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.

No abstract

Urine marking is central to mouse social behavior. Males use depletable and costly urine marks in intrasexual competition and mate attraction. We investigate how males alter signaling decisions across variable social landscapes using thermal imaging to capture spatiotemporal marking data. Thermal recording reveals fine-scale adjustments in urinary motor patterns in response to competition and social odors. Males demonstrate striking winner-loser effects in scent mark allocation effort and timing. Competitive experience primes temporal features of marking and modulates responses to scent familiarity. Males adjust signaling effort, mark latency, and marking rhythm, depending on the scent identities in the environment. Notably, recent contest outcome affects how males respond to familiar and unfamiliar urine. Winners increase marking effort toward unfamiliar relative to familiar male scents, whereas losers reduce marking effort to unfamiliar but increase to familiar rival scents. All males adjust their scent mark timing after a contest regardless of fight outcome, and deposit marks in more rapid bursts during marking bouts. In contrast to this dynamism, initial signal investment predicts aspects of scent marking days later, revealing the possibility of alternative marking strategies among competitive males. These data show that mice flexibly update their signaling decisions in response to changing social landscapes.

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.

Signals mediate competitive interactions by allowing rival assessment, yet are often energetically expensive to produce. One of the key mechanisms maintaining signal reliability is social costs. While the social costs of over-signalling are well known, the social costs of under-signalling are underexplored, particularly for dynamic signals. In this study, we investigate a dynamic and olfactory-mediated signalling system that is ubiquitous among mammals: scent marking. Male house mice territorially scent mark their environment with metabolically costly urine marks. Competitive male mice are thought to deposit abundant scent marks in the environment. However, we recently identified a cohort of low-marking males that win fights. We hypothesized that there may be social costs imposed on individuals who under-invest in signalling. Here we find that scent mark investment predicts fight dynamics. Winning males that produce fewer scent marks prior to a fight 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 signalling winners. We, therefore, find evidence for rival assessment of scent marks as well as social costs to under-signalling. This supports existing hypotheses for the importance of social punishment in maintaining optimal signalling equilibria. Our results further highlight the possibility of diverse signalling strategies in house mice.