Biology subjects

Miller, C. H.

Publications and source records attributed to Miller, C. H..

7 recordsLinked to original sources

bioRxiv2024

Seasonality of the estrus cycle in laboratory mice under constant conditions

Seasonality governs every aspect of life in the natural environment. Controlled laboratory settings are intended to keep animals under a constant set of environmental cues with no seasonality. However, prior research suggests that seasonal variation may exist despite aseasonal lab environments. Here, we examined if seasonal reproductive variation was present in a laboratory mouse strain (C57BL/6J) under standard laboratory housing conditions. We found that female C57BL/6J mice exhibited reproductive seasonality mirroring the outside environment, in a controlled "simulated summer" environment. In the winter and spring, females have longer ovulating phases (proestrus and estrus), compared to the fall. Females similarly experience lengthier complete cycles in the spring, with the most rapid cycling occurring in the fall. Additionally, females spent more time in ovulating phases across seasons than previously reported. Laboratory mice are sensitive to external seasonal changes, despite their local environment being light, temperature, and humidity controlled. This may be due to the detection of an unidentified external cue providing information about external seasonal changes. These findings represent just one example of how seasonality may impact mouse physiology in laboratory settings, emphasizing the need to account for such influences in biomedical research.

physiology↗

bioRxiv2022

Reproductive state switches the valence of male urinary pheromones in female mice

Internal states shape responses to sensory stimuli. Mammalian female reproductive states are understudied considering they are one of the most regular state changes in the animal kingdom. Here we examine female house mouse preferences toward male odors across the reproductive states of estrus and late-stage pregnancy. In house mice, urine scent marks are salient social odors that convey information about the sex and identity of individuals by major urinary proteins (MUPs). Males secrete a sex-specific pheromonal protein called darcin (MUP20). Additionally, genetically diverse mice secrete unique combinations of MUPs used in individual recognition. Prior work has revealed that male odors are powerful social stimuli for female mice, yet we have a limited understanding of how the valence of such odors change across reproductive states. We discovered a valence shift among estrus and pregnant females toward novel male urine, in which estrus females exhibit preference and pregnant females show strong avoidance. This valence switch also occurs toward darcin alone, providing further support for darcin as a strong sexual signal. However, when presented with familiar male urine, the approach-avoidance response disappears, even when additional darcin is added. In contrast, when an existing identity protein (MUP11) is added to familiar male urine the approach-avoidance response is recovered. This indicates that darcin in the absence of other identity information denotes a novel male and that familiar identity information present in male urine is sufficient to modify responses to darcin. Our findings suggest that the sex and identity information encoded by MUPs are likely processed via distinct, and potentially opposing pathways, that modulate responses toward complex social odor blends. Furthermore, we identify a state-modulated shift in decision-making toward social odors and propose a neural circuit model for this flow of information. These data underscore the importance of physiological state and signal context for interpreting the meaning and importance of social odors.

animal behavior and cognition↗

bioRxiv2022

Scent mark signal investment predicts fight dynamics in house mice

Signals mediate competitive interactions by allowing rival assessment, yet are often energetically expensive to produce. Individuals face tradeoffs when deciding when and where to signal, such that over or under-investing in signaling effort can be costly. One of the key mechanisms maintaining signal reliability is via social costs. While the social costs of over-signaling are well-known, the social costs of under-signaling are underexplored, particularly for dynamic signals. In this study we investigate a dynamic and olfactory-mediated signaling system that is ubiquitous among mammals: scent marking. Male house mice territorially scent mark their environment with metabolically costly urine marks. While competitive male mice are thought to deposit abundant scent marks in the environment, we recently identified a cohort of low-marking males that win fights. Whereas there are clear energetic costs to investing in urine signals in mice, we hypothesized that there may be social costs imposed on individuals who under-invest in signaling. Here we find that scent mark investment predicts fight dynamics. Despite fight outcome being unambiguous, aggressive intensity varies considerably across trials. Males that produce fewer scent marks engage in more intense fights that take longer to resolve. This effect appears to be driven by an unwillingness among losers to acquiesce to weakly signaling winners. We therefore find evidence for rival assessment of scent marks as well as social costs to under-signaling, which supports existing hypotheses for the importance of social punishment in maintaining optimal signaling equilibria. Our results further highlight the possibility of diverse signaling strategies in house mice.

ecology↗

bioRxiv2022

Spatial and social structure of rewilded laboratory mice

Social behavior and social organization have major influences on individual health and fitness. Yet, biomedical research focuses on studying a few genotypes under impoverished social conditions. Understanding how lab conditions have modified social organizations of model organisms, such as lab mice, relative to natural populations is a missing link between socioecology and biomedical science. Using a common garden design, we describe the formation of social structure in the well-studied laboratory mouse strain, C57BL/6J, in replicated mixed-sex populations over 10-day trials compared to control trials with wild-derived outbred house mice in outdoor field enclosures. We focus on three key features of mouse social systems: (i) territory establishment in males, (ii) female social relationships, and (iii) the social networks formed by the populations. Male territorial behaviors were similar but muted in C57 compared to wild-derived mice. Female C57 sharply differed from wild-derived females, showing little social bias toward cage mates and exploring substantially more of the enclosures compared to all other groups. Female behavior consistently generated denser social networks in C57 than in wild-derived mice. The repeatable societies formed under field conditions highlights opportunities to experimentally study the interplay between society and individual biology using model organisms.

animal behavior and cognition↗

bioRxiv2022

Dynamic changes to signal allocation rules in response to variable social environments in house mice

Male house mice use metabolically costly urine marks in intrasexual competition and mate attraction. Given the high costs of signaling and the depletable nature of urine reserves, males should dynamically modulate signal allocation as the social landscape is updated with new information. We investigate which aspects of male urine marking behavior are static or dynamic in light of changing social environments. To do this, we use thermal imaging to capture spatiotemporal data of urine deposition decisions. This novel method reveals fine-scale variation in urinary motor patterns in response to competition and social odors. Males demonstrate striking winner-loser effects in both the total allocation effort and temporal dynamics of scent marking. We find that competitive experience primes key temporal features of signal allocation and modulates responses to familiar and unfamiliar male scents. Males adjust their signaling effort, mark latency, and scent mark rhythm, depending on the scent identities present in the environment. Winners dramatically increase marking effort toward unfamiliar compared to familiar male scent, consistent with a dear enemy effect. Losers, in contrast, greatly reduce marking to unfamiliar scent but increase marking effort to the scent of their familiar rival, consistent with a nasty neighbor effect. Counter to the high lability of many features, the initial signal investment pattern influences allocation decisions days later, revealing the possibility of alternative scent mark strategies among competitive males. Thus, different features of urine mark signal allocation vary in responsiveness to fluctuating social landscapes, suggesting there are multiple distinct behavioral modules underlying marking behavior.

ecology↗

bioRxiv2019

Distinct evolutionary trajectories of V1R clades across mouse species

BackgroundMany animals rely heavily on olfaction to navigate their environment. Among rodents, olfaction is crucial for a wide range of social behaviors. The vomeronasal olfactory system in particular plays an important role in mediating social communication, including the detection of pheromones and recognition signals. Currently, very few vomeronasal receptors have known ligands, which severely limits our understanding of chemosensory-driven social communication. In this study we examine patterns of vomeronasal type-1 receptor (V1R) evolution in the house mouse and related species within the genus Mus. By exploring the evolution of these receptors, we provide insight into the functional roles of receptor subtypes as well as the dynamics of gene family evolution. ResultsWe generated transcriptomes from the vomeronasal organs of 5 Mus species, and produced high quality V1R repertoires for each species. We find that V1R clades in the house mouse and relatives exhibit distinct evolutionary trajectories. Some clades are highly conserved, while others reveal patterns of rapid evolutionary change. We identify putative species-specific gene expansions, including a dramatic clade D expansion in the house mouse. While gene gains are abundant, we detect very few gene losses. We describe a novel V1R clade and highlight candidate receptors for future de-orphanization. Based on clade-level evolutionary patterns, we identify receptor families that are strong candidates for detecting social signals and predator cues. Our results further support the view that V1Rs are important for detecting the physiological status of conspecifics, particularly female estrus cues. ConclusionAnalysis of clade-level evolution is critical for understanding species chemosensory adaptations. This study provides clear evidence that V1R clades are characterized by distinct evolutionary trajectories. As receptor evolution is shaped by ligand identity, these results provide a framework for examining the functional roles of different receptors.

evolutionary biology↗

bioRxiv2019

Patterns of urine scent mark pheromone evolution in house mice and relatives (Muridae: Mus)

Scent marks are important mediators of territorial behavior and sexual selection in many species, especially among mammals. As such, the evolution of compounds used in scent marks has the potential to inform our understanding of signal evolution in relation to social and sexual selection. A major challenge in studies of chemical communication is that the link between semiochemical compounds and genetic changes is often unclear. The major urinary proteins (MUPs) of house mice are elaborated pheromone blends that provide information on sex, status and individual identity. Importantly, MUPs are a direct protein product of genes, providing a clear link between genotype and phenotype. Here we examine the evolution of urinary pheromone signals among house mice and relatives by examining the sequences and patterns of expression of MUPs in the liver, where urine excreted MUPs are produced. MUP patterns have evolved among mouse species both by gene duplication and variation in expression. Notably, the sex-specificity of pheromone expression that has previously been assumed to be male-specific varies considerably across species. Our data reveal that individual identity signals in MUPs evolved prior to 0.35 million years ago and have rapidly diversified through recombining a modest number of perceptually salient amino acid variants. Amino acid variants are much more common on the exterior of the protein where they could interact with vomeronasal receptors, suggesting that perception have played a major role in shaping MUP diversity. Collectively, these data provide new insights into the diverse processes and pressures shaping pheromone signals, and suggest new avenues for using house mice and their wild relatives to probe the evolution of signals and signal processing.

evolutionary biology↗