Evaluating the evolutionary history, geographic distribution, and renal adaptations to arid environments of Microtus voles in Northern Pakistan

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2024-08

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The Ohio State University

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Abstract

Rodents are well known to exhibit physiological differences in kidney features depending on aridity. Voles in the highly speciose genus Microtus inhabit many habitats across Eurasia and North America and occupy areas that range from arid to wet climates. Prior to this study, only a single species of Microtus vole, M. yuldaschi, was known from Pakistan, having been collected at only two sites along the northern border. We sequenced the mitochondrial cytochrome b gene for 37 individual voles collected in Pakistan and additional specimens from outside of Pakistan and compared these to other Microtus sequences found in GenBank. We also examined how the ethanol-preserved kidneys of our target Microtus samples physically compared to rodents adapted to dry and wet climates, specifically the gerbil, Gerbilliscus, and the rainforest mouse Malacomys. We recovered Microtus in Pakistan as belonging to 3 separate radiations, each of which contain lineages that exhibit magnitudes of divergence that approach species-level genetic differences. Our results extend the range of the juniper vole, M. (Blanfordimys) yuldaschi in northernmost Pakistan and recover a divergent isolated lineage from Azad Kashmir. The Afghan vole, M. (B.) afghanus is found in several sites in northwestern Pakistan and shows patterns of population structuring based on geography. We report the presence of voles in the Safed Koh range that form a clade sister to the Transcaspian vole, M. (Microtus) transcaspicus. We find no statistically significant niche overlap among our target species and make relative comparisons regarding preferred habitat for each species. Microtus yuldaschi inhabits areas with relatively low precipitation that is highly seasonal, with dry summers and winters with more precipitation. The preferred habitat of M. transcaspicus also involves low precipitation. Microtus afghanus is also highly seasonal, but experiences higher precipitation levels than M. yuldaschi. We demonstrate the effectiveness of ethanol-preserved kidneys for comparative analyses of morphological features, highlighting anatomical differences influenced by aridity. Microtus yuldaschi appears to be a dry-adapted vole, whereas M. afghanus is more mesic-adapted. Several specimens of another vole in region, Hyperacrius, appear to be better adapted to mesic environments compared to M. afghanus. Evaluation of kidneys from voles in Azad Kashmir suggests that both M. yuldaschi and Hyperacrius inhabit the region. Our study highlights the physiological and genetic diversity among Microtus voles in Pakistan, elaborating on the adaptations of different species to varying climatic conditions and the importance of these regions as reservoirs of unrecognized small mammal biodiversity.

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Microtus, voles, Pakistan, phylogeny, niche modeling, Blanfordimys, kidney morphology, Safed Koh, Azad Kashmir

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