This content will become publicly available on May 26, 2027

Title: Climate mediates phenological and phylogenetic differentiation in plant invasions
Darwin’s Naturalization Conundrum holds that both functional similarity and distinctiveness can facilitate biological invasions: invaders similar to natives may succeed through preadaptation to local abiotic conditions, whereas functionally distinct invaders may succeed by reducing competition. Yet the contexts in which either mechanism dominates are unclear. Prior research has primarily attributed variability in native–invasive differentiation to shifts in the balance between biotic and climatic barriers to invasion from local to regional scales. However, similarity and distinctiveness are frequent at both local and regional levels, indicating key drivers of native–invasive differentiation remain overlooked. Crucially, theory and evidence show that as climatic stress increases, competition weakens. This implies that harsh climates should favor invaders functionally similar to natives, whereas mesic climates should favor distinctiveness. However, this hypothesis has not been tested across climate regimes and functional traits. We addressed this gap by combining models of species distributions and flowering phenology for 2,810 species across the United States, estimating phylogenetic distance and phenological differentiation between natives and invasives relative to differentiation among co-occurring natives. In warm, humid regions, invasives flowered earlier, less synchronously, and were more distantly related to natives. In cold or dry regions, they flowered at similar or later times, more synchronously, and were more closely related than natives themselves. Across all climates, invasives consistently exhibited longer flowering durations, with little evidence of greater phenological plasticity. These findings reveal that Darwin’s Conundrum reflects a predictable continuum shaped by environmental context, highlighting climate as a key axis of invasion success.  more » « less
Award ID(s):
2242804 2105903 2101884
PAR ID:
10688021
Author(s) / Creator(s):
; ; ; ; ; ; ;
Publisher / Repository:
National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
123
Issue:
21
ISSN:
0027-8424
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Although many species shift their phenology with climate change, species vary significantly in the direction and magnitude of these responses (i.e., phenological sensitivity). Studies increasingly detect early phenology or high phenological sensitivity to climate in non-native species, which may favor non-native species over natives in warming climates. Yet relatively few studies explicitly compare phenological responses to climate between native vs. non-native species or between non-native populations in the native vs. introduced range, limiting our ability to quantify the role of phenology in invasion success. Here, we review the empirical evidence for and against differences in phenology and phenological sensitivity to climate in both native vs. non-native species and native and introduced populations of non-native species. Contrary to common assumptions, native and non-native plant species did not consistently differ in mean phenology or phenological sensitivity. However, non-native plant species were often either just as or more sensitive, but rarely less sensitive, to climate as natives. Introduced populations of non-native plant species often show earlier reproduction than native populations of the same species, but there was mixed evidence for differences in phenological sensitivity between introduced and native plant populations. We found very few studies comparing native vs. invasive animal phenology. Future work should characterize phenological sensitivity to climate in native vs. non-native plant and animal species, in native vs. introduced populations of non-native species, and across different stages of invasion, and should carefully consider how differences in phenology might promote invasion success or disadvantage native species under climate change. 
    more » « less
  2. Biological invasions are profoundly altering Earth’s ecosystems, but generalities about the effects of nonnative species on the diversity and productivity of native communities have been elusive. This lack of generality may reflect the limited spatial and temporal extents of most previous studies. Using >5 million tree measurements across eastern US forests from 1995 to 2023, we quantified temporal trends in tree diversity and biomass. We then analyzed community-level changes in native tree diversity and biomass in relation to nonnative tree invasion and native species colonization. Across the entire eastern United States, native tree species richness decreased over time in plots where nonnatives occurred, whereas nonnative species richness and the biomass of both natives and nonnatives increased over time. At the community scale, native richness tended to decline following nonnative invasion, whereas native biomass and richness-independent measures of trait and phylogenetic diversity tended to remain stable. These patterns can be explained by the rarity of the displaced native species and their functional and phylogenetic similarity to native species that survived nonnative invasions. In contrast, native survivors tended to be functionally distinct from nonnative invaders, suggesting an important role for niche partitioning in community dynamics. Colonization by previously absent native species was associated with an increase in native richness (beyond the addition of native colonizers), which contrasts with declines in native richness that tended to follow nonnative invasion. These results suggest a causal role for nonnative species in the native richness decline of invaded communities. 
    more » « less
  3. Abstract Darwin's theory of natural selection provides two seemingly contradictory hypotheses for explaining the success of biological invasions: (1) the pre‐adaptation hypothesis posits that introduced species that are closely related to native species will be more likely to succeed due to shared advantageous characteristics; (2) the limiting similarity hypothesis posits that invaders that are more similar to resident species will be less likely to succeed due to competitive exclusion. Previous studies assessing this conundrum show mixed results, possibly stemming from inconsistent study spatial scales and failure to integrate both functional and phylogenetic information. Here, we address these limitations using a 33‐year grassland successional survey at Cedar Creek Ecosystem Science Reserve (USA). We incorporate functional dissimilarities, phylogenetic distances, environmental covariates, and species origin data for 303 vascular plant taxa (256 native, 47 introduced), collected from 2700 plots. In contrast with other studies, we test both hypotheses at two fine spatial scales—neighborhood (0.5 m2) and site (~40 m2)—to better capture competition and environmental filtering, respectively. Findings related to Darwin's naturalization conundrum depended on spatial scale and dissimilarity metric. Our results agreed with the pre‐adaptation hypothesis at site scale (40 m2)—a much finer resolution than typically used to test the pre‐adaptation hypothesis—highlighting the role of environmental filtering. At the neighborhood scale (0.5 m2), support for the limiting similarity hypothesis emerged when using functional dissimilarity, while phylogenetic distance aligned with the pre‐adaptation hypothesis, demonstrating that different dissimilarity metrics can yield contrasting conclusions. In addition, native and introduced species showed different abundance patterns in relation to functional ranked dissimilarities, with introduced species reaching higher cover when they were taller than co‐occurring species, had higher leaf dry matter content (LDMC) and lower seed mass. Introduced species also reached high cover with higher soil N concentrations and a shorter time after colonization, relative to native species. Our results suggest that inconsistent findings related to Darwin's naturalization conundrum may arise from an overreliance on single dissimilarity metrics and the use of spatial scales failing to capture underlying ecological processes. This highlights the need for more nuanced methodologies when testing the pre‐adaptation and limiting similarity hypotheses. 
    more » « less
  4. Abstract The disruptive effects of tertiary species on otherwise positive pairwise species interactions (e.g. context-dependent parasitism in pollinator syndromes) is well-known. However, few—if any—studies have investigated how invasive plants affect interactions between facilitative plants and their native plant communities. Further, if tertiary invasive species can change interactions among native species from positive to negative, then a tertiary native should be capable of the same phenom for pairwise interactions between natives and invasives. Our previous research indicates invasive black mustard ( Brassica nigra ) changes interaction signs for otherwise positive species interactions between the dominant, native facilitator California buckwheat ( Eriogonum fasciculatum ) and its co-dominant beneficiary California sagebrush ( Artemisia californica ) in semi-arid California coastal sage scrub habitat. Here, E. fasciculatum and A. californica seedlings increased B. nigra shoot growth in pairwise species interactions in the greenhouse. However, in three-way species interactions, E. fasciculatum and A. californica together reduced B. nigra SLA, height, and reproductive potential while not increasing shoot DW. In three-way species interactions, B. nigra did not significantly reduce E. fasciculatum facilitation of A. californica . Also surprisingly, light competition with B. nigra resulted in an increase in A. californica height , which reduced the negative effects of A. californica light competition on shade-intolerant E. fasciculatum. In an additive field experiment, A. californica protected E. fasciculatum from facilitating germination and growth of B. nigra when water competition was minimized. Taken together, this study demonstrates the importance of studying species interactions between competitive, native perennials in the current ecological context of invaded ecosystems. 
    more » « less
  5. Abstract Plants respond to their environment with both short‐term, within‐generation trait plasticity, and long‐term, between‐generation evolutionary changes. However, the relative magnitude of plant responses to short‐ and long‐term changes in the environment remains poorly understood. Shifts in phenological traits can serve as harbingers for responses to environmental change, and both a plant's current and source (i.e., genotype origin) environment can affect plant phenology via plasticity and local adaptation, respectively. To assess the role of current and source environments in explaining variation in flowering phenology ofBromus tectorum, an invasive annual grass, we conducted a replicated common garden experiment using 92 genotypes collected across western North America. Replicates of each genotype were planted in two densities (low = 100 seeds/1 m2, high = 100 seeds/0.04 m2) under two different temperature treatments (low = white gravel; high = black gravel; 2.1°C average difference) in a factorial design, replicated across four common garden locations in Idaho and Wyoming, USA. We tested for the effect of current environment (i.e., density treatment, temperature treatment, and common garden location), source environment (i.e., genotype source climate), and their interaction on each plant's flowering phenology. Flowering timing was strongly influenced by a plant's current environment, with plants that experienced warmer current climates and higher densities flowering earlier than those that experienced cooler current climates and lower densities. Genotypes from hot and dry source climates flowered consistently earlier than those from cool and wet source climates, even after accounting for genotype relatedness, suggesting that this genetically based climate cline is a product of natural selection. We found minimal evidence of interactions between current and source environments or genotype‐by‐environment interactions. Phenology was more sensitive to variation in the current climate than to variation in source climate. These results indicate that cheatgrass phenology reflects high levels of plasticity as well as rapid local adaptation. Both processes likely contribute to its current success as a biological invader and its capacity to respond to future environmental change. 
    more » « less