long, complex burrows constructed by oldfield mice (Peromyscus polionotus ssp.). Yet how these mice use burrows in the wild, and whether burrow length may affect fitness, remains unknown. A major barrier to studying behavior in the wild has been the lack of technologies to continuously monitor - in this case, nocturnal and underground - behavior. Here, we designed and implemented a novel radio frequency identification (RFID) system to track patterns of burrow use in a natural population of beach mice. We combine RFID monitoring with burrow measurements, genetic data, and social network analysis to uncover how these monogamous mice use burrows under fully natural ecological and social conditions. We first found that long burrows provide a more stable thermal environment and have higher juvenile activity than short burrows, underscoring the likely importance of long burrows for rearing young. We also find that adult mice consistently use multiple burrows throughout their home range and tend to use the same burrows at the same time as their genetic relatives, suggesting that inclusive fitness benefits may accrue for individuals that construct and maintain multiple burrows. Our study highlights how new automated tracking approaches can provide novel insights into animal behavior in the wild.

animal behavior and cognition↗

Behavioural mechanisms underlying the evolution of cooperative burrowing in Peromyscus mice

While some behaviours are largely fixed and invariant, others can respond flexibly to different social contexts. Here, we leverage the unique burrowing behaviour of deer mice (genus Peromyscus) to investigate if and how individuals of three species adapt their behaviour when digging individually versus with partners. First, we find that pairs of mice from monogamous (P. polionotus) but not promiscuous (P. maniculatus, P. leucopus) species cooperatively construct burrows that are approximately twice as long as those dug by individuals and similar in size to burrows found in the wild. However, the length of burrows built by P. polionotus pairs differs: opposite-sex pairs construct longer burrows than same-sex pairs. By designing a novel behavioural assay in which we can observe and measure burrowing behaviour directly, we find that longer burrows are achieved not by changing individual behaviour, but instead because opposite-sex pairs are more socially cohesive and thus more likely to dig simultaneously, which is a more efficient mode of burrow elongation. Thus, across social contexts, individual burrowing behaviour appears largely invariant, even when the resultant burrow from pairs of mice differs from expectation based on individual behaviour, underscoring the fixed nature of burrowing behaviour in Peromyscus mice.

evolutionary biology↗

Evolution and genetics of precocious burrowing behavior in Peromyscus mice

A central challenge in biology is to understand how innate behaviors evolve between closely related species. One way to elucidate how differences arise is to compare the development of behavior in species with distinct adult traits. Here, we report that Peromyscus polionotus is strikingly precocious with regard to burrowing behavior, but not other behaviors, compared to its sister species P. maniculatus. In P. polionotus, burrows were excavated as early as 17 days of age, while P. maniculatus did not build burrows until 10 days later. Moreover, the well-known differences in burrow architecture between adults of these species--P. polionotus adults excavate long burrows with an escape tunnel, while P. maniculatus dig short, single-tunnel burrows--were intact in juvenile burrowers. To test whether this juvenile behavior is influenced by early-life environment, pups of both species were reciprocally cross-fostered. Fostering did not alter the characteristic burrowing behavior of either species, suggesting these differences are genetic. In backcross F2 hybrids, we show that precocious burrowing and adult tunnel length are genetically correlated, and that a single P. polionotus allele in a genomic region linked to adult tunnel length is predictive of precocious burrow construction. The co-inheritance of developmental and adult traits indicates the same genetic region--either a single gene with pleiotropic effects, or closely linked genes-- acts on distinct aspects of the same behavior across life stages. Such genetic variants likely affect behavioral drive (i.e. motivation) to burrow, and thereby affect both the development and adult expression of burrowing behavior.\n\nHighlightsO_LIJuvenile P. polionotus construct burrows precociously compared to its sister species P. maniculatus\nC_LIO_LICross-fostering does not alter species-specific burrowing behavior\nC_LIO_LIA QTL linked to adult tunnel length predicts developmental onset of burrow construction in hybrids\nC_LIO_LIPleiotropic genetic variant(s) may affect behavioral drive across life stages\nC_LI

animal behavior and cognition↗