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The reddish-gray mouse lemur (Microcebus griseorufus) possesses striking phenotypic and behavioral variation. This project investigates differences in autopod proportions in neighboring populations of M. griseorufus from the Special Reserve at Bezà Mahafaly in southwest Madagascar. One population resides in an environment generally preferred by M. griseorufus-a spiny forest with large-trunked trees, vertically-oriented supports, and more open ground, while the other resides in a gallery forest with abundant small, often horizontal peripheral branches in high canopy. We demonstrate significant interpopulation differences in autopod morphophology despite no evidence of divergence in mitochondrial cytochrome b. We test two hypotheses regarding ultimate causation. The first, based on the Fine Branch Arborealism Hypothesis (FBAH), holds that autopod differences are related to different locomotor practices in the two environments, and the second, based on the Narrow Niche Hypothesis (NNH), holds that the observed differences reflect a relaxation (from ancestral to descendant conditions) of selective pressure for terrestrial locomotion and/or use of large, vertical supports combined with positive selection for locomoting in peripheral branch settings. Our data conform well to FBAH expectations and show some support for the NNH. Individuals from the gallery forest possess disproportionally long posterior digits that facilitate locomotion on small, flexible canopy supports while individuals from the spiny forest possess shorter posterior digits and a longer pollex/hallux that increase functional grasping diameter for large vertical supports and facilitate efficient ground locomotion. Focal individual data confirm differences in how often individuals descend to the ground and use vertical supports. We further show that predispersal juveniles, like adults, possess autopod morphologies suited to their natal forest. We explore two proximate mechanisms that could generate these cheiridial differences. The first posits an in vivo plastic response to different locomotor behaviors, the second posits differences that manifest in early development., (© 2017 Wiley Periodicals, Inc.)