Publications

*First/co-first authorship

†Undergraduate co-author

Preprints

2. Zipple, M. N., Kuo, D. C.†, Meng, X.†, Reichard, T. M.†, Guess, K.†, Vogt, C. C., Moeller, A., & Sheehan, M. J. (2024). Sex-specific competitive social feedback amplifies the role of early life contingency in male mice (p. 2024.04.19.590322). bioRxiv. https://doi.org/10.1101/2024.04.19.590322

Contingency (or 'luck') in early life plays an important role in shaping individuals' development. When individuals live within larger societies, social experiences may cause the importance of early contingencies to be magnified or dampened. Here we test the hypothesis that competition magnifies the importance of early contingency in a sex-specific manner by comparing the developmental trajectories of genetically identical, free-living mice who either experienced high levels of territorial competition (males) or did not (females). We show that male territoriality results in a competitive feedback loop that magnifies the importance of early contingency and pushes individuals onto divergent, self-reinforcing life trajectories, while the same process appears absent in females. Our results indicate that the strength of sexual selection may be self-limiting, as within-sex competition increases the importance of early life contingency, thereby reducing the ability of selection to lead to evolution. They also demonstrate the potential for contingency to lead to dramatic differences in life outcomes, even in the absence of any underlying differences in ability ('merit').

1. Miller, C. H., Reichard, T. M.†, Yang, J., Carlson-Clarke, B.†, Vogt, C. C., Warden, M. R., & Sheehan, M. J. (2022). Reproductive state switches the valence of male urinary pheromones in female mice (p. 2022.08.22.504866). bioRxiv. https://doi.org/10.1101/2022.08.22.504866

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.

Published

7. Zipple, M.N.*, Vogt, C.C.* and Sheehan, M.J. (2024). Genetically identical mice express alternative reproductive tactics depending on social conditions in the field. Proceedings of the Royal Society B: Biological Sciences, 291(2019), p. 20240099. Available at: https://doi.org/10.1098/rspb.2024.0099.


GitHub Repository

Animals that experience unpredictable social environmental conditions are predicted to evolve alternative reproductive tactics (or “conditional strategies”). In many species, establishing and maintaining a territory is critical to survival and reproduction, and an animal’s ability to do so is strongly influenced by the presence and density of competitors. Here we manipulate social conditions to study the alternative reproductive tactics displayed by genetically identical, age-matched laboratory mice competing for territories under ecologically realistic social environmental conditions. We introduced adult males and females of the laboratory mouse strain (C57BL/6J) into a large, outdoor field enclosure containing defendable resource zones under one of two social conditions. We first created a low-density social environment, such that the number of available territories exceeded the number of males. After males established stable territories, we introduced a pulse of intruder males and observed the resulting defensive and invasive tactics employed. In response to this change in social environment, males with large territories invested more in patrolling but were less effective at excluding intruder males as compared to resident males with small territories. Intruding males failed to establish territories and displayed an alternative tactic featuring greater exploration as compared to genetically identical territorial males. Alternative tactics did not lead to equal reproductive success—males that acquired territories experienced greater survival and had greater access to females. Thus, we identify three alternative reproductive tactics among genetically identical mice and demonstrate the ability to establish causal links between social experiences and individual behavior in ecologically relevant contexts.

6. Vogt, C. C., Zipple, M. N., Sprockett, D. D., Miller, C. H., Hardy, S. X.†, Arthur, M. K.†, Greenstein, A. M.†, Colvin, M. S., Michel, L. M., Moeller, A. H., & Sheehan, M. J. (2024). Female behavior drives the formation of distinct social structures in C57BL/6J versus wild-derived outbred mice in field enclosures. BMC Biology, 22(1), 35. https://doi.org/10.1186/s12915-024-01809-0


Press: Cornell Chronicle, Cosmos Magazine; GitHub Repository; Zenodo Data Repository; Preprint Version

Background: 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.


Results: 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.


Conclusions: C57 and wild-derived mice individually vary in their social and spatial behaviors which scale to shape overall social organization. The repeatable societies formed under field conditions highlights opportunities to experimentally study the interplay between society and individual biology using model organisms.

5. Legan, A.W.*, Vogt, C.C.* and Sheehan, M.J. (2023) ‘Postural analysis reveals persistent changes in paper wasp foundress behavioral state after conspecific challenge’, Ecology and Evolution, 13(9), p. e10436. Available at: https://doi.org/10.1002/ece3.10436.

Vigilant animals detect and respond to threats in the environment, often changing posture and movement patterns. Vigilance is modulated not only by predators but also by conspecific threats. In social animals, precisely how conspecific threats alter vigilance behavior over time is relevant to long-standing hypotheses about social plasticity. We report persistent effects of a simulated conspecific challenge on behavior of wild northern paper wasp foundresses, Polistes fuscatus. During the founding phase of the colony cycle, conspecific wasps can usurp nests from the resident foundress, representing a severe threat. We used automated tracking to monitor the movement and posture of P. fuscatus foundresses in response to simulated intrusions. Wasps displayed increased movement, greater bilateral wing extension, and reduced antennal separation after the threat was removed. These changes were not observed after presentation with a wooden dowel. By rapidly adjusting individual behavior after fending off an intruder, paper wasp foundresses might invest in surveillance of potential threats, even when such threats are no longer immediately present. The prolonged vigilance-like behavioral state observed here is relevant to plasticity of social recognition processes in paper wasps. 

4. Zipple, M.N., Vogt, C.C., and Sheehan, M.J. (2023). Re-wilding model organisms: Opportunities to test causal mechanisms in social determinants of health and aging. Neuroscience & Biobehavioral Reviews 152, 105238. 10.1016/j.neubiorev.2023.105238.

Social experiences are strongly associated with individuals’ health, aging, and survival in many mammalian taxa, including humans. Despite their role as models of many other physiological and developmental bases of health and aging, biomedical model organisms (particularly lab mice) remain an underutilized tool in resolving outstanding questions regarding social determinants of health and aging, including causality, context-dependence, reversibility, and effective interventions, due to the constraints of standard laboratory conditions on animals’ social lives. Even when kept in social housing, lab animals rarely experience social and physical environments that approach the richness, variability, and complexity they have evolved to navigate and benefit from. Here we argue that studying biomedical model organisms outside under complex, semi-natural social environments (“re-wilding”) allows researchers to capture the methodological benefits of both field studies of wild animals and laboratory studies of model organisms. We review recent efforts to re-wild mice and highlight discoveries that have only been made possible by researchers studying mice under complex, manipulable social environments. 

3. Dahake, A., Jain, P., Vogt, C.C., Kandalaft, W., Stroock, A.D., and Raguso, R.A. (2022). A signal-like role for floral humidity in a nocturnal pollination system. Nature Communications. 10.1038/s41467-022-35353-8.

Previous studies have considered floral humidity to be an inadvertent consequence of nectar evaporation, which could be exploited as a cue by nectar-seeking pollinators. By contrast, our interdisciplinary study of a night-blooming flower, Datura wrightii, and its hawkmoth pollinator, Manduca sexta, reveals that floral relative humidity acts as a mutually beneficial signal in this system. The distinction between cue- and signal-based functions is illustrated by three experimental findings. First, floral humidity gradients in Datura are nearly ten-fold greater than those reported for other species, and result from active (stomatal conductance) rather than passive (nectar evaporation) processes. These humidity gradients are sustained in the face of wind and are reconstituted within seconds of moth visitation, implying substantial physiological costs to these desert plants. Second, the water balance costs in Datura are compensated through increased visitation by Manduca moths, with concomitant increases in pollen export. We show that moths are innately attracted to humid flowers, even when floral humidity and nectar rewards are experimentally decoupled. Moreover, moths can track minute changes in humidity via antennal hygrosensory sensilla but fail to do so when these sensilla are experimentally occluded. Third, their preference for humid flowers benefits hawkmoths by reducing the energetic costs of flower handling during nectar foraging. Taken together, these findings suggest that floral humidity may function as a signal mediating the final stages of floral choice by hawkmoths, complementing the attractive functions of visual and olfactory signals beyond the floral threshold in this nocturnal plant-pollinator system.

2. Jernigan, C. M., Stafstrom, J. A., Zaba, N. C.†, Vogt, C. C., & Sheehan, M. J. (2022). Color is necessary for face discrimination in the Northern paper wasp, Polistes fuscatus. Animal Cognition. https://doi.org/10.1007/s10071-022-01691-9

Visual individual recognition requires animals to distinguish among conspecifics based on appearance. Though visual individual recognition has been reported in a range of taxa, the features that animals rely on to discriminate between individuals are often not well understood. Northern paper wasp females, Polistes fuscatus, possess individually distinctive color patterns on their faces, which mediate individual recognition. It is currently unclear what facial features P. fuscatus use to distinguish individuals. The anterior optic tubercle, a chromatic processing brain region, is especially sensitive to social experience during development, suggesting that color may be important for recognition in this species. We sought to test the roles of color in wasp facial recognition. Color may be important simply because it creates a pattern. If this is the case, then wasps should perform similarly when discriminating color or grayscale images of the same faces. Alternatively, color itself may be important for recognition, which would predict poorer performance on grayscale image discrimination relative to color images. We found wasps trained on grayscale faces, unlike those trained on color images, did not perform better than chance. Suggesting that color is necessary for the recognition of an image as a face by the wasp visual system.

1. Sheehan, M. J., Miller, C. H., Vogt, C. C., & Ligon, R. A. (2018). Behavioral Evolution: Can You Dig It? Current Biology, 28(1), R19–R21. https://doi.org/10.1016/j.cub.2017.11.016

Behaviors are among the most complex phenotypes, making the genetic dissection of behavioral differences extremely challenging. A careful dissection of ontogenetic differences in burrowing behavior between mouse species highlights the importance of integrative approaches to the study of behavioral evolution.