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Quantifying species’ niches across a clade reveals how environmental tolerances evolve, and offers insights into present and future distributions. We use herbarium specimens to explore climate niche evolution across 14 annual species of theStreptanthus(s.l.) clade (Brassicaceae), which originated in deserts and diversified into cooler, moister areas. To understand how climate niches evolved, we used historical climate records to estimate each species’ 1) classic annual climate niche, averaged over specimen collection sites; 2) growing season niche, from estimated specimen germination date to collection date, averaged across specimens (specimen-specific niche); and 3) standardized seasonal niche based on average growing seasons of all species (clade-seasonal niche). In addition to estimating how phenological variation maps onto climate niche evolution, we explored how spatial refugia shape the climate experienced by species by 1) analyzing how field soil texture changes relative to the climate space that species occupy and 2) comparing soil water holding capacity from each specimen locality to that of surrounding areas. Specimen-specific niches exhibited less clade-wide variation in climatic water deficit (CWD) than did annual or clade-seasonal niches, and specimen-specific temperature niches showed no phylogenetic signal, in contrast to annual and clade-seasonal temperature niches. Species occupying cooler regions tracked hotter and drier climates by growing later into the summer, and by inhabiting refugia on drought-prone soils. These results underscore how phenological shifts, spatial refugia, and germination timing shape “lived” climate. Despite occupying a large range of annual climates, we found these species are constrained in the conditions under which they thrive. 

Summary Herbarium specimens are widely distributed in space and time, thereby capturing diverse conditions. We reconstructed specimen ‘lived’ climate from knowledge of germination cues and collection dates for 14 annual species in theStreptanthus(s.l.) clade (Brassicaceae) to ask: which climate attributes best explain specimen phenological stage and estimated reproduction? Are climate effects on phenology and reproduction evolutionarily conserved?We used climate data geolocated to collection sites to reconstruct the climate experienced by specimens and to ask which aspects of climate best explain specimen reproductive traits. We mapped slopes of climate relationships with these traits on the phylogeny to explore evolutionary constraint and models of evolution.Precipitation amount and onset, more than temperature, best predicted specimen phenology, but weakly predicted reproduction. Earlier rainfall was associated with more phenological advancement, a relationship that showed phylogenetic signal. Few climate predictors explained specimen reproduction. Phenological compensation, interactions with other species, or challenges in estimating total reproduction from specimens may reduce the signal between climate and reproduction.We highlight the value of specimen‐tailored growing season estimates for reconstructing climate, incorporating evolutionary relationships in assessing responses to climate. We propose supplemental collection protocols to increase the utility of specimens for understanding climate impacts. 

Abstract 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 theStreptanthus/Caulanthusclade (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 threeCaulanthusspecies. Species' germination responses to the timing of rainfall and seasonal temperatures were phylogenetically constrained, withCaulanthusspecies 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. 

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 speciesArabidopsis 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 geneDOG1and 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‐dormancyDOG1allele 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 floweringFRIallele 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‐dormancyDOG1allele 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. Read the freePlain Language Summaryfor this article on the Journal blog. 

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. 

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. 

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) ofArabidopsis thalianatransgressively 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. Aplain language summaryis available for this article. 

PremiseThe 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 inStreptanthus tortuosuspopulations across an elevational gradient. MethodsUsing 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. ResultsPopulations 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. ConclusionsThe seasonal germination niche forS. tortuosusis 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.