Demographic fluctuations lead to rapid and cyclic shifts in genetic structure among populations of an alpine butterfly, Parnassius smintheus

• Published in: Journal of evolutionary biology Vol. 33; no. 5; pp. 668 - 681
• Main Authors: Jangjoo, Maryam, Matter, Stephen F., Roland, Jens, Keyghobadi, Nusha
• Format: Journal Article
• Language: English
• Published: Switzerland Blackwell Publishing Ltd 01.05.2020
• Subjects: bottleneck; Bottlenecks; Butterflies & moths; Demographics; Differentiation; Gene flow; Gene frequency; Genetic diversity; Genetic drift; Genetic structure; Insects; isolation by distance; landscape; Population genetics; Population number; Population studies; Populations; recovery; spatial genetic structure; time lag; gene flow; isolation by distance; genetic drift; spatial genetic structure; bottleneck; time lag; recovery; landscape
• ISSN: 1010-061X; 1420-9101
• DOI: 10.1111/jeb.13603

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. We document rapid and cyclic changes in genetic structure across a network of interconnected populations, due to continual shifts in the relative dominance of genetic drift versus gene flow as populations fluctuate in size. This study provides insights into the evolutionary dynamics of population networks and metapopulations, genetic effects of population size fluctuation, and time lags.