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

Abstract

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.

Scent mark signal investment predicts fight dynamics in house mice

“…Males were categorized as either low or high-marking individuals, based on whether their total number of urine deposition events fell below or above the median number of marks ( Figures 3A & S1A ). This categorization is supported by our prior work, which shows that initial mark investment predicts marking levels days later ( Figure S1 ; 48). In other words, males that are low or high-marking adhere to their respective marking groups days after an aggressive contest (48).…”

“…Previous work described males reducing their scent marking after losing (41). Indeed, in the trials reported here, we found that high-marking males dramatically reduce their marking efforts after losing (48). However, this scenario does not readily explain the observed patterns among winning males that continue to mark infrequently.…”

“…In our previous work examining signal allocation decisions, we were surprised to find that scent marking behavior did not clearly predict wins or losses during fights, and instead identified a cohort of low-signaling competitive males (48). Together, these results led us to investigate the aggressive contests within this dataset in greater detail to better understand the relationship between signaling and competitive ability (48).…”

“…This categorization is supported by our prior work, which shows that initial mark investment predicts marking levels days later (Figure S1; 48). In other words, males that are low or high-marking adhere to their respective marking groups days after an aggressive contest (48).…”

“…It is, therefore, generally assumed that urine marking is an honest indicator of a male’s status and competitive ability (38–41,45–47). Yet, we have recently tested this assumption and found it to be incomplete—urine marking prior to a contest did not predict wins or losses among size-matched rivals, in part due to the presence of low-marking competitive males (48).…”