Current research
One way organisms can cope with fluctuating environments is through anticipatory plasticity, a type of phenotypic plasticity where predictive cues of future conditions are used to adaptively adjust phenotypes before the environment changes. This type of plasticity is less understood than other types of plasticity, but appears to be a relatively widespread strategy across the tree of life. Our group is interested in understanding the proximate mechanisms that allow animals to integrate predictive cues, and the evolutionary processes that maintain this integration.
Read more in our recent synthesis here, with a free plain language summary here.
From Petrullo et al., 2025, Functional Ecology. Mediation of anticipatory plasticity by the neuroendocrine system, epigenome and gut microbiota, their putative molecular mechanisms, and their synergies. Interactions among these systems can occur via the gut–brain axis, and through interplay among substrates like short-chain fatty acids (SCFAs), stress- and appetite-related hormones and their receptors, and genetic regulatory proteins like histones. Through independent and collective effects of these physiological systems and their connections, animals may sense and integrate predictive cues to coordinate anticipatory phenotypic change.
Many animals can change their phenotypes [observable traits] flexibly depending on the demands of their current environment. When these changes result in a fitness benefit, they can be considered adaptive. In wild red squirrels, many females increase adaptively increase reproductive effort by having more pups in the months before a boom of new food occurs (anticipatory reproduction). But some do not, or instead incorrectly increase reproductive effort in years when new food is low to non-existent. We found that the lifetime fitness cost of responding in low-food years was much lower than the cost of failing to respond in rare high-food years. Females that had more pups in low-food years were more likely to have more pups if they encountered a high-food year in their future. Like anticipatory plasticity, these findings help us to understand how animals may use probabilistic strategies to navigate environmental uncertainty.
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From Petrullo et al., 2023, Science. Overestimating mast cues enhances maternal lifetime fitness. (A) Each false positive error (erroneously producing a large litter in a non-mast year) made across a female’s lifetime significantly decreased her probability of making the costliest error (false negative/small litter in a mast year).
Developmental origins of life history plasticity
An organism's early life conditions can exert significant influence over what the rest of its life looks like. Understanding how early-life events shape developmental, reproductive, and physiological trajectories across the lifespan is a central focus of our group's research. Our work in this area is inherently interdisciplinary, combining theoretical frameworks from across subfields to make predictions about how and when animals will use developmental information to adaptively adjust their life history trajectories and preserce fitness despite a rough start.
Growing up squirrel in the southwest Yukon can be tough. Predators abound, winters are extremely cold, food is not consistently available and finding a vacant territory is key in order to survive in the short-term. In line with data from humans and non-human animals (birds, other mammals), juvenile red squirrels that experience a lot of hardship in their first year of life tend to live shorter total lives (i.e., reduced adult lifespan). We have previously shown that a high-quality environment in the second year of life can offset some of this effect. But what does this mean for lifetime fitness? Are juveniles that experienced developmental hardship "doomed" to poorer fitness, or can they compensate for early-life adversity by reorganizing their life history trajectories, given a shorter lifespan?
Microbiome-led integration of environmental cues
Female red squirrels exhibit adaptive increases in reproductive effort in response to ecological cues just prior to a food boom when new and stored food is lowest (anticipatory reproduction). How do female squirrels do more with less? We are currently investigating the relationship between resource pulses, the gut microbiome, and anticipatory reproduction as gut microbiota have the potential to alter host metabolic status by increasing energy availability, nutrient extraction efficiency, and energy harvest from the host diet. Our preliminary data suggest a reconfiguration of the female gut
microbiome in the months leading up to a food pulse. Our group is interested in combining biomarkers of host metabolism, metabolomics, and microbiome data with detailed life history and demographic data to address this question.
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Hypothesized pathway by which gut microbiota may contribute to adaptive phenotypic plasticity.
Microbial transmission as information transfer
Mammalian offspring receive microbiota from multiple sources during early life, and transmission across maternal pools (vaginal, fecal, milk, skin) make up the primary origin source of most first gut microbes. Understanding how and why these maternal microbes contribute to variable developmental trajectories among offspring is central to determining the role host-associated microbiota play in broader patterns of mammalian adaptation and evolution. We are investigating the processes that govern the assembly and maturation of the early life gut microbiome, the maternal origin sources of these patterns, and their contributions to phenotypic variation during development.
Beyond vertical transmission, animals can also spread microbes host-to-host via social interactions ("social transmission"). Most work has focused on social microbial transmission in highly social and semi-social species, but solitary or territorial animals can also spread microbes via aggressive interactions. We find a strong signal of social microbial transmission linked to periods of heightened population density and frequent territorial intrusions by conspecifics in solitary red squirrels, suggesting that even non-social species may maintain pathways for social microbial transfer. Read more here.
The host endocrine system and its resident gut microbiota are involved in bidirectional "cross-talk" in which gut microbes influence host hormone production and vice versa. As both of these physiological components respond to ecological and environmental stimuli, understanding whether these responses are coordinated or independent will contribute to a broader understanding of the evolution of the gut-brain axis in wild animals. As most studies on the gut-brain axis come from experimental models, we are especially interested in integrating ecological factors into hormone-microbiome studies in wild populations. This is also the main thrust of our NIH MIRA (R35) award.
Read more here:
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Petrullo, L., Ren, T., Wu, M., Boonstra, R., Palme, R., Boutin S., McAdam, A.G., Dantzer, B. Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels. Scientific Reports 12, 2605. [pdf]
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Petrullo, L., Santangeli, A., Wistbacka, R., Husby, A., Raulo, A. Indirect environmental effect on the gut-brain axis in a wild mammal. Molecular Ecology 34, e70149, [pdf]