Evolutionary and physiological drivers of phenotypic plasticity
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 (reproductive plasticity). 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. The evolution of adaptive plasticity therefore may hinge on the way animals balance the relative costs and benefits of different phenotypic responses over the lifetime.
Hear and read more about this work below:
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Petrullo, L., Boutin, S., Lane, J.E., McAdam, A.G., Dantzer, B. Phenotype-environment mismatch errors enhance lifetime fitness in wild red squirrels. Science 379, 269-272. [pdf]
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University of Michigan press release [link]
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Michigan Minds Podcast [link]
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St. Albert Gazette [link]
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Popular Science [link]
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Modified 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 control female’s lifetime significantly decreased her probability of making the costliest error.
Does the gut microbiome play a role in anticipatory reproduction?
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. Preliminary data demonstrate mast cue-induced changes in gut microbiome composition among females. We are combining biomarkers of host metabolism, metabolomics, and microbiome analysis with detailed life history and demographic data to address this question.
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Conceptual figure illustrating hypothesized pathway through which the gut microbiome contributes to adaptive phenotypic plasticity.
Maternal and early-life effects on developmental variation
Vertical transmission of maternal microbiota
Mammalian offspring receive their gut 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. To get at these questions, we work with a captive breeding colony of vervet monkeys at Wake Forest University in North Carolina. We are especially interested in investigating the role of milk microbiota in variation in infant immune, metabolic, and neuroendocrine outcomes.
Read more here:
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Petrullo, L., Baniel, A., Jorgensen, M., Sams, S., Snyder-Mackler, N., Lu, A. Early life gut microbiome dynamics mediate maternal effects on infant growth in vervet monkeys. iScience 25, 103948. [pdf]
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Petrullo, L., Jorgensen, M., Snyder-Mackler, N., Lu, A. Composition and stability of the vervet monkey milk microbiome. American Journal of Primatology, e22982. [pdf]
Modified from Petrullo et al., 2022, iScience. (A) Across all infants, the infant gut microbiome shares ~10% more ASVs with milk than with the maternal gut at T1 (2-5 days old). Transmission rates do not differ at T2 (4 months old). (B) Infants born to low parity females exhibit stronger ASV sharing with the milk microbiome at T1 (2–5 days old) compared to infants of high parity females.
What causes variation in physiological responses to environmental conditions?
The eco-gut-brain axis
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.
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]
Figure from Petrullo et al., 2022, Scientific Reports. Ecology and host biology influence gut microbiome alpha diversity via changes in host glucocorticoids. Structural equation model assessing direct and indirect effects of ecological and host factors on glucocorticoids (GCs) and gut microbiome alpha diversity (Chao1 richness). Solid black arrows represent significant positive paths; solid red arrows represent significant negative paths; dotted arrows represent non-significant paths. Text labels indicate standardized beta estimates (i.e., effect sizes) and significance (P < 0.05*, P < 0.01**, P < 0.001***) for each of the predicted pathways tested in the SEM.
Specificity of physiological responses
Physiological systems, in their scope and sensitivity, can shape the evolutionary trajectories of organisms by inhibiting or promoting adaptive phenotypic responses to environmental challenges. However, in highly fluctuating environments, animals face a "cocktail party problem" where they receive lots of information at once and have to discern what is worth listening and responding to. When information is relevant for an animal's fitness, it's especially valuable. We found no evidence for this sort of selectivity in glucocorticoid responses in red squirrels, and individuals exhibited hormonal responses to environmental conditions regardless of whether those conditions acted as "agents of selection" by impacting the relationship between traits + fitness. We are currently interested in determining whether squirrels exhibit selectivity in gut microbiome responses to fluctuating environmental conditions.
Read more here:
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Petrullo, L., Delaney, D., Boutin S., McAdam, A.G., Lane, J.E., Boonstra, R., Palme, R., Dantzer, B. The glucocorticoid response to environmental change is not specific to agents of natural selection in wild red squirrels. Hormones and Behavior 146, 105262. [pdf]