Genome-wide fluctuating selection under demographic cycling in Icelandic rock ptarmigan

Abstract

Understanding how natural populations adapt to continuously shifting environments is central to evolutionary biology. Multi-annual population cycles impose temporally varying selective pressures, yet disentangling the resulting genomic signals from those of sustained directional selection and genetic drift has been challenging due to a lack of high-resolution temporal data. Here we investigate the genomic consequences of demographic cycling in a population of rock ptarmigan (Lagopus muta) from northeastern Iceland. We analyzed whole-genome sequences from 91 individuals sampled over an 11-year period, encompassing two population peaks (2010 and 2018) and two troughs (2007 and 2013). Testing allele frequency change at each SNP against a null model of drift and sampling, we identified candidate loci and grouped them by correlation of their temporal trajectories. Cluster trajectories fluctuated through time, and two were closely correlated with the regional census, one significantly tracking the demographic cycle, while a smaller set changed monotonically in a manner consistent with sustained directional selection. Each cluster contained loci distributed across many chromosomes, indicative of genome-wide responses to selection. The most strongly fluctuating loci overlapped candidate genes of possible functional relevance, most notably CTNNA2 (Catenin Alpha-2), which is associated with startle response and anxiety-like behaviors and may relate to predator avoidance. Our findings indicate that fluctuating selection comprises much of the temporal genomic response in this natural population, and suggest that multi-annual demographic cycles can drive rapid and widespread allele frequency change, highlighting the value of temporal genomics for clarifying the interplay between demography and natural selection in wild populations.