Many populations, especially in insects, fluctuate in size, and periods of particularly low population size can have strong effects on genetic variation. Effects of demographic bottlenecks on genetic diversity of single populations are widely documented. Effects of bottlenecks on genetic structure among multiple interconnected populations are less studied, as are genetic changes across multiple cycles of demographic collapse and recovery. We take advantage of a long‐term data set comprising demographic, genetic and movement data from a network of populations of the butterfly, Parnassius smintheus, to examine the effects of fluctuating population size on spatial genetic structure. We build on a previous study that documented increased genetic differentiation and loss of spatial genetic patterns (isolation by distance and by intervening forest cover) after a network‐wide bottleneck event. Here, we show that genetic differentiation was reduced again and spatial patterns returned to the system extremely rapidly, within three years (i.e. generations). We also show that a second bottleneck had similar effects to the first, increasing differentiation and erasing spatial patterns. Thus, bottlenecks consistently drive random divergence of allele frequencies among populations in this system, but these effects are rapidly countered by gene flow during demographic recovery. Our results reveal a system in which the relative influence of genetic drift and gene flow continually shift as populations fluctuate in size, leading to cyclic changes in genetic structure. Our results also suggest caution in the interpretation of patterns of spatial genetic structure, and its association with landscape variables, when measured at only a single point in time.

中文翻译：

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人口统计学波动导致高山蝴蝶 Parnassius smintheus 种群遗传结构的快速循环变化

许多种群，尤其是昆虫种群，其规模波动，种群规模特别低的时期会对遗传变异产生强烈影响。人口瓶颈对单一种群遗传多样性的影响已被广泛记录。瓶颈对多个相互关联种群之间遗传结构的影响研究较少，人口崩溃和恢复的多个周期中的遗传变化也是如此。我们利用包含来自蝴蝶 Parnassius smintheus 种群网络的人口统计、遗传和运动数据的长期数据集来检查种群规模波动对空间遗传结构的影响。我们建立在先前的研究的基础上，该研究记录了在网络范围的瓶颈事件之后增加的遗传分化和空间遗传模式的丧失（距离隔离和干预森林覆盖）。在这里，我们表明遗传分化再次减少，空间模式在三年内（即世代）非常迅速地恢复到系统中。我们还表明，第二个瓶颈与第一个瓶颈具有相似的影响，增加了差异化并消除了空间模式。因此，瓶颈始终驱动该系统中种群间等位基因频率的随机发散，但这些影响在人口恢复期间被基因流迅速抵消。我们的结果揭示了一个系统，其中遗传漂变和基因流的相对影响随着种群大小的波动而不断变化，导致遗传结构的周期性变化。我们的结果还表明，当仅在单个时间点进行测量时，在解释空间遗传结构模式及其与景观变量的关联时要谨慎。