A Long-Lived Alpine Perennial Advances Flowering under Warmer Conditions but Not Enough to Maintain Reproductive Success.

AbstractAssessing whether phenological shifts in response to climate change confer a fitness advantage requires investigating the relationships among phenology, fitness, and environmental drivers of selection. Despite widely documented advancements in phenology with warming climate, we lack empirical estimates of how selection on phenology varies in response to continuous climate drivers or how phenological shifts in response to warming conditions affect fitness. We leverage an unusual long-term dataset with repeated, individual measurements of phenology and reproduction in a long-lived alpine plant. We analyze phenotypic plasticity in flowering phenology in relation to two climate drivers, snowmelt timing and growing degree days (GDDs). Plants flower earlier with increased GDDs and earlier snowmelt, and directional selection also favors earlier flowering under these conditions. However, reproduction still declines with warming and early snowmelt, even when flowering is early. Furthermore, the steepness of this reproductive decline increases dramatically with warming conditions, resulting in very little fruit production regardless of flowering time once GDDs exceed approximately 225 degree days or snowmelt occurs before May 15. Even though advancing phenology confers a fitness advantage relative to stasis, these shifts are insufficient to maintain reproduction under warming, highlighting limits to the potential benefits of phenological plasticity under climate change.

Local adaptation: Causal agents of selection and adaptive trait divergence.

Divergent selection across the landscape can favor the evolution of local adaptation in populations experiencing contrasting conditions. Local adaptation is widely observed in a diversity of taxa, yet we have a surprisingly limited understanding of the mechanisms that give rise to it. For instance, few have experimentally confirmed the biotic and abiotic variables that promote local adaptation, and fewer yet have identified the phenotypic targets of selection that mediate local adaptation. Here, we highlight critical gaps in our understanding of the process of local adaptation and discuss insights emerging from in-depth investigations of the agents of selection that drive local adaptation, the phenotypes they target, and the genetic basis of these phenotypes. We review historical and contemporary methods for assessing local adaptation, explore whether local adaptation manifests differently across life history, and evaluate constraints on local adaptation.

Estimating phenological sensitivity in contemporary vs. historical data sets: Effects of climate resolution and spatial scale.

PREMISE: Phenological sensitivity, or the degree to which a species' phenology shifts in response to warming, is an important parameter for comparing and predicting species' responses to climate change. Phenological sensitivity is often measured using herbarium specimens or local studies in natural populations. These approaches differ widely in spatiotemporal scales, yet few studies explicitly consider effects of the geographic extent and resolution of climate data when comparing phenological sensitivities quantified from different data sets for a given species. METHODS: We compared sensitivity of flowering phenology to growing degree days of the alpine plant Silene acaulis using two data sets: herbarium specimens and a 6 yr observational study in four populations at Niwot Ridge, Colorado, USA. We investigated differences in phenological sensitivity obtained using variable spatial scales and climate data sources. RESULTS: Herbarium specimens underestimated phenological sensitivity compared to observational data, even when herbarium samples were limited geographically or to nearby weather station data. However, when observational data were paired with broader-scale climate data, as is typically used in herbarium data sets, estimates of phenological sensitivity were more similar. CONCLUSIONS: This study highlights the potential for variation in data source, geographic scale, and accuracy of macroclimate data to produce very different estimates of phenological responses to climate change. Accurately predicting phenological shifts would benefit from comparisons between methods that estimate climate variables and phenological sensitivity over a variety of spatial scales.

The 'black box' of plant demography: how do seed type, climate and seed fungal communities affect grass seed germination?

Demographic studies measure drivers of plant fecundity including seed production and survival, but few address both abiotic and biotic drivers of germination such as variation in climate among sites, population density, maternal plants, seed type and fungal pathogen abundance. We examined germination and microbial communities of seeds of Danthonia californica, which are either chasmogamous (external, wind-pollinated) or cleistogamous (internal, self-fertilized) and Festuca roemeri, which are solely chasmogamous. Seed populations were sourced across environmental gradients. We tested germination and used high-throughput sequencing to characterize seed fungal community structure. For F. roemeri, maternal plants significantly influenced germination as did climate and pathogens; germination increased from wetter, cooler sites. For D. californica, the main drivers of germination were maternal plant, seed type and pathogens; on average, more chasmogamous seeds germinated. Fungal communities depended largely on seed type, with fewer fungi associated with cleistogamous seeds, but the communities also depended on site factors such as vapor pressure deficit, plant density and whether the seeds had germinated. Putative pathogens that were negatively correlated with germination were more abundant for both D. californica and F. roemeri chasmogamous seeds than D. californica cleistogamous seeds. In D. californica, cleistogamous and chasmogamous seeds contain vastly different fungal communities.

Latitudinal gradients in population growth do not reflect demographic responses to climate.

Spatial gradients in population growth, such as across latitudinal or elevational gradients, are often assumed to primarily be driven by variation in climate, and are frequently used to infer species' responses to climate change. Here, we use a novel demographic, mixed-model approach to dissect the contributions of climate variables vs. other latitudinal or local site effects on spatiotemporal variation in population performance in three perennial bunchgrasses. For all three species, we find that performance of local populations decreases with warmer and drier conditions, despite latitudinal trends of decreasing population growth toward the cooler and wetter northern portion of each species' range. Thus, latitudinal gradients in performance are not predictive of either local or species-wide responses to climate. This pattern could be common, as many environmental drivers, such as habitat quality or species' interactions, are likely to vary with latitude or elevation, and thus influence or oppose climate responses.

Portfolio effects, climate change, and the persistence of small populations: analyses on the rare plant Saussurea weberi.

The mechanisms that stabilize small populations in the face of environmental variation are crucial to their long-term persistence. Building from diversity-stability concepts in community ecology, within-population diversity is gaining attention as an important component of population stability. Genetic and microhabitat variation within populations can generate diverse responses to common environmental fluctuations, dampening temporal variability across the population as a whole through portfolio effects. Yet, the potential for portfolio effects to operate at small scales within populations or to change with systematic environmental shifts, such as climate change, remain largely unexplored. We tracked the abundance of a rare alpine perennial plant, Saussurea weberi, in 49 1-m2 plots within a single population over 20 yr. We estimated among-plot correlations in log annual growth rate to test for population-level synchrony and quantify portfolio effects across the 20-yr study period and also in 5-yr subsets based on June temperature quartiles. Asynchrony among plots, due to different plot-level responses to June temperature, reduced overall fluctuations in abundance and the probability of decline in population models, even when accounting for the effects of density dependence on dynamics. However, plots became more synchronous and portfolio effects decreased during the warmest years of the study, suggesting that future climate warming may erode stabilizing mechanisms in populations of this rare plant.

The scale of local adaptation in Mimulus guttatus: comparing life history races, ecotypes, and populations.

Fitness trade-offs between environments are central to the evolution of biodiversity. Although transplant studies often document fitness trade-offs consistent with local adaptation (LA), many have also found an advantage of foreign genotypes (foreign advantage (FA)). Understanding the mechanisms driving the magnitude and distribution of fitness variation requires comparative approaches that test the ecological scales at which these different patterns emerge. We used a common garden transplant experiment to compare the relative fitnesses of native vs foreign genotypes at three nested ecological scales within Mimulus guttatus: annual vs perennial life history races, perennial ecotypes across an elevational range, and populations within perennial elevational ecotypes. We integrated fitness across the life-cycle and decomposed LA vs FA into contributions from different fitness components. We found LA, measured as home-site advantage, between annual and perennial races and a trend towards LA among populations within montane habitats. Conversely, we found strong FA of low-elevation perennials in a montane environment. LA between life history races reflects the fitness advantages of adult survival and vegetative growth in a mesic environment. Within the perennial race, recent climate conditions or nonselective processes, such as dispersal limitation or mutational load, could explain FA of low-elevation perennials in a montane environment.

Seed type and origin-dependent seedling emergence patterns in Danthonia californica, a species commonly used in grassland restoration.

Danthonia californica Bolander (Poaceae)is a native perennial bunchgrass commonly used in the restoration of prairie ecosystems in the western United States. Plants of this species simultaneously produce both chasmogamous (potentially outcrossed) and cleistogamous (obligately self-fertilized) seeds. Restoration practitioners almost exclusively use chasmogamous seeds for outplanting, which are predicted to perform better in novel environments due to their greater genetic diversity. Meanwhile, cleistogamous seeds may exhibit greater local adaptation to the conditions in which the maternal plant exists. We performed a common garden experiment at two sites in the Willamette Valley, Oregon, to assess the influence of seed type and source population (eight populations from a latitudinal gradient) on seedling emergence and found no evidence of local adaptation for either seed type. Cleistogamous seeds outperformed chasmogamous seeds, regardless of whether seeds were sourced directly from the common gardens (local seeds) or other populations (nonlocal seeds). Furthermore, average seed weight had a strong positive effect on seedling emergence, despite the fact that chasmogamous seeds had significantly greater mass than cleistogamous seeds. At one common garden, we observed that seeds of both types sourced from north of our planting site performed significantly better than local or southern-sourced seeds. We also found a significant seed type and distance-dependent interaction, with cleistogamous seedling emergence peaking approximately 125 km from the garden. These results suggest that cleistogamous seeds should be considered for greater use in D. californica restoration.

Dissecting impacts of phenological shifts for performance across biological scales.

Although phenological shifts in response to climate are often assumed to benefit species' performance and viability, phenology's role in allowing population persistence and mediating species-level responses in the face of climate change remain unclear. Here, we develop a framework to understand when and why phenological shifts at three biological scales will influence performance: individuals, populations, and macroecological patterns. Specifically, we highlight three underexplored assumptions: (i) individual variability in phenology does not affect population fitness; (ii) population growth rates are sensitive to vital rates affected by phenology; and (iii) phenology mediates species-level responses to climate change including patterns of extinction, invasion, and range shifts. We outline promising methods for understanding how phenological shifts will influence performance within and across biological scales.

Climate sensitivity across latitude: scaling physiology to communities.

While we know climate change will impact individuals, populations, and communities, we lack a cross-scale synthesis for understanding global variation in climate change impacts and predicting their ecological effects. Studies of latitudinal variation in individuals' thermal responses have developed primarily in isolation from studies of natural populations' warming responses. Further, it is unclear whether latitudinal variation in temperature-dependent population responses will manifest into latitudinal patterns in community stability. Integrating across scales, we discuss the key drivers of latitudinal variation in climate change effects, with the goal of identifying key pieces of information necessary to predict warming effects in natural communities. We propose two experimental approaches synthesizing latitudinal variability in climate change impacts across scales of biological organization.

Climate warming threatens the persistence of a community of disturbance-adapted native annual plants.

With ongoing climate change, populations are expected to exhibit shifts in demographic performance that will alter where a species can persist. This presents unique challenges for managing plant populations and may require ongoing interventions, including in situ management or introduction into new locations. However, few studies have examined how climate change may affect plant demographic performance for a suite of species, or how effective management actions could be in mitigating climate change effects. Over the course of two experiments spanning 6 yr and four sites across a latitudinal gradient in the Pacific Northwest, United States, we manipulated temperature, precipitation, and disturbance intensity, and quantified effects on the demography of eight native annual prairie species. Each year we planted seeds and monitored germination, survival, and reproduction. We found that disturbance strongly influenced demographic performance and that seven of the eight species had increasingly poor performance with warmer conditions. Across species and sites, we observed 11% recruitment (the proportion of seeds planted that survived to reproduction) following high disturbance, but just 3.9% and 2.3% under intermediate and low disturbance, respectively. Moreover, mean seed production following high disturbance was often more than tenfold greater than under intermediate and low disturbance. Importantly, most species exhibited precipitous declines in their population growth rates (λ) under warmer-than-ambient experimental conditions and may require more frequent disturbance intervention to sustain populations. Aristida oligantha, a C4 grass, was the only species to have λ increase with warmer conditions. These results suggest that rising temperatures may cause many native annual plant species to decline, highlighting the urgency for adaptive management practices that facilitate their restoration or introduction to newly suitable locations. Frequent and intense disturbances are critical to reduce competitors and promote native annuals' persistence, but even such efforts may prove futile under future climate regimes.

Asynchrony in individual and subpopulation fecundity stabilizes reproductive output of an alpine plant population.

Population-wide outcomes such as abundance, reproductive output, or mean survival can be stabilized by non-synchronous variation in the performance of individuals or subpopulations. Such "portfolio effects" have been increasingly documented at the scale of subpopulations and are thought to play an important role in generating stability of population phenomena in the face of environmental variation. However, few studies quantify the strength and origin of portfolio effects at the finer scale of individuals. We used 16 yr of fruit production and climate data for an alpine plant to dissect the scale of portfolio effects in reproduction, as well as the contribution of individual traits including size and flowering time in driving reproductive output. Asynchrony in reproductive success substantially reduces variation in population-level reproductive output, with approximately one-fourth of this stabilizing effect arising from individual differences, mostly not those characterized by measured traits, and approximately three-fourths from asynchrony across subpopulations. These results emphasize the different scales and causes of portfolio effects. The decomposition for portfolio effects we provide can facilitate similar breakdowns of the strength and causes of these effects in other systems.