Population climatic history predicts phenotypic responses in novel environments for Arabidopsis thaliana in North America.

PREMISE: Determining how species perform in novel climatic environments is essential for understanding (1) responses to climate change and (2) evolutionary consequences of biological invasions. For the vast majority of species, the number of population characteristics that will predict performance and patterns of natural selection in novel locations in the wild remains limited. METHODS: We evaluated phenological, vegetative, architectural, and fitness-related traits in experimental gardens in contrasting climates (Ontario, Canada, and South Carolina, USA) in the North American non-native distribution of Arabidopsis thaliana. We assessed the effects of climatic distance, geographic distance, and genetic features of history on performance and patterns of natural selection in the novel garden settings. RESULTS: We found that plants had greater survivorship, flowered earlier, were larger, and produced more fruit in the south, and that genotype-by-environment interactions were significant between gardens. However, our analyses revealed similar patterns of natural selection between gardens in distinct climate zones. After accounting for genetic ancestry, we also detected that population climatic distance best predicted performance within gardens. CONCLUSIONS: These data suggest that colonization success in novel, non-native environments is determined by a combination of climate and genetic history. When performance at novel sites was assessed with seed sources from geographically and genetically disparate, established non-native populations, proximity to the garden alone was insufficient to predict performance. Our study highlights the need to evaluate seed sources from diverse origins to describe comprehensively phenotypic responses to novel environments, particularly for taxa in which many source populations may contribute to colonization.

Strong genetic differentiation but not local adaptation toward the range limit of a coastal dune plant.

All species have limited geographic distributions; but the ecological and evolutionary mechanisms causing range limits are largely unknown. That many species' geographic range limits are coincident with niche limits suggests limited evolutionary potential of marginal populations to adapt to conditions experienced beyond the range. We provide a test of range limit theory by combining population genetic analysis of microsatellite polymorphisms with a transplant experiment within, at the edge of, and 60 km beyond the northern range of a coastal dune plant. Contrary to expectations, lifetime fitness increased toward the range limit with highest fitness achieved by most populations at and beyond the range edge. Genetic differentiation among populations was strong, with very low, nondirectional gene flow suggesting range limitation via constraints to dispersal. In contrast, however, local adaptation was negligible, and a distance-dependent decline in fitness only occurred for those populations furthest from home when planted beyond the range limit. These results challenge a commonly held assumption that stable range limits match niche limits, but also raise questions about the unique value of peripheral populations in expanding species' geographical ranges.

Microsatellite primers for Camissoniopsis cheiranthifolia (Onagraceae) and cross-amplification in related species.

PREMISE OF THE STUDY: We developed 24 nuclear microsatellite primers from an enriched genomic library for the Pacific coastal dune endemic Camissoniopsis cheiranthifolia to study the consequences of mating system differentiation, the genetics of species' range limits, and hybridization with its closest sister taxon, C. bistorta. • METHODS AND RESULTS: Twenty-four primer pairs were developed and characterized in four populations of C. cheiranthifolia and one population of C. bistorta. We also tested eight additional taxa for cross-amplification. The average number of alleles per locus per species was 4.3 and 6.0, respectively. The number of loci that amplified and were variable within the eight related taxa ranged from six to 17. • CONCLUSIONS: These markers will be useful in studying mating system evolution, the genetic structure of species' ranges, hybridization, and the provenance of material used for habitat restoration in C. cheiranthifolia, C. bistorta, and related species.

Are species' range limits simply niche limits writ large? A review of transplant experiments beyond the range.

Many species' range limits (RL) occur across continuous environmental gradients without obvious barriers imposing them. Such RL are expected to reflect niche limits (NL) and thus to occur where populations cease to be self-sustaining. Transplant experiments comparing fitness within and beyond species' ranges can test this hypothesis, but interpretive power depends strongly on experimental design. We first identify often overlooked aspects of transplant design that are critical to establishing the causes of RL, especially incorporating transplant sites at, and source populations from, the range edge. We then conduct a meta-analysis of published beyond-range transplant experiments (n = 11 tests). Most tests (75%) found that performance declined beyond the range, with the strongest declines detected when the measure of performance was lifetime fitness (83%), suggesting that RL commonly involve niche constraints (declining habitat quality). However, only 46% supported range limits occurring at NL; 26% (mostly geographic RL) fell short of NL with self-sustaining transplants beyond the range, and 23% (all elevational RL) exceeded NL with range-edge populations acting as demographic sinks. These data suggest an important but divergent role for dispersal, which may commonly constrain geographic distributions while extending elevational limits. Meta-analysis results also supported the importance of biotic interactions at RL, particularly the long-held assertion of their role in causing low-elevation and equatorial limits.

Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana.

Introduced species frequently show geographic differentiation, and when differentiation mirrors the ancestral range, it is often taken as evidence of adaptive evolution. The mouse-ear cress (Arabidopsis thaliana) was introduced to North America from Eurasia 150-200 years ago, providing an opportunity to study parallel adaptation in a genetic model organism. Here, we test for clinal variation in flowering time using 199 North American (NA) accessions of A. thaliana, and evaluate the contributions of major flowering time genes FRI, FLC, and PHYC as well as potential ecological mechanisms underlying differentiation. We find evidence for substantial within population genetic variation in quantitative traits and flowering time, and putatively adaptive longitudinal differentiation, despite low levels of variation at FRI, FLC, and PHYC and genome-wide reductions in population structure relative to Eurasian (EA) samples. The observed longitudinal cline in flowering time in North America is parallel to an EA cline, robust to the effects of population structure, and associated with geographic variation in winter precipitation and temperature. We detected major effects of FRI on quantitative traits associated with reproductive fitness, although the haplotype associated with higher fitness remains rare in North America. Collectively, our results suggest the evolution of parallel flowering time clines through novel genetic mechanisms.

Broad geographic covariation between floral traits and the mating system in Camissoniopsis cheiranthifolia (Onagraceae): multiple stable mixed mating systems across the species' range?

BACKGROUND AND AIMS: Plants vary widely in the extent to which seeds are produced via self-fertilization vs. outcrossing, and evolutionary change in the mating system is thought to be accompanied by genetic differentiation in a syndrome of floral traits. We quantified the pattern of variation and covariation in floral traits and the proportion of seeds outcrossed (t) to better understand the evolutionary processes involved in mating system differentiation among and within populations of the short-lived Pacific coastal dune endemic Camissoniopsis cheiranthifolia across its geographic range in western North America. METHODS: We quantified corolla width and herkogamy, two traits expected to influence the mating system, for 48 populations sampled in the field and for a sub-sample of 29 populations grown from seed in a glasshouse. We also measured several other floral traits for 9-19 populations, estimated t for 16 populations using seven allozyme polymorphisms, and measured the strength of self-incompatibility for nine populations. KEY RESULTS: Floral morphology and self-incompatibility varied widely but non-randomly, such that populations could be assigned to three phenotypically and geographically divergent groups. Populations spanned the full range of outcrossing (t = 0·001-0·992), which covaried with corolla width, herkogamy and floral life span. Outcrossing also correlated with floral morphology within two populations that exhibited exceptional floral variation. CONCLUSIONS: Populations of C. cheiranthifolia seem to have differentiated into three modal mating systems: (1) predominant outcrossing associated with self-incompatibility and large flowers; (2) moderate selfing associated with large but self-compatible flowers; and (3) higher but not complete selfing associated with small, autogamous, self-compatible flowers. The transition to complete selfing has not occurred even though the species appears to possess the required genetic capacity. We hypothesize that outcrossing populations in this species have evolved to different stable states of mixed mating.

Ecological correlates of fitness across the northern geographic range limit of a Pacific Coast dune plant.

A species is expected to occur where the prevailing biotic and abiotic conditions fall within its fundamental niche. Geographic range limits should, therefore, occur when the survival and fitness of individuals along ecological gradients is reduced to the point at which populations are no longer self-sustaining. Abrupt limits to a species' distribution are expected to reflect abrupt changes in the ecological conditions that cause sharp declines in fitness across the limit. We investigated the correlation between geographic variation in environment and fitness across the abrupt northern range limit of a coastal dune plant, Camissoniopsis cheiranthifolia (Onagraceae). In each of 64 plots distributed across five sites along a 200-km transect spanning the species' northern range limit (four within the range plus one beyond the limit), we measured plant community composition as a proxy for variation in biotic and abiotic environmental factors and lifetime fitness of genetically standardized experimental populations of C. cheiranthifolia. There was substantial variation in plant community composition among plots and sites across the range limit, and fitness of experimental plants covaried strongly with the first principal component of plant community composition. However, we did not detect an abrupt shift in plant community or the expected decline in fitness across the range limit. In fact, fitness and recruitment increased toward the limit and were relatively high beyond the limit. This suggests that habitat beyond the range did not occur outside of the species' fundamental niche. These results challenge niche-based explanations for range limits and suggest that hypotheses involving the finer-scale distribution of habitat patches or constraints on dispersal warrant more serious consideration.

Discordant longitudinal clines in flowering time and phytochrome C in Arabidopsis thaliana.

Using seasonal cues to time reproduction appropriately is crucial for many organisms. Plants in particular often use photoperiod to signal the time to transition to flowering. Because seasonality varies latitudinally, adaptation to local climate is expected to result in corresponding clines in photoperiod-related traits. By experimentally manipulating photoperiod cues and measuring the flowering responses and photoperiod plasticity of 138 Eurasian accessions of Arabidopsis thaliana, we detected strong longitudinal but not latitudinal clines in flowering responses. The presence of longitudinal clines suggests that critical photoperiod cues vary among populations occurring at similar latitudes. Haplotypes at PHYC, a locus hypothesized to play a role in adaptation to light cues, were also longitudinally differentiated. Controlling for neutral population structure revealed that PHYC haplotype influenced flowering time; however, the distribution of PHYC haplotypes occurred in the opposite direction to the phenotypic cline, suggesting that loci other than PHYC are responsible for the longitudinal pattern in photoperiod response. Our results provide previously missing empirical support for the importance of PHYC in mediating photoperiod sensitivity in natural populations of A. thaliana. However, they also suggest that other loci and epistatic interactions likely play a role in the determination of flowering time and that the environmental factors influencing photoperiod in plants vary longitudinally as well as latitudinally.

Increased seed dispersal potential towards geographic range limits in a Pacific coast dune plant.

Dispersal may be favoured at geographic range edges by unstable population and metapopulation dynamics. However, dispersal may also evolve in response to geographic variation in other life-history traits, especially the mating system. Here, increased dispersal at range margins was tested for with a range-wide analysis of seed dispersal and mating system traits in Abronia umbellata, a plant endemic to Pacific coastal dunes of North America. Seeds disperse within winged anthocarps. Anthocarps from 34 populations varied widely in wing size (mass-corrected wing index). Wing index correlated negatively with threshold wind velocity for dispersal in wind tunnel tests, suggesting that wings facilitate tumbling over open sandy substrate. As predicted, wing index increased and threshold velocity decreased towards both range limits. Flower size, herkogamy and self-incompatibility declined towards range limits, indicating a shift to self-fertilization, and flower size and wing index correlated negatively. However, the increase in wing index towards range limits remained after statistically controlling flower size. These results are consistent with selection favouring dispersal at range margins. The evolutionary lability of dispersal across the range may affect the interaction between selection and gene flow in the establishment and maintenance of geographic range limits.

Testing the abundant center model using range-wide demographic surveys of two coastal dune plants.

It is widely accepted that species are most abundant at the center of their geographic ranges and become progressively rarer toward range limits. Although the abundant center model (ACM) has rarely been tested with range-wide surveys, it influences much thinking about the ecology and evolution of species' distributions. We tested ACM predictions using two unrelated but ecologically similar plants, Camissonia cheiranthifolia and Abronia umbellata. We intensively sampled both throughout their one-dimensional distributions within the Pacific coastal dunes of North America, from northern Baja California, Mexico, to southern Oregon, USA. Data from > 1100 herbarium specimens indicated that these limits have been stable for at least the last 100 years. Range-wide field surveys detected C. cheiranthifolia at 87% of 124 sites and A. umbellata at 54% of 113 sites, but site occupancy did not decline significantly toward range limits for either species. Permutation analysis did not detect a significant fit of geographical variation in local density to the ACM. Mean density did not correlate negatively with mean individual performance (plant size or number of seeds/plant), probably because both species occur at low densities. Although size and seeds per plant varied widely, central populations tended to have the highest values for size only. For C. cheiranthifolia, we observed asymmetry in the pattern of variation between the northern and southern halves of the range consistent with the long-standing prediction that range limits are imposed by different ecological factors in different parts of the geographical distribution. However, these asymmetries were difficult to interpret and likely reflect evolutionary differentiation as well as plastic responses to ecological variation. Both density and seeds per plant contributed to variation in seed production per unit area. In C. cheiranthifolia only, sites with highest seed production tended to occur at the range center, as predicted by the ACM and assumed by theory proposing that range limits evolve via antagonism between natural selection and gene flow.