The seasonal timing of life history transitions is often critical to fitness, and many organisms rely upon environmental cues to match life cycle events with favorable conditions. In plants, the timing of seed germination is mediated by seasonal cues such as rainfall and temperature. Variation in cue responses among species can reflect evolutionary processes and adaptation to local climate and can affect vulnerability to changing conditions. Indeed, climate change is altering the timing of precipitation, and germination responses to such change can have consequences for individual fitness, population dynamics, and species distributions. Here, we assessed responses to the seasonal timing of germination‐triggering rains for eleven species spanning the
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Abstract Streptanthus /Caulanthus clade (Brassicaceae). To do so, we experimentally manipulated the onset date of rainfall events, measured effects on germination fraction, and evaluated whether responses were constrained by evolutionary relationships across the phylogeny. We then explored the possible consequences of these responses to contemporary shifts in precipitation timing. Germination fractions decreased with later onset of rains and cooler temperatures for all but threeCaulanthus species. Species' germination responses to the timing of rainfall and seasonal temperatures were phylogenetically constrained, withCaulanthus species appearing less responsive. Further, four species are likely already experiencing significant decreases in germination fractions with observed climate change, which has shifted the timing of rainfall towards the cooler, winter months in California. Overall, our findings emphasize the sensitivity of germination to seasonal conditions, underscore the importance of interacting environmental cues, and highlight vulnerability to shifting precipitation patterns with climate change, particularly in more northern, mesic species. -
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Abstract In Mediterranean climates, the timing of seasonal rains determines germination, flowering phenology and fitness. As climate change alters seasonal precipitation patterns, it is important to ask how these changes will affect the phenology and fitness of plant populations. We addressed this question experimentally with the annual plant species
Arabidopsis thaliana .In a first experiment, we manipulated the date of rainfall onset and recorded germination phenology on sand and soil substrates. In a second experiment, we manipulated germination date, growing season length and mid‐season drought to measure their effects on flowering time and fitness. Within each experiment, we manipulated seed dormancy and flowering time using multilocus near‐isogenic lines segregating strong and weak alleles of the seed dormancy gene
DOG1 and the flowering time geneFRI . We synthesized germination phenology data from the first experiment with fitness functions from the second experiment to project population fitness under different seasonal rainfall scenarios.Germination phenology tracked rainfall onset but was slower and more variable on sand than on soil. Many seeds dispersed on sand in spring and summer delayed germination until the cooler temperatures of autumn. The high‐dormancy
DOG1 allele also prevented immediate germination in spring and summer. Germination timing strongly affected plant fitness. Fecundity was highest in the October germination cohort and declined in spring germinants. The late floweringFRI allele had lower fecundity, especially in early fall and spring cohorts. Projections of population fitness revealed that: (1) Later onset of autumn rains will negatively affect population fitness. (2) Slow, variable germination on sand buffers populations against fitness impacts of variable spring and summer rainfall. (3) Seasonal selection favours high dormancy and early flowering genotypes in a Mediterranean climate with hot dry summers. The high‐dormancyDOG1 allele delayed germination of spring‐dispersed fresh seeds until more favourable early fall conditions, resulting in higher projected population fitness.These findings suggest that Mediterranean annual plant populations are vulnerable to changes in seasonal precipitation, especially in California where rainfall onset is already occurring later. The fitness advantage of highly dormant, early flowering genotypes helps explain the prevalence of this strategy in Mediterranean populations.
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The seasonal timing of seed germination determines a plant’s realized environmental niche, and is important for adaptation to climate. The timing of seasonal germination depends on patterns of seed dormancy release or induction by cold and interacts with flowering-time variation to construct different seasonal life histories. To characterize the genetic basis and climatic associations of natural variation in seed chilling responses and associated life-history syndromes, we selected 559 fully sequenced accessions of the model annual species Arabidopsis thaliana from across a wide climate range and scored each for seed germination across a range of 13 cold stratification treatments, as well as the timing of flowering and senescence. Germination strategies varied continuously along 2 major axes: 1) Overall germination fraction and 2) induction vs. release of dormancy by cold. Natural variation in seed responses to chilling was correlated with flowering time and senescence to create a range of seasonal life-history syndromes. Genome-wide association identified several loci associated with natural variation in seed chilling responses, including a known functional polymorphism in the self-binding domain of the candidate gene DOG1. A phylogeny of DOG1 haplotypes revealed ancient divergence of these functional variants associated with periods of Pleistocene climate change, and Gradient Forest analysis showed that allele turnover of candidate SNPs was significantly associated with climate gradients. These results provide evidence that A. thaliana ’s germination niche and correlated life-history syndromes are shaped by past climate cycles, as well as local adaptation to contemporary climate.more » « less
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Contrary to previous assumptions that most mutations are deleterious, there is increasing evidence for persistence of large-effect mutations in natural populations. A possible explanation for these observations is that mutant phenotypes and fitness may depend upon the specific environmental conditions to which a mutant is exposed. Here, we tested this hypothesis by growing large-effect flowering time mutants of Arabidopsis thaliana in multiple field sites and seasons to quantify their fitness effects in realistic natural conditions. By constructing environment-specific fitness landscapes based on flowering time and branching architecture, we observed that a subset of mutations increased fitness, but only in specific environments. These mutations increased fitness via different paths: through shifting flowering time, branching, or both. Branching was under stronger selection, but flowering time was more genetically variable, pointing to the importance of indirect selection on mutations through their pleiotropic effects on multiple phenotypes. Finally, mutations in hub genes with greater connectedness in their regulatory networks had greater effects on both phenotypes and fitness. Together, these findings indicate that large-effect mutations may persist in populations because they influence traits that are adaptive only under specific environmental conditions. Understanding their evolutionary dynamics therefore requires measuring their effects in multiple natural environments.more » « less
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Abstract Increasing temperatures during climate change are known to alter the phenology across diverse plant taxa, but the evolutionary outcomes of these shifts are poorly understood. Moreover, plant temperature‐sensing pathways are known to interact with competition‐sensing pathways, yet there remains little experimental evidence for how genotypes varying in temperature responsiveness react to warming in realistic competitive settings.
We compared flowering time and fitness responses to warming and competition for two near‐isogenic lines (NILs) of
Arabidopsis thaliana transgressively segregating temperature‐sensitive and temperature‐insensitive alleles for major‐effect flowering time genes. We grew focal plants of each genotype in intraspecific and interspecific competition in four treatments contrasting daily temperature profiles in summer and fall under contemporary and warmed conditions. We measured phenology and fitness of focal plants to quantify plastic responses to season, temperature and competition and the dependence of these responses on flowering time genotype.The temperature‐insensitive NIL was constitutively early flowering and less fit, except in a future‐summer climate in which its fitness was higher than the later flowering, temperature‐sensitive NIL in low competition. The late‐flowering NIL showed accelerated flowering in response to intragenotypic competition and to increased temperature in the summer but delayed flowering in the fall. However, its fitness fell with rising temperatures in both seasons, and in the fall its marginal fitness gain from decreasing competition was diminished in the future.
Functional alleles at temperature‐responsive genes were necessary for plastic responses to season, warming and competition. However, the plastic genotype was not the most fit in every experimental condition, becoming less fit than the temperature‐canalized genotype in the warm summer treatment.
Climate change is often predicted to have deleterious effects on plant populations, and our results show how increased temperatures can act through genotype‐dependent phenology to decrease fitness. Furthermore, plasticity is not necessarily adaptive in rapidly changing environments since a nonplastic genotype proved fitter than a plastic genotype in a warming climate treatment.
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Summary The relevance of flowering time variation and plasticity to climate adaptation requires a comprehensive empirical assessment. We investigated natural selection and the genetic architecture of flowering time in Arabidopsis through field experiments in Europe across multiple sites and seasons.
We estimated selection for flowering time, plasticity and canalization. Loci associated with flowering time, plasticity and canalization by genome‐wide association studies were tested for a geographic signature of climate adaptation.
Selection favored early flowering and increased canalization, except at the northernmost site, but was rarely detected for plasticity. Genome‐wide association studies revealed significant associations with flowering traits and supported a substantial polygenic inheritance. Alleles associated with late flowering, including functional
FRIGIDA variants, were more common in regions experiencing high annual temperature variation. Flowering time plasticity to fall vs spring and summer environments was associated withGIGANTEA SUPPRESSOR 5 , which promotes early flowering under decreasing day length and temperature.The finding that late flowering genotypes and alleles are associated with climate is evidence for past adaptation. Real‐time phenotypic selection analysis, however, reveals pervasive contemporary selection for rapid flowering in agricultural settings across most of the species range. The response to this selection may involve genetic shifts in environmental cuing compared to the ancestral state.
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Premise The timing of germination has profound impacts on fitness, population dynamics, and species ranges. Many plants have evolved responses to seasonal environmental cues to time germination with favorable conditions; these responses interact with temporal variation in local climate to drive the seasonal climate niche and may reflect local adaptation. Here, we examined germination responses to temperature cues in
Streptanthus tortuosus populations across an elevational gradient.Methods Using common garden experiments, we evaluated differences among populations in response to cold stratification (chilling) and germination temperature and related them to observed germination phenology in the field. We then explored how these responses relate to past climate at each site and the implications of those patterns under future climate change.
Results Populations from high elevations had stronger stratification requirements for germination and narrower temperature ranges for germination without stratification. Differences in germination responses corresponded with elevation and variability in seasonal temperature and precipitation across populations. Further, they corresponded with germination phenology in the field; low‐elevation populations germinated in the fall without chilling, whereas high‐elevation populations germinated after winter chilling and snowmelt in spring and summer. Climate‐change forecasts indicate increasing temperatures and decreasing snowpack, which will likely alter germination cues and timing, particularly for high‐elevation populations.
Conclusions The seasonal germination niche for
S. tortuosus is highly influenced by temperature and varies across the elevational gradient. Climate change will likely affect germination timing, which may cascade to influence trait expression, fitness, and population persistence.
