Extreme copy number variation at a tRNA ligase affecting phenology and fitness in yellow monkeyflowers

Abstract

Copy number variation (CNV) is a major part of the genetic diversity segregating within populations, but remains poorly understood relative to single nucleotide variation. Here, we report on a tRNA ligase gene (Migut.N02091; RLG1a) exhibiting unprecedented, and fitness-relevant, CNV within an annual population of the yellow monkeyflower Mimulus guttatus. RLG1a variation was associated with multiple traits in pooled population sequencing (PoolSeq) scans of phenotypic and phenological cohorts. Resequencing of inbred lines revealed intermediate frequency three-copy variants of RLG1a (trip+; 5/35 = 14%), and trip+ lines exhibited elevated RLG1a expression under multiple conditions. trip+ carriers, in addition to being over-represented in late-flowering and large-flowered PoolSeq populations, flowered later under stressful conditions in a greenhouse experiment (P < 0.05). In wild population samples, we discovered an additional rare RLG1a variant (high+) that carries 250-300 copies of RLG1a totaling ∼5.7Mb (20-40% of a chromosome). In the progeny of a high+ carrier, Mendelian segregation of diagnostic alleles and qPCR-based copy counts indicate that high+ is a single tandem array unlinked from the single copy RLG1a locus. In the wild, high+ carriers had highest fitness in two particularly dry and/or hot years (2015 and 2017; both p < 0.01), while single copy individuals were twice as fecund as either CNV type in a lush year (2016: p < 0.005). Our results demonstrate fluctuating selection on CNVs affecting phenological traits in a wild population, suggest that plant tRNA ligases mediate stress-responsive life-history traits, and introduce a novel system for investigating the molecular mechanisms of gene amplification.

A second unveiling: haplotig masking of the eastern oyster genome improves population-level inference

“…Understanding the role of structural variants in adaptation and population structure has taken a more prominent role in molecular ecology (Bazzicalupo et al, 2020; Mérot, Oomen, Tigano, & Wellenreuther, 2020; Modak et al, 2021; Nelson et al, 2019; Prunier et al, 2019; Wellenreuther, Mérot, Berdan, & Bernatchez, 2019). Our analysis indicates that while haplotigs do affect structural variant detection and discovery, haplotigs, do not affect estimates of differentiation based on copy number variation.…”

The genomic scale of fluctuating selection in a natural plant population

“…Except for 2021, these collections were conducted as part of other studies (Fishman and Kelly, 2015, Kelly, 2008, Fishman and Willis, 2008, Lee et al., 2016, Nelson et al., 2019). To make sequencing libraries, we randomly sorted maternal families into two groups within each year (Samples 1 and 2 in Figure 1).…”

“…Among all plants that had produced fruit, a random sample was harvested with all seeds from each plant collected into an envelope. The number of maternal families varied from year-to-year and are reported in Except for 2021, these collections were conducted as part of other studies (Fishman and Kelly, 2015, Kelly, 2008, Fishman and Willis, 2008, Lee et al, 2016, Nelson et al, 2019. To make sequencing libraries, we randomly sorted maternal families into two groups within each year (Samples 1 and 2 in Figure 1).…”

Opportunities and challenges for high‐quality biodiversity tissue archives in the age of long‐read sequencing

“…Looking beyond the study of human populations, there is also increasing evidence that structural variation in non‐model organisms is directly or indirectly responsible for adaptive phenotypes in nature (Weissensteiner et al, 2020; Wellenreuther et al, 2019). For instance, inversions can preserve linkage between beneficial alleles despite gene flow (Lee et al, 2017), copy‐number variants can influence gene dosage expression (Nelson et al, 2019) and chromosomal rearrangements can drive reproductive isolation (de Vos et al, 2020). These observations emphasize that structural variants can have a demonstrable effect on fitness, prevent recombination and may eventually drive speciation (Feulner & De‐Kayne, 2017).…”