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.

Highlights

  • There is overwhelming evidence that local selection pressures have shaped the genetic composition and ecological performance of natural populations [1,2,3]

  • We monitored average silique production in experimental A. thaliana populations over five naturally consecutive plantings by counting the average number of siliques produced per pot (Fig 1)

  • In the remaining of the analysis, plant density was included as a cofactor, so that the genetic and environmental effect reported below are independent of population density

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Summary

Introduction

There is overwhelming evidence that local selection pressures have shaped the genetic composition and ecological performance of natural populations [1,2,3]. The phenotypes that plants manifest in nature, i.e. their timing of germination, their growth rate, and their timing of reproduction, are plastically regulated by environmental conditions that vary both temporally and geographically [7]. Much is known about the molecular mechanisms of many plastic plant traits [8,9,10]. This plasticity may buffer the effect of environmental fluctuations on fitness and thereby decrease year-to-year fluctuations in selective pressures [5]. We know little about how environmental fluctuations influence the amount of phenotypic variation that is expressed in natural conditions, nor do we know how it impacts population levels of fitness variance, an elemental requirement for adaptive evolution [11]

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