Patterns and effects of gene flow on adaptation across spatial scales: implications for management.

Gene flow can have rapid effects on adaptation and is an important evolutionary tool available when undertaking biological conservation and restoration. This tool is underused partly because of the perceived risk of outbreeding depression and loss of mean fitness when different populations are crossed. In this article, we briefly review some theory and empirical findings on how genetic variation is distributed across species ranges, describe known patterns of gene flow in nature with respect to environmental gradients, and highlight the effects of gene flow on adaptation in small or stressed populations in challenging environments (e.g., at species range limits). We then present a case study involving crosses at varying spatial scales among mountain populations of a trigger plant (Stylidium armeria: Stylidiaceae) in the Australian Alps to highlight how some issues around gene flow effects can be evaluated. We found evidence of outbreeding depression in seed production at greater geographic distances. Nevertheless, we found no evidence of maladaptive gene flow effects in likelihood of germination, plant performance (size), and performance variance, suggesting that gene flow at all spatial scales produces offspring with high adaptive potential. This case study demonstrates a path to evaluating how increasing sources of gene flow in managed wild and restored populations could identify some offspring with high fitness that could bolster the ability of populations to adapt to future environmental changes. We suggest further ways in which managers and researchers can act to understand and consider adaptive gene flow in natural and conservation contexts under rapidly changing conditions.

Archaeal and Bacterial Diversity and Distribution Patterns in Mediterranean-Climate Vernal Pools of Mexico and the Western USA.

Biogeographic patterns in microorganisms are poorly understood, despite the importance of microbial communities for a range of ecosystem processes. Our knowledge of microbial ecology and biogeography is particularly deficient in rare and threatened ecosystems. We tested for three ecological patterns in microbial community composition within ephemeral wetlands-vernal pools-located across Baja California (Mexico) and California (USA): (1) habitat filtering; (2) a latitudinal diversity gradient; and (3) distance decay in community composition. Paired water and soil samples were collected along a latitudinal transect of vernal pools, and bacterial and archaeal communities were characterized using 16S rDNA sequencing. We identified two main microbial communities, with one community present in the soil matrix that included archaeal and bacterial soil taxa, and another community present in the overlying water that was dominated by common freshwater bacterial taxa. Aquatic microbial communities were more diverse in the north, and displayed a significant but inverted latitudinal diversity pattern. Aquatic communities also exhibited a significant distance-decay pattern, with geographic proximity, and precipitation explaining part of the community variation. Collectively these results indicate greater sensitivity to spatial and environmental variation in vernal pool aquatic microbial communities than in soil microbial communities. We conclude that vernal pool aquatic microbial communities can display distribution patterns similar to those exhibited by larger organisms, but differ in some key aspects, such as the latitudinal gradient in diversity.

How is adaptive potential distributed within species ranges?

Quantitative genetic variation (QGV) represents a major component of adaptive potential and, if reduced toward range-edge populations, could prevent a species' expansion or adaptive response to rapid ecological change. It has been hypothesized that QGV will be lower at the range edge due to small populations-often the result of poor habitat quality-and potentially decreased gene flow. However, whether central populations are higher in QGV is unknown. We used a meta-analytic approach to test for a general QGV-range position relationship, including geographic and climatic distance from range centers. We identified 35 studies meeting our criteria, yielding nearly 1000 estimates of QGV (including broad-sense heritability, narrow-sense heritability, and evolvability) from 34 species. The relationship between QGV and distance from the geographic range or climatic niche center depended on the focal trait and how QGV was estimated. We found some evidence that QGV declines from geographic centers but that it increases toward niche edges; niche and geographic distances were uncorrelated. Nevertheless, few studies have compared QGV in both central and marginal regions or environments within the same species. We call for more research in this area and discuss potential research avenues related to adaptive potential in the context of global change.

Draining the Swamping Hypothesis: Little Evidence that Gene Flow Reduces Fitness at Range Edges.

The genetic swamping hypothesis proposes that gene flow from central to peripheral populations inhibits local adaptation and is one of the most widely recognized explanations for range limitation. We evaluated empirical support for this hypothesis in studies quantifying patterns of gene flow to peripheral populations and their resulting fitness outcomes. We found little evidence that gene flow is generally asymmetric from central to peripheral populations and also that gene flow tends to have positive effects on edge population fitness. These findings contravene the long-held assumption that genetic swamping is a common driver of species range limits, and bear important implications for understanding the role of gene flow in range evolution and for predicting and managing eco-evolutionary responses to climate change.

Evidence for adaptive responses to historic drought across a native plant species range.

As climatic conditions change, species will be forced to move or adapt to avoid extinction. Exacerbated by ongoing climate change, California recently experienced a severe and exceptional drought from 2011 to 2017. To investigate whether an adaptive response occurred during this event, we conducted a "resurrection" study of the cutleaf monkeyflower (Mimulus laciniatus), an annual plant, by comparing trait means and variances of ancestral seed collections ("pre-drought") with contemporary descendant collections ("drought"). Plants were grown under common conditions to test whether this geographically restricted species has the capacity to respond evolutionarily to climate stress across its range. We examined if traits shifted in response to the recent, severe drought and included populations across an elevation gradient, including populations at the low- and high-elevation edges of the species range. We found that time to seedling emergence in the drought generation was significantly earlier than in the pre-drought generation, a response consistent with drought adaptation. Additionally, trait variation in days to emergence was reduced in the drought generation, which suggests selection or bottleneck events. Days to first flower increased significantly by elevation, consistent with climate adaptation across the species range. Drought generation plants were larger and had greater reproduction, which was likely a carryover effect of earlier germination. These results demonstrate that rapid shifts in trait means and variances consistent with climate adaptation are occurring within populations, including peripheral populations at warm and cold climate limits, of a plant species with a relatively restricted range that has so far not shifted its elevation distribution during contemporary climate change. Thus, rapid evolution may mitigate, at least temporarily, range shifts under global climate change. This study highlights the need for better understanding rapid adaptation as a means for plant communities to cope with extraordinary climate events.

Testing the niche-breadth-range-size hypothesis: habitat specialization vs. performance in Australian alpine daisies.

Relatively common species within a clade are expected to perform well across a wider range of conditions than their rarer relatives, yet experimental tests of this "niche-breadth-range-size" hypothesis remain surprisingly scarce. Rarity may arise due to trade-offs between specialization and performance across a wide range of environments. Here we use common garden and reciprocal transplant experiments to test the niche-breadth-range-size hypothesis, focusing on four common and three rare endemic alpine daisies (Brachyscome spp.) from the Australian Alps. We used three experimental contexts: (1) alpine reciprocal seedling experiment, a test of seedling survival and growth in three alpine habitat types differing in environmental quality and species diversity; (2) warm environment common garden, a test of whether common daisy species have higher growth rates and phenotypic plasticity, assessed in a common garden in a warmer climate and run simultaneously with experiment 1; and (3) alpine reciprocal seed experiment, a test of seed germination capacity and viability in the same three alpine habitat types as in experiment 1. In the alpine reciprocal seedling experiment, survival of all species was highest in the open heathland habitat where overall plant diversity is high, suggesting a general, positive response to a relatively productive, low-stress environment. We found only partial support for higher survival of rare species in their habitats of origin. In the warm environment common garden, three common daisies exhibited greater growth and biomass than two rare species, but the other rare species performed as well as the common species. In the alpine reciprocal seed experiment, common daisies exhibited higher germination across most habitats, but rare species maintained a higher proportion of viable seed in all conditions, suggesting different life history strategies. These results indicate that some but not all rare, alpine endemics exhibit stress tolerance at the cost of reduced growth rates in low-stress environments compared to common species. Finally, these findings suggest the seed stage is important in the persistence of rare species, and they provide only weak support at the seedling stage for the niche-breadth-range-size hypothesis.

Extensive variation, but not local adaptation in an Australian alpine daisy.

Alpine plants often occupy diverse habitats within a similar elevation range, but most research on local adaptation in these plants has focused on elevation gradients. In testing for habitat-related local adaptation, local effects on seed quality and initial plant growth should be considered in designs that encompass multiple populations and habitats. We tested for local adaptation across alpine habitats in a morphologically variable daisy species, Brachyscome decipiens, in the Bogong High Plains in Victoria, Australia. We collected seed from different habitats, controlled for maternal effects through initial seed size estimates, and characterized seedling survival and growth in a field transplant experiment. We found little evidence for local adaptation for survival or plant size, based on three adaptation measures: Home versus Away, Local versus Foreign, and Sympatric versus Allopatric (SA). The SA measure controlled for planting site and population (site-of-origin) effects. There were significant differences due to site-of-origin and planting site effects. An important confounding factor was the size of plants directly after transplantation of seedlings, which had a large impact on subsequent seedling survival and growth. Initial differences in plant width and height influenced subsequent survival across the growing season but in opposing directions: wide plants had higher survival, but tall plants had lower survival. In an additional controlled garden experiment at Cranbourne Royal Botanic Gardens, site-of-origin effects detected in the field experiments disappeared under more benign homogeneous conditions. Although B. decipiens from different source areas varied significantly when grown across a range of alpine habitats, these differences did not translate into a local or habitat-related fitness advantage. This lack of local advantage may signal weak past selection, and/or weak adaptive transgeneration (plasticity) effects.

What can local and geographic population limits tell us about distributions?

PREMISE OF THE STUDY: Understanding the evolutionary and ecological factors that determine plant distributions is of primary importance in botanical research. These factors may vary in predictable ways across different spatial scales, and thus, we can leverage scale to reveal the underlying processes limiting plant distributions. METHODS: We review various research considerations across local and geographic scales, including the investigation of dispersal and habitat limitation, evolutionary factors, abiotic and biotic factors, and research logistics. We also present two case studies, slender monkeyflower (Mimulus leptaleus) and cut-leaf monkeyflower (Mimulus laciniatus), in the California Sierra Nevada. KEY RESULTS: At a local spatial scale (within 50 m), no seeds were produced from plants sown at sites located just beyond known patches of M. leptaleus, but within the species' geographic range. At a much broader spatial scale (kilometers), at the highest and lowest elevations of the species' range, we found greatly reduced abundance and fecundity in plants sown outside of the geographic range limits of M. laciniatus. CONCLUSIONS: These cases illustrate two contrasting spatial scales, yet agree in their illustration of strong habitat limitation. We end by discussing future avenues of research and by suggesting ways botanical researchers can frame their studies to maximize information gained on species requirements, distribution limits, and conservation among varying spatial scales.

Climate structures genetic variation across a species' elevation range: a test of range limits hypotheses.

Gene flow may influence the formation of species range limits, and yet little is known about the patterns of gene flow with respect to environmental gradients or proximity to range limits. With rapid environmental change, it is especially important to understand patterns of gene flow to inform conservation efforts. Here we investigate the species range of the selfing, annual plant, Mimulus laciniatus, in the California Sierra Nevada. We assessed genetic variation, gene flow, and population abundance across the entire elevation-based climate range. Contrary to expectations, within-population plant density increased towards both climate limits. Mean genetic diversity of edge populations was equivalent to central populations; however, all edge populations exhibited less genetic diversity than neighbouring interior populations. Genetic differentiation was fairly consistent and moderate among all populations, and no directional signals of contemporary gene flow were detected between central and peripheral elevations. Elevation-driven gene flow (isolation by environment), but not isolation by distance, was found across the species range. These findings were the same towards high- and low-elevation range limits and were inconsistent with two common centre-edge hypotheses invoked for the formation of species range limits: (i) decreasing habitat quality and population size; (ii) swamping gene flow from large, central populations. This pattern demonstrates that climate, but not centre-edge dynamics, is an important range-wide factor structuring M. laciniatus populations. To our knowledge, this is the first empirical study to relate environmental patterns of gene flow to range limits hypotheses. Similar investigations across a wide variety of taxa and life histories are needed.

Speciation on a local geographic scale: the evolution of a rare rock outcrop specialist in Mimulus.

Speciation can occur on both large and small geographical scales. In plants, local speciation, where small populations split off from a large-ranged progenitor species, is thought to be the dominant mode, yet there are still few examples to verify speciation has occurred in this manner. A recently described morphological species in the yellow monkey flowers, Mimulus filicifolius, is an excellent candidate for local speciation because of its highly restricted geographical range. Mimulus filicifolius was formerly identified as a population of M. laciniatus due to similar lobed leaf morphology and rocky outcrop habitat. To investigate whether M. filicifolius is genetically divergent and reproductively isolated from M. laciniatus, we examined patterns of genetic diversity in ten nuclear and eight microsatellite loci, and hybrid fertility in M. filicifolius and its purported close relatives: M. laciniatus, M. guttatus and M. nasutus. We found that M. filicifolius is genetically divergent from the other species and strongly reproductively isolated from M. laciniatus. We conclude that M. filicifolius is an independent rock outcrop specialist despite being morphologically and ecologically similar to M. laciniatus, and that its small geographical range nested within other wide-ranging members of the M. guttatus species complex is consistent with local speciation.

Niche and range size patterns suggest that speciation begins in small, ecologically diverged populations in North American monkeyflowers (Mimulus spp.).

Closely related species (e.g., sister taxa) often occupy very different ecological niches and can exhibit large differences in geographic distributions despite their shared evolutionary history. Budding speciation is one process that may partially explain how differences in niche and distribution characteristics may rapidly evolve. Budding speciation is the process through which new species form as initially small colonizing populations that acquire reproductive isolation. This mode of species formation predicts that, at the time of speciation, sister species should have highly asymmetrical distributions. We tested this hypothesis in North American monkeyflowers, a diverse clade with a robust phylogeny, using data on geographical ranges, climate, and plant community attributes. We found that recently diverged sister pairs have highly asymmetrical ranges and niche breadths, relative to older sister pairs. Additionally, we found that sister species occupy distinct environmental niche positions, and that 80% of sister species have completely or partially overlapping distributions (i.e., are broadly sympatric). Together, these results suggest that budding speciation has occurred frequently in Mimulus, that it has likely taken place both inside the range and on the range periphery, and that observed divergences in habitat and resource use could be associated with speciation in small populations.

Genetic isolation by environment or distance: which pattern of gene flow is most common?

Gene flow among populations can enhance local adaptation if it introduces new genetic variants available for selection, but strong gene flow can also stall adaptation by swamping locally beneficial genes. These outcomes can depend on population size, genetic variation, and the environmental context. Gene flow patterns may align with geographic distance (IBD--isolation by distance), whereby immigration rates are inversely proportional to the distance between populations. Alternatively gene flow may follow patterns of isolation by environment (IBE), whereby gene flow rates are higher among similar environments. Finally, gene flow may be highest among dissimilar environments (counter-gradient gene flow), the classic "gene-swamping" scenario. Here we survey relevant studies to determine the prevalence of each pattern across environmental gradients. Of 70 studies, we found evidence of IBD in 20.0%, IBE in 37.1%, and both patterns in 37.1%. In addition, 10.0% of studies exhibited counter-gradient gene flow. In total, 74.3% showed significant IBE patterns. This predominant IBE pattern of gene flow may have arisen directly through natural selection or reflect other adaptive and nonadaptive processes leading to nonrandom gene flow. It also precludes gene swamping as a widespread phenomenon. Implications for evolutionary processes and management under rapidly changing environments (e.g., climate change) are discussed.

Niche breadth predicts geographical range size: a general ecological pattern.

The range of resources that a species uses (i.e. its niche breadth) might determine the geographical area it can occupy, but consensus on whether a niche breadth-range size relationship generally exists among species has been slow to emerge. The validity of this hypothesis is a key question in ecology in that it proposes a mechanism for commonness and rarity, and if true, may help predict species' vulnerability to extinction. We identified 64 studies that measured niche breadth and range size, and we used a meta-analytic approach to test for the presence of a niche breadth-range size relationship. We found a significant positive relationship between range size and environmental tolerance breadth (z = 0.49), habitat breadth (z = 0.45), and diet breadth (z = 0.28). The overall positive effect persisted even when incorporating sampling effects. Despite significant variability in the strength of the relationship among studies, the general positive relationship suggests that specialist species might be disproportionately vulnerable to habitat loss and climate change due to synergistic effects of a narrow niche and small range size. An understanding of the ecological and evolutionary mechanisms that drive and cause deviations from this niche breadth-range size pattern is an important future research goal.

Niche partitioning between close relatives suggests trade-offs between adaptation to local environments and competition.

Niche partitioning among close relatives may reflect trade-offs underlying species divergence and coexistence (e.g., between stress tolerance and competitive ability). We quantified the effects of habitat and congeneric species interactions on fitness for two closely related herbaceous plant species, Mimulus guttatus and Mimulus laciniatus, in three common habitat types within their sympatric range. Drought stress strongly reduced survival of M. guttatus in fast-drying seeps occupied by M. laciniatus, suggesting that divergent habitat adaptation maintains this niche boundary. However, neither seedling performance nor congeneric competition explained the absence of M. laciniatus from shady streams where M. guttatus thrives. M. laciniatus may be excluded from this habitat by competition with other species in the community or mature M. guttatus. Species performance and competitive ability were similar in sympatric meadows where plant community stature and the growing season length are intermediate between seeps and streams. Stochastic effects (e.g., dispersal among habitats or temporal variation) may contribute to coexistence in this habitat. Habitat adaptation, species interactions, and stochastic mechanisms influence sympatric distributions for these recently diverged species.

Gene flow increases fitness at the warm edge of a species' range.

According to theory, gene flow to marginal populations may stall or aid adaptation at range limits by swamping peripheral populations with maladaptive gene flow or by enhancing genetic variability and reducing inbreeding depression, respectively. We tested these contrasting predictions by manipulating patterns of gene flow of the annual plant, Mimulus laciniatus, at its warm range limit. Gene flow was experimentally applied by using crosses within warm-limit populations (selfed and outcrossed), between warm-limit populations, and between warm-limit and central range populations across two elevational transects. We measured the fitness of offspring in a common garden at the warm-edge species range limit. All sources of gene flow increased seedling emergence at the range limit, suggesting local inbreeding depression at both range limit populations; however, lifetime reproductive success only increased significantly when pollen originated from another warm-limit population. Center-to-warm-edge gene flow was maladaptive by delaying time to development at this warm, fast-drying range limit, whereas edge-to-edge gene flow hastened emergence time and time to reproduction. By empirically testing theory on the effects of gene flow on the formation of geographic range limits, we find benefits of gene flow among populations to be greatest when gene flow is between populations occupying the same range limit. Our results emphasize the overlooked importance of gene flow among populations occurring near the same range limit and highlight the potential for prescriptive gene flow as a conservation option for populations at risk from climate change.