Extreme copy number variation at a tRNA ligase gene affecting phenology and fitness in yellow monkeyflowers. Issue 6 (10th December 2018)

• Record Type: Journal Article
• Authors: Nelson, Thomas C.; Monnahan, Patrick J.; McIntosh, Mariah K.; Anderson, Kayli; MacArthur‐Waltz, Evan; Finseth, Findley R.; Kelly, John K.; Fishman, Lila
• Other Names: Wellenreuther Maren guestEditor.; Mérot Claire guestEditor.; Berdan Emma guestEditor.; Bernatchez Louis guestEditor.
• Is Part Of: Molecular ecology. Volume 28:Issue 6(2019)
• Page Start: 1460
• Page End: 1475
• Publication Date: 2018-12-10
• Subjects: balancing selection -- flowering time -- fluctuating selection -- life history -- standing variation -- structural variant; Molecular ecology -- Periodicals; Molecular population biology -- Periodicals; 576
• DOI: 10.1111/mec.14904
• Languages: English
• ISSNs: 0962-1083

Abstract

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 totalling ~5.7 Mb (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 to 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.