Temporal fitness fluctuations in experimental Arabidopsis thaliana populations

Abstract

Understanding the genetics of lifetime fitness is crucial to understand a species’ ecological preferences and ultimately predict its ability to cope with novel environmental conditions. Yet, there is a dearth of information regarding the impact of the ecological variance experienced by natural populations on expressed phenotypic and fitness differences. Here, we follow the natural dynamics of experimental A. thaliana populations over 5 successive plantings whose timing was determined by the natural progression of the plant’s life cycle and disentangle the environmental and genetic factors that drive plant ecological performance at a given locality. We show that, at the temperate latitude where the experiment was conducted, a given genotype can experience winter-, spring- or summer-annual life cycles across successive seasons. Lifetime fitness across these seasons varied strongly, with a fall planting yielding 36-fold higher fitness compared to a spring planting. In addition, the actual life-stage at which plant overwinter oscillated across years, depending on the timing of the end of the summer season. We observed a rare but severe fitness differential coinciding with inadequate early flowering in one of the five planting. Substrate variation played a comparatively minor role, but also contributed to modulate the magnitude of fitness differentials between genotypes. Finally, reciprocal introgressions on chromosome 4 demonstrated that the fitness effect of a specific chromosomal region is strongly contingent on micro-geographic and seasonal fluctuations. Our study contributes to emphasize the extent to which the fitness impact of phenotypic traits and the genes that encode them in the genome can fluctuate. Experiments aiming at dissecting the molecular basis of local adaptation must apprehend the complexity introduced by temporal fluctuations because they massively affect the expression of phenotype and fitness differences.

Linking genes with ecological strategies in Arabidopsis thaliana

“…Much of the flowering time variation measured in the lab, however, does not manifest as variation in flowering phenology in the field (Wilczek et al , 2009; Brachi et al , 2010; Hu et al , 2017). It is indeed tightly dependent on the environmental conditions prevailing during seedling establishment, and hence on another developmental trait: the timing of germination (Donohue, 2002; Wilczek et al , 2009).…”

“…For example, maintaining a spring germinating cohort is important for the maintenance of populations exposed to low winter temperature (Picó, 2012; Akiyama and Ågren, 2014). Furthermore, later flowering can lead to late seed dispersal, which can result in overwintering at the seed stage (Hu et al , 2017).…”

“…Normally, diverse life history trait combinations can allow comparable population growth rates in field conditions (Taylor et al , 2017). In some years, however, early winter frost can wipe out genotypes expressing inadequate life histories (Hu et al 2017). Minimum winter temperature and precipitation, in fact, were also the main climatic factors that acted as selective pressures on flowering time and their underpinning genes in a set of Iberian A. thaliana genotypes (Méndez-Vigo et al , 2011).…”

Support for the Adaptive Decoupling Hypothesis from Whole-Transcriptome Profiles of a Hypermetamorphic and Sexually Dimorphic Insect,Neodiprion lecontei

“…Although this prediction has been confirmed by several studies for sex-biased genes (Assis et al, 2012; Drosophila 12 Genomes et al, 2007; Mank, Nam, Brunstrom, & Ellegren, 2010; Proschel et al, 2006; L. Yang, Zhang, & He, 2016), it has rarely been tested in the context of stage-biased expression across metamorphic boundaries (but see (Perry et al, 2014)). An alternative approach would be to use experimental genomics to connect genetic variants directly to fitness at different life stages (e.g., (Egan et al, 2015; Gloss, Groen, & Whiteman, 2016; Gompert et al, 2019; Ingvarsson, Hu, Lei, & de Meaux, 2017)). Following exposure to a selection regime that favors different traits at different ontogenetic stages, the ADH predicts that genes with the most decoupled expression will exhibit the most pronounced allele frequency shifts.…”

Association analysis of phenotypic and metabolomic changes in Arabidopsis accessions and their F₁ hybrids affected by different photoperiod and sucrose supply

“…There was little effect on the fresh weight of C24 when increasing the exogenous Suc concentration from 1.5 to 2% (Wang et al 2019). Geographical variation of Col and C24 accessions might have a considerable influence on nutrient uptake or photoperiodic stimulus (Fujimoto et al 2012;Hu et al 2017;Ibañez et al 2017;Miao et al 2018;Stangeland et al 2009;Yang et al 2010).…”