Evolvability and trait function predict phenotypic divergence of plant populations.

Understanding the causes and limits of population divergence in phenotypic traits is a fundamental aim of evolutionary biology, with the potential to yield predictions of adaptation to environmental change. Reciprocal transplant experiments and the evaluation of optimality models suggest that local adaptation is common but not universal, and some studies suggest that trait divergence is highly constrained by genetic variances and covariances of complex phenotypes. We analyze a large database of population divergence in plants and evaluate whether evolutionary divergence scales positively with standing genetic variation within populations (evolvability), as expected if genetic constraints are evolutionarily important. We further evaluate differences in divergence and evolvability-divergence relationships between reproductive and vegetative traits and between selfing, mixed-mating, and outcrossing species, as these factors are expected to influence both patterns of selection and evolutionary potentials. Evolutionary divergence scaled positively with evolvability. Furthermore, trait divergence was greater for vegetative traits than for floral (reproductive) traits, but largely independent of the mating system. Jointly, these factors explained ~40% of the variance in evolutionary divergence. The consistency of the evolvability-divergence relationships across diverse species suggests substantial predictability of trait divergence. The results are also consistent with genetic constraints playing a role in evolutionary divergence.

Local adaptation primes cold-edge populations for range expansion but not warming-induced range shifts.

According to theory, edge populations may be poised to expand species' ranges if they are locally adapted to extreme conditions, or ill-suited to colonise beyond-range habitat if their offspring are genetically and competitively inferior. We tested these contrasting predictions by transplanting low-, mid-, and high-elevation (edge) populations of an annual plant throughout and above its elevational distribution. Seed from poor-quality edge habitat (one of two transects) had inferior emergence, but edge seeds also had adaptive phenology (both transects). High-elevation plants flowered earlier, required less heat accumulation to mature seed, and so achieved higher lifetime fitness at and above the range edge. Experimental warming improved fitness above the range, but eliminated the advantage of local cold-edge populations, supporting recent models in which cold-adapted edge populations do not facilitate warming-induced range shifts. The highest above-range fitness was achieved by a 'super edge phenotype' from a neighbouring mountain, suggesting key adaptations exist regionally even if absent from local edge populations.

Understanding Maladaptation by Uniting Ecological and Evolutionary Perspectives.

Evolutionary biologists have long trained their sights on adaptation, focusing on the power of natural selection to produce relative fitness advantages while often ignoring changes in absolute fitness. Ecologists generally have taken a different tack, focusing on changes in abundance and ranges that reflect absolute fitness while often ignoring relative fitness. Uniting these perspectives, we articulate various causes of relative and absolute maladaptation and review numerous examples of their occurrence. This review indicates that maladaptation is reasonably common from both perspectives, yet often in contrasting ways. That is, maladaptation can appear strong from a relative fitness perspective, yet populations can be growing in abundance. Conversely, resident individuals can appear locally adapted (relative to nonresident individuals) yet be declining in abundance. Understanding and interpreting these disconnects between relative and absolute maladaptation, as well as the cases of agreement, is increasingly critical in the face of accelerating human-mediated environmental change. We therefore present a framework for studying maladaptation, focusing in particular on the relationship between absolute and relative fitness, thereby drawing together evolutionary and ecological perspectives. The unification of these ecological and evolutionary perspectives has the potential to bring together previously disjunct research areas while addressing key conceptual issues and specific practical problems.

Interannual variation in season length is linked to strong co-gradient plasticity of phenology in a montane annual plant.

Species are commonly distributed along latitudinal and elevational gradients of growing season length to which they might respond via phenotypic plasticity and/or adaptive genetic differentiation. However, the relative contribution of these processes and whether plasticity, if it occurs, facilitates expansion along season-length gradients remain unclear, but are important for predicting species fates during anthropogenic change. We quantified phenological trait variation in the montane annual Rhinanthus minor for three generations at 12 sites across 900 m of elevation in the Canadian Rocky Mountains and conducted a reciprocal transplant experiment for two generations among nine sites. We compared clines and interannual variation of phenological traits between natural and transplanted individuals. Season length declined by c. 37% along our elevational gradient and, as expected, plants emerged, reached first flower and made their first seed in c. 41% fewer growing degree days under shorter growing seasons. Although reciprocal transplants revealed modest genetic differentiation across elevation, trait clines primarily were due to striking co-gradient plasticity that paralleled genetic differentiation. Co-gradient plasticity likely evolved in response to considerable interannual variation in season length across our elevational transect, and should prepare R. minor to make adaptive changes to phenology in response to ongoing climate change predicted for montane environments.

The contribution of hybridization to range-wide population genetic structure in a Pacific coastal dune plant.

PREMISE: Interspecific hybridization can cause genetic structure across species ranges if the mating system and degree of sympatry/parapatry with close relatives varies geographically. The coastal dune endemic Camissoniopsis cheiranthifolia (Onagraceae) exhibits genetic subdivisions across its range, some of which are associated with shifts in mating system from outcrossing to selfing, while others are not. For instance, strong differentiation between large-flowered, self-incompatible (LF-SI) and large-flowered, self-compatible (LF-SC) populations occurs without much reduction in outcrossing or obvious barriers to gene flow. We hypothesized that LF-SI diverged from LF-SC via hybridization with the predominantly inland SI sister species C. bistorta. METHODS: We analyzed spatial proximity using 1460 herbarium records and genetic variation at 12 microsatellites assayed for 805 and 404 individuals from 32 C. cheiranthifolia and 18 C. bistorta populations, respectively. We also assayed nine chloroplast microsatellites for 124 and 111 individuals from 27 and 19 populations, respectively. RESULTS: Closer parapatry was associated with unexpectedly high genetic continuity between LF-SI C. cheiranthifolia and C. bistorta. LF-SI genotypes clustered with C. bistorta exclusive of other C. cheiranthifolia genotypes. Similarly, pairwise FST among SI C. cheiranthifolia and C. bistorta, adjusted for geographic proximity, was not higher between heterospecific than conspecific populations. CONCLUSIONS: The lack of genetic differentiation between LF-SI C. cheiranthifolia and C. bistorta populations, even those located away from the zone of parapatry, suggests that, instead of hybridizing with C. bistorta, LF-SI C. cheiranthifolia is rather an ecotype of C. bistorta that has adapted to coastal dune habitat independent of other lineages in C. cheiranthifolia proper.

Global biogeography of mating system variation in seed plants.

Latitudinal gradients in biotic interactions have been suggested as causes of global patterns of biodiversity and phenotypic variation. Plant biologists have long speculated that outcrossing mating systems are more common at low than high latitudes owing to a greater predictability of plant-pollinator interactions in the tropics; however, these ideas have not previously been tested. Here, we present the first global biogeographic analysis of plant mating systems based on 624 published studies from 492 taxa. We found a weak decline in outcrossing rate towards higher latitudes and among some biomes, but no biogeographic patterns in the frequency of self-incompatibility. Incorporating life history and growth form into biogeographic analyses reduced or eliminated the importance of latitude and biome in predicting outcrossing or self-incompatibility. Our results suggest that biogeographic patterns in mating system are more likely a reflection of the frequency of life forms across latitudes rather than the strength of plant-pollinator interactions.

Variation in pollen limitation and floral parasitism across a mating system transition in a Pacific coastal dune plant: evolutionary causes or ecological consequences?

BACKGROUND AND AIMS: Evolutionary transitions from outcrossing to self-fertilization are thought to occur because selfing provides reproductive assurance when pollinators or mates are scarce, but they could also occur via selection to reduce floral vulnerability to herbivores. This study investigated geographic covariation between floral morphology, fruit set, pollen limitation and florivory across the geographic range of Camissoniopsis cheiranthifolia, a Pacific coastal dune endemic that varies strikingly in flower size and mating system. METHODS: Fruit set was quantified in 75 populations, and in 41 of these floral herbivory by larvae of a specialized moth (Mompha sp.) that consumes anthers in developing buds was also quantified. Experimental pollen supplementation was performed to quantify pollen limitation in three large-flowered, outcrossing and two small-flowered, selfing populations. These parameters were also compared between large- and small-flowered phenotypes within three mixed populations. KEY RESULTS: Fruit set was much lower in large-flowered populations, and also much lower among large- than small-flowered plants within populations. Pollen supplementation increased per flower seed production in large-flowered but not small-flowered populations, but fruit set was not pollen limited. Hence inadequate pollination cannot account for the low fruit set of large-flowered plants. Floral herbivory was much more frequent in large-flowered populations and correlated negatively with fruit set. However, florivores did not preferentially attack large-flowered plants in three large-flowered populations or in two of three mixed populations. CONCLUSIONS: Selfing alleviated pollen limitation of seeds per fruit, but florivory better explains the marked variation in fruit set. Although florivory was more frequent in large-flowered populations, large-flowered individuals were not generally more vulnerable within populations. Rather than a causative selective factor, reduced florivory in small-flowered, selfing populations is probably an ecological consequence of mating system differentiation, with potentially significant effects on population demography and biotic interactions.

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.

Is adaptation associated with long-term persistence beyond a geographic range limit?

Adaptation to new habitats might facilitate species' range shifts in response to climate change. In 2005, we transplanted experimental populations of coastal dune plant Camissoniopsis cheiranthifolia into four sites within and one site beyond its poleward range limit. Beyond-range transplants had high fitness and often delayed reproduction. To test for adaptation associated with experimental range expansion, we transplanted descendants from beyond and within-range populations after 10 generations in situ into two sites within the range, one at the range edge, and two sites beyond the range. We expected to detect adaptation to beyond-range conditions due to substantial genetic variation within experimental populations and environmental variation among sites. However, individuals from beyond-range experimental populations were not fitter than those from within the range when planted at either beyond-range site, indicating no adaptation to the beyond-range site or beyond-range environments in general. Beyond-range descendants also did not suffer lower fitness within the range. Although reproduction was again delayed beyond the range, late reproduction was not favored more strongly beyond than within the range, and beyond-range descendants did not delay reproduction more than within-range descendants. Persistence in beyond-range environments may not require adaptation, which could allow a rapid response to climate change.

Dramatic vestigialization of floral fragrance across a transition from outcrossing to selfing in Abronia umbellata (Nyctaginaceae).

PREMISE OF THE STUDY: Vestigialization of traits that no longer enhance fitness is a common theme in evolution. Plants often use colorful, scented flowers to attract pollinators that mediate outcross pollination. After an evolutionary shift from outcrossing to self-fertilization, where cross-pollination is no longer necessary, attractive traits may be reduced, especially because these traits may also attract herbivores. Selection may be particularly strong in moth-pollinated lineages where pollinators are also herbivores. METHODS: We used field surveys and common garden glasshouse experiments to test this hypothesis by quantifying components of flower size and display and floral volatiles in outcrossing vs. selfing populations of the moth-pollinated Pacific coastal dune endemic Abronia umbellata. KEY RESULTS: Floral face diameter and flower tube length were 43% and 54% smaller in selfing than outcrossing populations, and selfers displayed 15% fewer flowers per umbel. Selfers emitted 99% less total floral volatiles per flower per hour than outcrossers; a much stronger reduction. The chemical composition of volatiles also differed between outcrossers and selfers. Similar differences were observed in a common glasshouse environment, suggesting genetic differentiation in these floral attractive traits among populations. Contrary to expectations, there were no differences in leaf or flower herbivory between selfing and outcrossing populations. CONCLUSIONS: Floral fragrance is much more dramatically reduced in selfing compared to outcrossing populations than other floral attractive traits, but probably not due to selection exerted by moth herbivory. Reduction in aspects of flower size may be constrained by developmental linkages with fruit and seed size.

Population bottleneck associated with but likely preceded the recent evolution of self-fertilization in a coastal dune plant.

Evolution of self-fertilization may be initiated by a historical population bottleneck, which should diagnostically reduce lineage-wide genetic variation. However, selfing can also strongly reduce genetic variation after it evolves. Distinguishing process from pattern is less problematic if mating system divergence is recent and geographically simple. Dramatically reduced diversity is associated with the transition from outcrossing to selfing in the Pacific coastal endemic Abronia umbellata that includes large-flowered, self-incompatible populations (var. umbellata) south of San Francisco Bay and small-flowered, autogamous populations (var. breviflora) to the north. Compared to umbellata, synonymous nucleotide diversity across 10 single-copy nuclear genes was reduced by 94% within individual populations and 90% across the whole selfing breviflora lineage, which contained no unique polymorphisms. The geographic pattern of genetic variation is consistent with a single origin of selfing that occurred recently (7-28 kya). These results are best explained by a historical bottleneck, but the two most northerly umbellata populations also contained little variation and clustered with selfing populations, suggesting that substantial diversity loss preceded the origin of selfing. A bottleneck may have set the stage for the eventual evolution of selfing by purging genetic load that prevents the spread of selfing.

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.

Long-term persistence of experimental populations beyond a species' natural range.

Ecological experiments usually infer long-term processes from short-term data, and the analysis of geographic range limits is a good example. Species' geographic ranges may be limited by low fitness due to niche constraints, a hypothesis most directly tested by comparing the fitness of populations transplanted within and beyond the range. Such studies often fail to find beyond-range fitness declines strong enough to conclude that geographic range limits are solely imposed by niche limits. However, almost all studies only follow transplants for a single generation, which will underestimate the importance of niche limitation because critical but infrequent range-limiting events may be missed and methodological issues may artificially boost the fitness of beyond-range transplants. Here, we present the first multi-generation beyond-range transplant experiment that involves adequate replication and proper experimental controls. In 2005, experimental populations of the coastal dune plant Camissoniopsis cheiranthifolia were planted at four sites within and one site beyond the northern limit. Fitness of initial transplants was high beyond the limit, suggesting that the range was limited by dispersal and not niche constraints. To better address the niche-limitation hypothesis, we quantified density and fitness of descendant C. cheiranthifolia populations 12-14 yr (˜10 generations) after transplant. Average annual fruit production and density of reproductive individuals were as high beyond the range as at four comparable experimental populations and eight natural populations within the range, and the beyond-range population had more than tripled in size since it was planted. This provides unprecedented support for the conclusion that northern range limit of C. cheiranthifolia results from something other than niche limitation, likely involving constraints on local dispersal.

Chronic selection for early reproductive phenology in an annual plant across a steep, elevational gradient of growing season length.

Colonization along ubiquitous gradients of growing season length should require adaptation of phenological traits, driven by natural selection. Although phenology often varies with season length and genetic differentiation in phenological traits sometimes seems adaptive, few studies test whether natural selection is responsible for these patterns. The annual plant Rhinanthus minor is genetically differentiated for phenology across a 1000-m elevational gradient of growing season length in the Canadian Rocky Mountains. We estimated phenotypic selection on five phenological traits for three generations of naturally occurring individuals at 12 sites (n = 10,112), and two generations of genetically and phenotypically more variable transplanted populations at nine of these sites (n = 24,611). Selection was weak for most traits, but consistently favored early flowering across the gradient rather than only under short seasons. There was no evidence that apparent selection favoring early reproduction arose from failure to consider all components of fitness, or variation in other correlated phenological traits. Instead, selection for earlier flowering may be balanced by selection for strong cogradient phenological plasticity that indirectly favors later flowering. However, this probably does not explain the consistency of selection on flowering time across this steep, elevational gradient of growing season length.

Evolutionary constraints on adaptive evolution during range expansion in an invasive plant.

Biological invasions may expose populations to strong selection for local adaptation along geographical gradients in climate. However, evolution during contemporary timescales can be constrained by low standing genetic variation and genetic correlations among life-history traits. We examined limits to local adaptation associated with northern migration of the invasive wetland plant purple loosestrife (Lythrum salicaria) using a selection model incorporating a trade-off between flowering time and size at reproduction, and common garden experiments of populations sampled along a latitudinal transect of approximately 1200 km in eastern North America. A strong trade-off between flowering time and size at reproduction caused early-flowering plants to be smaller with reduced seed production in northern populations. Northward spread was associated with a decline in genetic variance within populations and an increase in genetic skew for flowering time and size, with limited genetic variation for small, early-flowering genotypes. These patterns were predicted by our selection model of local adaptation to shorter growing seasons and were not consistent with expectations from non-adaptive processes. Reduced fecundity may limit population growth and rates of spread in northern populations. Identifying genetic constraints on key life-history traits can provide novel insights into invasion dynamics and the causes of range limits in introduced species.

Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation.

Reduced allocation to structures for pollinator attraction is predicted in selfing species. We explored the association between outcrossing and floral display in a broad sample of angiosperms. We used the demonstrated relationship to test for bias against selfing species in the outcrossing rate distribution, the shape of which has relevance for the stability of mixed mating. Relationships between outcrossing rate, flower size, flower number and floral display, measured as the product of flower size and number, were examined using phylogenetically independent contrasts. The distribution of floral displays among species in the outcrossing rate database was compared with that of a random sample of the same flora. The outcrossing rate was positively associated with the product of flower size and number; individually, components of display were less strongly related to outcrossing. Compared with a random sample, species in the outcrossing rate database showed a deficit of small floral display sizes. We found broad support for reduced allocation to attraction in selfing species. We suggest that covariation between mating systems and total allocation to attraction can explain the deviation from expected trade-offs between flower size and number. Our results suggest a bias against estimating outcrossing rates in the lower half of the distribution, but not specifically against highly selfing species.

Correlations among fertility components can maintain mixed mating in plants.

Classical models studying the evolution of self-fertilization in plants conclude that only complete selfing and complete outcrossing are evolutionarily stable. In contrast with this prediction, 42% of seed-plant species are reported to have rates of self-fertilization between 0.2 and 0.8. We propose that many previous models fail to predict intermediate selfing rates because they do not allow for functional relationships among three components of reproductive fitness: self-fertilized ovules, outcrossed ovules, and ovules sired by successful pollen export. Because the optimal design for fertility components may differ, conflicts among the alternative pathways to fitness are possible, and the greatest fertility may be achieved with some self-fertilization. Here we develop and analyze a model to predict optimal selfing rates that includes a range of possible relationships among the three components of reproductive fitness, as well as the effects of evolving inbreeding depression caused by deleterious mutations and of selection on total seed number. We demonstrate that intermediate selfing is optimal for a wide variety of relationships among fitness components and that inbreeding depression is not a good predictor of selfing-rate evolution. Functional relationships subsume the myriad effects of individual plant traits and thus offer a more general and simpler perspective on mating system evolution.

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.

Floral morphology mediates temporal variation in the mating system of a self-compatible plant.

The mating system of self-compatible plants may fluctuate between years in response to ecological factors that cause variation in the deposition of self pollen vs. outcross pollen on stigmas. Such temporal variation may have significant ecological and evolutionary consequences, but it has rarely been studied, and the mechanisms that mediate temporal variation have almost never been investigated. We tested for variation in the proportion of seeds self-fertilized (s) between two years within 19 populations of the short-lived herb Aquilegia canadensis. Selfing varied widely among populations (range in s = 0.17-1.00, mean s = 0.82) but was inconsistent across years, indicating significant temporal variation. Three populations exhibited especially wide swings in the mating system between years. Mean s did not decrease with increasing population size (N), nor was the fluctuation in s associated with mean N or the change in N. As expected, s declined with increasing separation between anthers and stigmas within flowers (herkogamy), and s fluctuated to a greater extent in populations with more herkogamous flowers. Self-compatible plants can experience wide temporal variation in self-fertilization, and floral traits such as herkogamy may mediate temporal variation by forestalling self-pollination and thus allowing outcrossing during periods when pollinators are frequent.