The genomic scale of fluctuating selection in a natural plant population

Abstract

This study characterizes evolution at ≈1.86 million Single Nucleotide Polymorphisms (SNPs) within a natural population of yellow monkeyflower (Mimulus guttatus). Most SNPs exhibit minimal change over a span of 23 generations (less than 1% per year), consistent with neutral evolution in a large population. However, several thousand SNPs display strong fluctuations in frequency. Multiple lines of evidence indicate that these ‘Fluctuating SNPs’ are driven by temporally varying selection. Unlinked loci exhibit synchronous changes with the same allele increasing consistently in certain time intervals but declining in others. This synchrony is sufficiently pronounced that we can roughly classify intervals into two categories, “green” and “yellow,” corresponding to conflicting selection regimes. Alleles increasing in green intervals are associated with early life investment in vegetative tissue and delayed flowering. The alternative alleles that increase in yellow intervals are associated with rapid progression to flowering. Selection on the Fluctuating SNPs produces a strong ripple effect on variation across the genome. Accounting for estimation error, we estimate the distribution of allele frequency change per generation in this population. While change is minimal for most SNPs, diffuse hitchhiking effects generated by selected loci may be driving neutral SNPs to a much greater extent than classic genetic drift.

Substitution load revisited: a high proportion of deaths can be selective

“…Similarly, there is no cancelling out across generations, e.g. seasonally fluctuating selection must incur many selective deaths in order to effect the large allele frequency fluctuations that have been observed around the long-term mean (Kelly 2022; Machado et al 2021; Rudman et al 2022).…”

“…Similarly, there is no cancelling out across generations, e.g. seasonally fluctuating selection must incur many selective deaths in order to effect the large allele frequency fluctuations that have been observed around the long-term mean (Kelly 2022; Machado et al 2021; Rudman et al 2022). This high demand for selective deaths also applies, given life history trade-offs, to unobserved effects that more quickly cancel out between successive life history transitions.…”

The quantitative genetics of gene expression in Mimulus guttatus

“…This species exhibits remarkably high gene sequence and insertion/deletion (indel) variation, even within local populations [30]. In fact, it is difficult to reliably map Illumina sequencing reads to intergenic regions of the M. guttatus reference genome where indel variation is very high [31]. Such variation could affect gene expression insofar as binding of regulatory elements to the DNA surrounding genes affects expression.…”

The contribution of gene flow, selection, and genetic drift to five thousand years of human allele frequency change

“…Many different modes of selection are expected to generate these covariance patterns (Buffalo & Coop, 2020; Santiago & Caballero, 1998). This approach has been applied to experimental evolution datasets (Brennan et al, 2022; Buffalo & Coop, 2020) and to natural populations where temporal sampling is available (in Mimulus , oaks and cod; Kelly, 2022; Reid et al, 2023; Saleh et al, 2022). These applications, along with related methods (Bertram, 2021), have revealed that a reasonable proportion of total allele frequency change, especially in artificial selection experiments, can be attributed to widespread selection beyond just a few outliers.…”