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Abstract Phenotypic plasticity is a strategy by which animals alter behaviour, morphology and/or physiology in response to cues of current conditions to cope with environmental heterogeneity.If environmental change is impending and cues reliably predict future conditions, animals can also respond in anticipation of these changes (i.e. anticipatory plasticity) if they possess the mechanistic architecture necessary to do so. This phenomenon has been documented across the tree of life, but how animals integrate cues of future conditions and mount anticipatory responses remains largely ambiguous.Here, we synthesize theoretical principles from sensory biology and animal communication with recent advances in physiological ecology to identify candidate physiological mechanisms underpinning anticipatory plasticity in animal systems.We discuss how socio‐ecological rhythms, cue perception and interactions between the epigenome, neuroendocrine system and gut microbiota can contribute to the maintenance and evolution of anticipatory plasticity, including anticipatory reproduction.We shed light on the proximate and ultimate mechanisms that facilitate the evolution and maintenance of anticipatory plasticity in the face of environmental heterogeneity, contributing to a broader understanding of how animals may respond to rapid global change as environmental cues become unreliable and conditions unpredictable. Read the freePlain Language Summaryfor this article on the Journal blog. 

Despite considerable research on reproductive timing, factors influencing intraspecific variation in gestation length in wild mammals have received limited attention, largely due to a lack of high-resolution data. We examined potential drivers of gestation length variation in a wild population of North American red squirrels ( Tamiasciurus hudsonicus Erxleben, 1777) in Yukon, Canada. Drawing on 27 years of conception and parturition data, we found that gestation length was highly conserved, with minimal variation (35.4 ± 1.49 days; mean ± standard deviation). Gestation length was unaffected by maternal age, litter size, or litter sex ratio. Likewise, the anticipation of an upcoming food pulse, caused by synchronous conifer seed masting, had no statistically significant influence on gestation length. This finding stands in contrast to other reproductive traits in red squirrels, which are known to shift in response to food pulses. Overall, our results suggest that gestation length in red squirrels is buffered against environmental variability, likely due to stabilizing selection or strong heritability. 

Early-life adversity, even when transient, can have lasting effects on individual phenotypes and reduce lifespan across species. If these effects can be mitigated by a high-quality later-life environment, then differences in future resources may explain variable resilience to early-life adversity. Using data from over 1000 wild North American red squirrels, we tested the hypothesis that the costs of early-life adversity for adult lifespan could be offset by later-life food abundance. We identified six adversities that reduced juvenile survival in the first year of life, though only one—birth date—had continued independent effects on adult lifespan. We then built a weighted early-life adversity (wELA) index integrating the sum of adversities and their effect sizes. Greater weighted early-life adversity predicted shorter adult lifespans in males and females, but a naturally occurring food boom in the second year of life ameliorated this effect. Experimental food supplementation did not replicate this pattern, despite increasing lifespan, indicating that the buffering effect of a future food boom may hinge on more than an increase in available calories. Our results suggest a non-deterministic role of early-life conditions for later-life phenotype, highlighting the importance of evaluating the consequences of early-life adversity in the context of an animal's entire life course. 

Abstract Female advertisement of reproductive state and receptivity has the potential to play a large role in the mating systems of many taxa, but investigations of this phenomenon are underrepresented in the literature. North American red squirrels (Tamiasciurus hudsonicus) are highly territorial and engage in scramble competition mating, with males converging from spatially disparate territories to engage in mating chases. Given the narrow estrus window exhibited in this species, the ubiquitous use of vocalizations to advertise territory ownership, and the high synchronicity of males arriving from distant territories, we hypothesized that female vocalizations contain cues relating to their estrous state. To test this hypothesis, we examined the spectral and temporal properties of female territorial rattle vocalizations collected from females of known reproductive condition over 3 years. While we found no distinct changes associated with estrus specifically, we did identify significant changes in the spectral characteristics of rattles relating to both female body mass and reproductive state relative to parturition. To the best of our knowledge, this is the first evidence of changes in vocal characteristics associated with late pregnancy in a nonhuman mammal. 

ABSTRACT Microbial transmission is hypothesised to be a major benefit of sociality, facilitated by affiliative behaviours such as grooming and communal nesting in group‐living animals. Whether microbial transmission is also present in animals that do not form groups because territoriality limits interactions and prevents group formation remains unknown. Here, we investigate relationships among gut microbiota, population density and dynamic behavioural and spatial measures of territoriality in wild North American red squirrels (Tamiasciurus hudsonicus). Periods of high population density predicted population‐level gut microbial homogeneity but individual‐level diversification, alongside changes in obligately anaerobic, non‐sporulating taxa indicative of social transmission. Microbial alpha‐diversity increased with more frequent territorial intrusions, and pairs with stronger intrusion‐based social associations had more similar gut microbiota. As some of the first evidence for social microbial transmission in a solitary system, our findings suggest that fluctuations in density and territorial behaviours can homogenise and diversify host microbiomes among otherwise non‐interacting animals. 

In fluctuating environments, phenotypic mismatching may reflect an error-avoidance bias that enhances a mother squirrel’s overall lifetime fitness.