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Seasonal blood-brain barrier plasticity links environmental cues to migratory behavior in monarch butterflies

Aldrin B. LugenaiD, Kayla M. GoforthiD, Vinaya ShettyiD, Ying ZhangiD, Antonio González‐RodrígueziD, M. Isabel RamíreziD, Christine MerliniD

Abstract

Seasonal migration requires animals to reversibly switch behavioral states in response to environmental cues, yet the molecular and cellular mechanisms underlying these transitions remain poorly understood. Monarch butterflies provide a powerful model, as Eastern North American populations undergo a long-distance southward migration in the fall followed by a cold-dependent reversal in flight orientation after overwintering each spring. Here, we show that cold exposure induces coordinated transcriptional changes in the monarch brain, marked by attenuated integrin-mediated extracellular matrix (ECM) signaling at the blood-brain barrier (BBB). Cold-exposed monarchs exhibit increased penetration of fluorescent markers into the brain, consistent with increased BBB permeability. Notably, our findings align with previous genomic evidence identifying collagen type IV alpha 1, a major ECM component, as a locus under divergent selection between migratory and non-migratory populations. Together, these results implicate seasonal modulation of BBB permeability as a mechanism linking environmental temperature to plastic migratory behavior and identify the BBB as a dynamic interface through which seasonal cues may reprogram neural function and behavior.

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02 /Specification & Classification

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