Abstract

Whether the effect of migration-selection-drift equilibrium on population structure is governed by spatial or environmental differences is usually elucidated by isolation-by-distance (IBD), isolation-by-environment (IBE), and isolation-by-resistance (IBR) tests. The population structure of Ammopiptanthus mongolicus, a broad-leaved evergreen psammophyte in eastern Central Asia, was previously thought to follow an isolation by distance pattern. However, recent studies have emphasized the effects of environmental factors on its growth and distribution, suggesting an important influence of local adaptation on the genetic structure of the species. Using inter-simple sequence repeat (ISSR) markers, we verified the previously inferred low intra-population variation and high inter-population differentiation. However, in contrast to previous studies, the results of partial Mantel tests and a maximum likelihood population effects mixed model (MLPE) suggested that local climate differences, rather than geographic distances or resistance distances, are the main factor affecting population differentiation. Further analysis with removal of multicollinear climatic variables and univariate MLPE found that summer and winter precipitation were crucial for shaping the current population genetic structure. Since local precipitation is related to the regeneration, colonization, and overwintering survival of A. mongolicus, its influence on demographic change may explain its effect on the population genetic structure. In addition, precipitation is related to terrain despite westward decreases, which explains the independence of genetic difference and geographic distance. The identified role of IBE suggests that collecting germplasm resources from genetically differentiated populations could be a more effective strategy to preserve the overall genetic diversity of the species than the establishment of corridors to enhance gene flow among populations.

Highlights

  • Random genetic drift, environment-leading selection, genetic draft, and background selection may affect the genetic diversity of organisms[1]

  • That is, when environmental conditions differ, the reduced establishment success of immigrants may accelerate the genetic fixation rate due to the decreased chance of outcrossing, thereby enhancing genetic isolation. This phenomenon appears in adaptive loci but could extend to the whole genome via genetic draft caused by selective sweeps[1]

  • When evaluating “single-large or several-small” (SLOSS) strategies for planning a protected area, the several-small strategy and/or collection of germplasm resources from different populations for ex situ conservation should be adopted for species with a signature of local adaptation, whereas a single-large strategy may be appropriate for species with IBD or low genetic structure[15]

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Summary

Introduction

Environment-leading selection, genetic draft (hitchhiking), and background selection may affect the genetic diversity of organisms[1]. Geographic distance and environmental difference are two key factors affecting genetic structure between populations[2] The former is related to the interplay of genetic drift and movement, while the latter is usually related to the adaptability to environmental pressure[3]. That is, when environmental conditions differ, the reduced establishment success of immigrants may accelerate the genetic fixation rate due to the decreased chance of outcrossing, thereby enhancing genetic isolation This phenomenon appears in adaptive loci but could extend to the whole genome via genetic draft caused by selective sweeps[1]. The impact of geographic distance or environmental difference on genetic differences among populations of a species reveals differences in resilience in adapting to heterogeneous environments[11]. The test of IBD, IBE, and IBR can help to understand the process of population genetic differentiation, which will provide a reference for habitat conservation and management of endangered species

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