Abstract

Analyzing genetic variation through time and space is important to identify key evolutionary and ecological processes in populations. However, using contemporary genetic data to infer the dynamics of genetic diversity may be at risk of a bias, as inferences are performed from a set of extant populations, setting aside unavailable, rare, or now extinct lineages. Here, we took advantage of new developments in next‐generation sequencing to analyze the spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus, a steppic Southwestern‐Palearctic species. We applied a recently developed hybridization capture (hyRAD) protocol that allows retrieving orthologous sequences even from degraded DNA characteristic of museum specimens. We identified single nucleotide polymorphisms in 68 historical and 51 modern samples in order to (i) unravel the spatial genetic structure across part of the species distribution and (ii) assess the loss of genetic diversity over the past century in Swiss populations. Our results revealed (i) the presence of three potential glacial refugia spread across the European continent and converging spatially in the Alpine area. In addition, and despite a limited population sample size, our results indicate (ii) a loss of allelic richness in contemporary Swiss populations compared to historical populations, whereas levels of expected heterozygosities were not significantly different. This observation is compatible with an increase in the bottleneck magnitude experienced by central European populations of O. decorus following human‐mediated land‐use change impacting steppic habitats. Our results confirm that application of hyRAD to museum samples produces valuable information to study genetic processes across time and space.

Highlights

  • The aim of this study was to combine genetic data generated from museum specimens and modern samples to reconstruct the spatial genetic structure of O. decorus across its distribution range and to uncover the changes in genetic diversity over the past decades at the Swiss scale

  • We analyzed mitochondrial and single nucleotide polymorphism (SNP) data and highlighted four lineages, which produced spatial genetic clustering at the scale of the western Palearctic that were generally consistent between both approaches

  • We identified a decrease in allelic richness in contemporary populations

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Summary

| INTRODUCTION

Understanding processes shaping the genetic variation in species through space and time is crucial in various fields of biology, ranging from informing conservation decisions (e.g., Inoue, Lang, & Berg, 2015; Mukesh, Sharma, Shukla, & Sathyakumar, 2015) and unraveling the demographic history of species (e.g., Gong et al, 2015; Tsuda, Nakao, Ide, & Tsumura, 2015; Vera Escalona, Habit, & Ruzzante, 2015) to. Recent or older divergence followed by recent gene flow both result in weakly differentiated populations (Ramakrishnan & Hadly, 2009) Events such as genetic bottlenecks may eliminate past genetic signatures, rendering ancient demographic processes difficult to detect (Heled & Drummond, 2008). Overcoming these difficulties might be achieved by analyzing historical genetic data in order to get a direct insight into the demographic and evolutionary history of populations (Schwartz et al, 2007) This might allow, for instance, understanding the causes of temporal fluctuations in effective population size as indirectly identified using genetic diversity estimates and may provide information about the response of populations to past events such as human-­driven disturbances (e.g., Hartmann, Schaefer, & Segelbacher, 2014; Poudel, Moeller, Li, Shah, & Gao, 2014). We discuss how the retrieved information can inform about future prospects regarding conservation of O. decorus in Switzerland and validate the benefits of incorporating museum samples into genetic analyses

| MATERIAL AND METHODS
| DISCUSSION
CONFLICT OF INTEREST
Findings
DATA ACCESSIBILITY
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