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 inter-connected populations are less studied, as are genetic changes across multiple cycles of demographic collapse and recovery. We take advantage of a long-term dataset 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.

The data files provide microsatellite genotypes, in Genepop format, for the years 2008 and 2013 for the butterfly Parnassius smintheus. Landscape data and microsatellite genotypes for the years 1995 and 2005, which are also used in the manuscript, are available under the following Dryad entry: Caplins, Serena A. et al. (2015), Data from: Landscape structure and the genetic effects of a population collapse, v2, Dryad, Dataset, https://doi.org/10.5061/dryad.d715g.