Identifying predictors of translocation success in rare plant species.

The fundamental goal of a rare plant translocation is to create self-sustaining populations with the evolutionary resilience to persist in the long term. Yet, most plant translocation syntheses focus on a few factors influencing short-term benchmarks of success (e.g., survival and reproduction). Short-term benchmarks can be misleading when trying to infer future growth and viability because the factors that promote establishment may differ from those required for long-term persistence. We assembled a large (n = 275) and broadly representative data set of well-documented and monitored (7.9 years on average) at-risk plant translocations to identify the most important site attributes, management techniques, and species' traits for six life-cycle benchmarks and population metrics of translocation success. We used the random forest algorithm to quantify the relative importance of 29 predictor variables for each metric of success. Drivers of translocation outcomes varied across time frames and success metrics. Management techniques had the greatest relative influence on the attainment of life-cycle benchmarks and short-term population trends, whereas site attributes and species' traits were more important for population persistence and long-term trends. Specifically, large founder sizes increased the potential for reproduction and recruitment into the next generation, whereas declining habitat quality and the outplanting of species with low seed production led to increased extinction risks and a reduction in potential reproductive output in the long-term, respectively. We also detected novel interactions between some of the most important drivers, such as an increased probability of next-generation recruitment in species with greater seed production rates, but only when coupled with large founder sizes. Because most significant barriers to plant translocation success can be overcome by improving techniques or resolving site-level issues through early intervention and management, we suggest that by combining long-term monitoring with adaptive management, translocation programs can enhance the prospects of achieving long-term success.

Identificación de pronosticadores del éxito de reubicación en especies raras de plantas Resumen El objetivo fundamental de la reubicación de plantas raras es la creación de poblaciones autosuficientes con resiliencia evolutiva que persistan a la larga. De todas maneras, la mayoría de las síntesis de estas reubicaciones se enfocan en unos cuantos factores que influyen sobre los parámetros a corto plazo del éxito (supervivencia y reproducción). Los parámetros a corto plazo pueden ser engañosos si se intenta inferir el crecimiento y la viabilidad en el futuro ya que los factores que promueven el establecimiento pueden diferir de aquellos requeridos para la persistencia a largo plazo. Ensamblamos un conjunto grande de datos representativos en general (n = 275) de las reubicaciones de plantas en riesgo bien documentadas y monitoreadas (7.9 años en promedio) para identificar los atributos de sitio más importantes, las técnicas de manejo y los rasgos de las especies para seis parámetros de ciclos de vida y medidas poblacionales del éxito de reubicación. Usamos el algoritmo de bosque aleatorio para cuantificar la importancia relativa de las 29 variables de pronosticadores para cada medida del éxito. Los factores en los resultados de las reubicaciones variaron con los marcos temporales y las medidas de éxito. Las técnicas de manejo tuvieron la mayor influencia relativa sobre la obtención de parámetros de ciclos de vida y tendencias poblacionales a corto plazo, mientras que los atributos de sitio y los rasgos de la especie fueron más importantes para la persistencia poblacional y las tendencias a largo plazo. En específico, las grandes cantidades de fundadores incrementaron el potencial de reproducción y reclutamiento de la siguiente generación, mientras que la declinación de la calidad del hábitat incrementó el riesgo de extinción y el trasplante de especies con baja producción de semillas redujo el rendimiento del potencial reproductivo a la larga. También detectamos interacciones novedosas entre algunos de los factores más importantes, como el aumento en la probabilidad del reclutamiento en la siguiente generación en especies con tasas mayores de producción de semillas, pero sólo cuando se emparejó con grandes cantidades de fundadores. Ya que las barreras más significativas para el éxito de la reubicación de plantas pueden superarse al mejorar las técnicas o resolver los temas a nivel de sitio por medio de un manejo y una intervención temprana, sugerimos que con la combinación del monitoreo a largo plazo con el manejo adaptativo los programas de reubicación pueden aumentar el prospecto de lograr el éxito a largo plazo.

Adaptation across geographic ranges is consistent with strong selection in marginal climates and legacies of range expansion.

Every species experiences limits to its geographic distribution. Some evolutionary models predict that populations at range edges are less well adapted to their local environments due to drift, expansion load, or swamping gene flow from the range interior. Alternatively, populations near range edges might be uniquely adapted to marginal environments. In this study, we use a database of transplant studies that quantify performance at broad geographic scales to test how local adaptation, site quality, and population quality change from spatial and climatic range centers toward edges. We find that populations from poleward edges perform relatively poorly, both on average across all sites (15% lower population quality) and when compared to other populations at home (31% relative fitness disadvantage), consistent with these populations harboring high genetic load. Populations from equatorial edges also perform poorly on average (18% lower population quality) but, in contrast, outperform foreign populations (16% relative fitness advantage), suggesting that populations from equatorial edges have strongly adapted to unique environments. Finally, we find that populations from sites that are thermally extreme relative to the species' niche demonstrate strong local adaptation, regardless of their geographic position. Our findings indicate that both nonadaptive processes and adaptive evolution contribute to variation in adaptation across species' ranges.

Local Adaptation to Biotic Interactions: A Meta-analysis across Latitudes.

Adaptation to local conditions can increase species' geographic distributions and rates of diversification, but which components of the environment commonly drive local adaptation-particularly the importance of biotic interactions-is unclear. Biotic interactions should drive local adaptation when they impose consistent divergent selection; if this is common, we expect transplant experiments to detect more frequent and stronger local adaptation when biotic interactions are left intact. We tested this hypothesis using a meta-analysis of transplant experiments from >125 studies (mostly of plants). Overall, local adaptation was common, and biotic interactions affected fitness. Nevertheless, local adaptation was neither more common nor stronger when biotic interactions were left intact, either between experimental treatments within studies (control vs. biotic interactions experimentally manipulated) or between studies that used natural versus biotically altered transplant environments. However, the effect of ameliorating negative interactions varied with latitude, suggesting that interactions may promote local adaptation more often in tropical than in temperate ecosystems, although few tropical studies were available to test this. Our results suggest that biotic interactions often fail to drive local adaptation even though they strongly affect fitness, perhaps because temperate biotic environments are unpredictable at the spatiotemporal scales required for local adaptation.

Variation in the seasonal germination niche across an elevational gradient: the role of germination cueing in current and future climates.

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.

Geographic variation in reproductive assurance of Clarkia pulchella.

Climate can affect plant populations through direct effects on physiology and fitness, and through indirect effects on their relationships with pollinating mutualists. We therefore expect that geographic variation in climate might lead to variation in plant mating systems. Biogeographic processes, such as range expansion, can also contribute to geographic patterns in mating system traits. We manipulated pollinator access to plants in eight sites spanning the geographic range of Clarkia pulchella to investigate geographic and climatic drivers of fruit production and seed set in the absence of pollinators (reproductive assurance). We examined how reproductive assurance and fruit production varied with the position of sites within the range of the species and with temperature and precipitation. We found that reproductive assurance in C. pulchella was greatest in populations in the northern part of the species' range and was not well explained by any of the climate variables that we considered. In the absence of pollinators, some populations of C. pulchella have the capacity to increase fruit production, perhaps through resource reallocation, but this response is climate dependent. Pollinators are important for reproduction in this species, and recruitment is sensitive to seed input. The degree of autonomous self-pollination that is possible in populations of this mixed-mating species may be shaped by historic biogeographic processes or variation in plant and pollinator community composition rather than variation in climate.

Gene flow improves fitness at a range edge under climate change.

Populations at the margins of a species' geographic range are often thought to be poorly adapted to their environment. According to theoretical predictions, gene flow can inhibit these range edge populations if it disrupts adaptation to local conditions. Alternatively, if range edge populations are small or isolated, gene flow can provide beneficial genetic variation and may facilitate adaptation to environmental change. We tested these competing predictions in the annual wildflower Clarkia pulchella using greenhouse crosses to simulate gene flow from sources across the geographic range into two populations at the northern range margin. We planted these between-population hybrids in common gardens at the range edge and evaluated how genetic differentiation and climatic differences between edge populations and gene flow sources affected lifetime fitness. During an anomalously warm study year, gene flow from populations occupying historically warm sites improved fitness at the range edge and plants with one or both parents from warm populations performed best. The effects of the temperature provenance of gene flow sources were most apparent at early life history stages, but precipitation provenance also affected reproduction. We also found benefits of gene flow that were independent of climate: after climate was controlled for, plants with parents from different populations performed better at later lifestages than those with parents from the same population, indicating that gene flow may improve fitness via relieving homozygosity. Further supporting this result, we found that increasing genetic differentiation of parental populations had positive effects on fitness of hybrid seeds. Gene flow from warmer populations, when it occurs, is likely to contribute adaptive genetic variation to populations at the northern range edge as the climate warms. On heterogeneous landscapes, climate of origin may be a better predictor of gene flow effects than geographic proximity.

A synthesis of transplant experiments and ecological niche models suggests that range limits are often niche limits.

Global change has made it important to understand the factors that shape species' distributions. Central to this area of research is the question of whether species' range limits primarily reflect the distribution of suitable habitat (i.e. niche limits) or arise as a result of dispersal limitation. Over-the-edge transplant experiments and ecological niche models are commonly used to address this question, yet few studies have taken advantage of a combined approach for inferring the causes of range limits. Here, we synthesise results from existing transplant experiments with new information on the predicted suitability of sites based on niche models. We found that individual performance and habitat suitability independently decline beyond range limits across multiple species. Furthermore, inferences from transplant experiments and niche models were generally concordant within species, with 31 out of 40 cases fully supporting the hypothesis that range limits are niche limits. These results suggest that range limits are often niche limits and that the factors constraining species' ranges operate at scales detectable by both transplant experiments and niche models. In light of these findings, we outline an integrative framework for addressing the causes of range limits in individual species.

Effects of range-wide variation in climate and isolation on floral traits and reproductive output of Clarkia pulchella.

PREMISE OF THE STUDY: Plant mating systems and geographic range limits are conceptually linked by shared underlying drivers, including landscape-level heterogeneity in climate and in species' abundance. Studies of how geography and climate interact to affect plant traits that influence mating system and population dynamics can lend insight to ecological and evolutionary processes shaping ranges. Here, we examined how spatiotemporal variation in climate affects reproductive output of a mixed-mating annual, Clarkia pulchella. We also tested the effects of population isolation and climate on mating-system-related floral traits across the range. METHODS: We measured reproductive output and floral traits on herbarium specimens collected across the range of C. pulchella. We extracted climate data associated with specimens and derived a population isolation metric from a species distribution model. We then examined how predictors of reproductive output and floral traits vary among populations of increasing distance from the range center. Finally, we tested whether reproductive output and floral traits vary with increasing distance from the center of the range. KEY RESULTS: Reproductive output decreased as summer precipitation decreased, and low precipitation may contribute to limiting the southern and western range edges of C. pulchella. High spring and summer temperatures are correlated with low herkogamy, but these climatic factors show contrasting spatial patterns in different quadrants of the range. CONCLUSIONS: Limiting factors differ among different parts of the range. Due to the partial decoupling of geography and environment, examining relationships between climate, reproductive output, and mating-system-related floral traits reveals spatial patterns that might be missed when focusing solely on geographic position.

Phylogenetic structure and host abundance drive disease pressure in communities.

Pathogens play an important part in shaping the structure and dynamics of natural communities, because species are not affected by them equally. A shared goal of ecology and epidemiology is to predict when a species is most vulnerable to disease. A leading hypothesis asserts that the impact of disease should increase with host abundance, producing a 'rare-species advantage'. However, the impact of a pathogen may be decoupled from host abundance, because most pathogens infect more than one species, leading to pathogen spillover onto closely related species. Here we show that the phylogenetic and ecological structure of the surrounding community can be important predictors of disease pressure. We found that the amount of tissue lost to disease increased with the relative abundance of a species across a grassland plant community, and that this rare-species advantage had an additional phylogenetic component: disease pressure was stronger on species with many close relatives. We used a global model of pathogen sharing as a function of relatedness between hosts, which provided a robust predictor of relative disease pressure at the local scale. In our grassland, the total amount of disease was most accurately explained not by the abundance of the focal host alone, but by the abundance of all species in the community weighted by their phylogenetic distance to the host. Furthermore, the model strongly predicted observed disease pressure for 44 novel host species we introduced experimentally to our study site, providing evidence for a mechanism to explain why phylogenetically rare species are more likely to become invasive when introduced. Our results demonstrate how the phylogenetic and ecological structure of communities can have a key role in disease dynamics, with implications for the maintenance of biodiversity, biotic resistance against introduced weeds, and the success of managed plants in agriculture and forestry.