Isolation by environment and its consequences for range shifts with global change: Landscape genomics of the invasive plant common tansy.

Invasive species are a growing global economic and ecological problem. However, it is not well understood how environmental factors mediate invasive range expansion. In this study, we investigated the recent and rapid range expansion of common tansy across environmental gradients in Minnesota, USA. We densely sampled individuals across the expanding range and performed reduced representation sequencing to generate a dataset of 3071 polymorphic loci for 176 individuals. We used non-spatial and spatially explicit analyses to determine the relative influences of geographic distance and environmental variation on patterns of genomic variation. We found no evidence for isolation by distance but strong evidence for isolation by environment, indicating that environmental factors may have modulated patterns of range expansion. Land use classification and soils were particularly important variables related to population structure although they operated on different spatial scales; land use classification was related to broad-scale patterns and soils were related to fine-scale patterns. All analyses indicated a distinctive genetic cluster in the most recently invaded portion of the range. Individuals from the far northwestern range margin were separated from the remainder of the range by reduced migration, which was associated with environmental resistance. This portion of the range was invaded primarily in the last 15 years. Ecological niche models also indicated that this cluster was associated with the expansion of the niche. While invasion is often assumed to be primarily influenced by dispersal limitation, our results suggest that ongoing invasion and range shifts with climate change may be strongly affected by environmental heterogeneity.

Chronosequence of invasion reveals minimal losses of population genomic diversity, niche expansion, and trait divergence in the polyploid, leafy spurge.

Rapid evolution may play an important role in the range expansion of invasive species and modify forecasts of invasion, which are the backbone of land management strategies. However, losses of genetic variation associated with colonization bottlenecks may constrain trait and niche divergence at leading range edges, thereby impacting management decisions that anticipate future range expansion. The spatial and temporal scales over which adaptation contributes to invasion dynamics remain unresolved. We leveraged detailed records of the ~130-year invasion history of the invasive polyploid plant, leafy spurge (Euphorbia virgata), across ~500 km in Minnesota, U.S.A. We examined the consequences of range expansion for population genomic diversity, niche breadth, and the evolution of germination behavior. Using genotyping-by-sequencing, we found some population structure in the range core, where introduction occurred, but panmixia among all other populations. Range expansion was accompanied by only modest losses in sequence diversity, with small, isolated populations at the leading edge harboring similar levels of diversity to those in the range core. The climatic niche expanded during most of the range expansion, and the niche of the range core was largely non-overlapping with the invasion front. Ecological niche models indicated that mean temperature of the warmest quarter was the strongest determinant of habitat suitability and that populations at the leading edge had the lowest habitat suitability. Guided by these findings, we tested for rapid evolution in germination behavior over the time course of range expansion using a common garden experiment and temperature manipulations. Germination behavior diverged from the early to late phases of the invasion, with populations from later phases having higher dormancy at lower temperatures. Our results suggest that trait evolution may have contributed to niche expansion during invasion and that distribution models, which inform future management planning, may underestimate invasion potential without accounting for evolution.

Context Dependence of Local Adaptation to Abiotic and Biotic Environments: A Quantitative and Qualitative Synthesis.

Understanding how spatially variable selection shapes adaptation is an area of long-standing interest in evolutionary ecology. Recent meta-analyses have quantified the extent of local adaptation, but the relative importance of abiotic and biotic factors in driving population divergence remains poorly understood. To address this gap, we combined a quantitative meta-analysis and a qualitative metasynthesis to (1) quantify the magnitude of local adaptation to abiotic and biotic factors and (2) characterize major themes that influence the motivation and design of experiments that seek to test for local adaptation. Using local-foreign contrasts as a metric of local adaptation (or maladaptation), we found that local adaptation was greater in the presence than in the absence of a biotic interactor, especially for plants. We also found that biotic environments had stronger effects on fitness than abiotic environments when ignoring whether those environments were local versus foreign. Finally, biotic effects were stronger at low latitudes, and abiotic effects were stronger at high latitudes. Our qualitative analysis revealed that the lens through which local adaptation has been examined differs for abiotic and biotic factors. It also revealed biases in the design and implementation of experiments that make quantitative results challenging to interpret and provided directions for future research.

Species distribution models throughout the invasion history of Palmer amaranth predict regions at risk of future invasion and reveal challenges with modeling rapidly shifting geographic ranges.

Palmer amaranth (Amaranthus palmeri) is an annual plant native to the desert Southwest of the United States and Mexico and has become invasive and caused large economic losses across much of the United States. In order to examine the temporal and spatial dynamics of past invasion, and to predict future invasion, we developed a broad array of species distribution models (SDMs). In particular, we constructed sequential SDMs throughout the invasion history and asked how well those predicted future invasion (1970 to present). We showed that invasion occurred from a restricted set of environments in the native range to a diverse set in the invaded range. Spatial autocorrelation analyses indicated that rapid range expansion was facilitated by stochastic, long-distance dispersal events. Regardless of SDM approach, all SDMs built using datasets from early in the invasion (1970-2010) performed poorly and failed to predict most of the current invaded range. Together, these results suggest that climate is unlikely to have influenced early stages of range expansion. SDMs that incorporated data from the most recent sampling (2011-2017) performed considerably better, predicted high suitability in regions that have recently become invaded, and identified mean annual temperature as a key factor limiting northward range expansion. Under future climates, models predicted both further northward range expansion and significantly increased suitability across large portions of the U.S. Overall, our results indicate significant challenges for SDMs of invasive species far from climate equilibrium. However, our models based on recent data make more robust predictions for northward range expansion of A. palmeri with climate change.

Mating System Evolution under Strong Pollen Limitation: Evidence of Disruptive Selection through Male and Female Fitness in Clarkia xantiana.

Selection on floral traits in hermaphroditic plants is determined by both male and female reproductive success. However, predictions regarding floral trait and mating system evolution are often based solely on female fitness. Selection via male fitness has the potential to affect the outcomes of floral evolution. In this study, we used paternity analysis to assess individual selfing rates and selection on floral traits via male and female fitness in an experimental population of Clarkia xantiana where pollen limitation of seed set was strong. We detected selection through both female and male fitness with reinforcing or noninterfering patterns of selection through the two sex functions. For female fitness, selection favored reduced herkogamy and protandry, traits that promote increased autonomous selfing. For male fitness, selection on petal area was disruptive, with higher trait values conferring greater pollinator attraction and outcross siring success and smaller trait values leading to higher selfed siring success. Combining both female and male fitness, selection on petal area and protandry was disruptive because intermediate phenotypes were less successful as both males and females. Finally, functional relationships among male and female fertility components indicated that selfing resulted in seed discounting and pollen discounting. Under these functional relationships, the evolutionarily stable selfing rate can be intermediate or predominantly selfing or outcrossing, depending on the segregating load of deleterious mutations.

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.

Mating system divergence affects the distribution of sequence diversity within and among populations of recently diverged subspecies of Clarkia xantiana (Onagraceae).

PREMISE OF THE STUDY: The population biology of outcrossing and self-fertilizing taxa is thought to differ because of the advantage that selfers have in colonizing unoccupied sites where mates and pollinators may be limiting (Baker's Law). This reduced tendency for outcrossers to colonize new sites, along with their greater dependence on pollinators to disperse pollen, has the potential to differently influence the genetic diversity and structure of outcrossing and selfing populations. METHODS: We conducted a comparative population genetic study of two sister outcrossing and selfing subspecies of Clarkia xantiana that have very recently diverged. We used DNA sequence variation (>40 kb from eight nuclear loci) from large samples of individuals from 14 populations to assess geographic patterns of genetic diversity and make inferences about the demographic and colonization histories of each subspecies. KEY RESULTS: We show that sequence variation is strongly reduced across all selfing populations. The demographic history of selfing populations exhibits recent colonization bottlenecks, whereas such bottlenecks are rarely observed for the outcrosser. The greater effect of genetic drift in the selfer has resulted in strong population genetic structure, but with no pattern of isolation by distance. By contrast, the stronger effect of gene flow in the outcrosser has resulted in considerably less structure, but a significant pattern of isolation by distance. CONCLUSIONS: Taken together, our results suggest that selfing populations are not at migration-drift equilibrium, are affected by strong episodes of genetic drift during colonization, and experience little or no subsequent gene flow from other populations after those founder events.

No association between plant mating system and geographic range overlap.

PREMISE OF THE STUDY: Automatic self-fertilization may influence the geography of speciation, promote reproductive isolation between incipient species, and lead to ecological differentiation. As such, selfing taxa are predicted to co-occur more often with their closest relatives than are outcrossing taxa. Despite suggestions that this pattern may be general, the extent to which mating system influences range overlap in close relatives has not been tested formally across a diverse group of plant species pairs. METHODS: We tested for a difference in range overlap between species pairs for which zero, one, or both species are selfers, using data from 98 sister species pairs in 20 genera across 15 flowering plant families. We also used divergence time estimates from time-calibrated phylogenies to ask how range overlap changes with divergence time and whether this effect depends on mating system. KEY RESULTS: We found no evidence that automatic self-fertilization influenced range overlap of closely related plant species. Sister pairs with more recent divergence times had modestly greater range overlap, but this effect did not depend on mating system. CONCLUSIONS: The absence of a strong influence of mating system on range overlap suggests that mating system plays a minor or inconsistent role compared with many other mechanisms potentially influencing the co-occurrence of close relatives.

Geographic range size is predicted by plant mating system.

Species' geographic ranges vary enormously, and even closest relatives may differ in range size by several orders of magnitude. With data from hundreds of species spanning 20 genera in 15 families, we show that plant species that autonomously reproduce via self-pollination consistently have larger geographic ranges than their close relatives that generally require two parents for reproduction. Further analyses strongly implicate autonomous self-fertilisation in causing this relationship, as it is not driven by traits such as polyploidy or annual life history whose evolution is sometimes correlated with selfing. Furthermore, we find that selfers occur at higher maximum latitudes and that disparity in range size between selfers and outcrossers increases with time since their evolutionary divergence. Together, these results show that autonomous reproduction--a critical biological trait that eliminates mate limitation and thus potentially increases the probability of establishment--increases range size.

Rapid evolution of reproductive isolation between incipient outcrossing and selfing Clarkia species.

A major goal of speciation research is to understand the processes involved in the earliest stages of the evolution of reproductive isolation (RI). One important challenge has been to identify systems where lineages have very recently diverged and opportunities for hybridization are present. We conducted a comprehensive examination of the components of RI across the life cycle of two subspecies of Clarkia xantiana, which diverged recently (ca. 65,000 bp). One subspecies is primarily outcrossing, but self-compatible, whereas the other is primarily selfing. The subspecies co-occur in a zone of sympatry but hybrids are rarely observed. Premating barriers resulted in nearly complete isolation in both subspecies with flowering time and pollinator preference (for the outcrosser over the selfer) as the strongest barriers. We found that the outcrosser had consistently more competitive pollen, facilitating hybridization in one direction, but no evidence for pollen-pistil interactions as an isolating barrier. Surprisingly, postzygotic isolation was detected at the stage of hybrid seed development, but in no subsequent life stages. This crossing barrier was asymmetric with crosses from the selfer to outcrosser most frequently failing. Collectively, the results provide evidence for rapid evolution of multiple premating and postzygotic barriers despite a very recent divergence time.

Floral and mating system divergence in secondary sympatry: testing an alternative hypothesis to reinforcement in Clarkia.

BACKGROUND AND AIMS: Reproductive character displacement (RCD) is often an important signature of reinforcement when partially cross-compatible taxa meet in secondary sympatry. In this study, floral evolution is examined during the Holocene range expansion of Clarkia xantiana subsp. parviflora from eastern Pleistocene refugia to a western zone of sympatry with its sister taxon, subsp. xantiana. Floral divergence between the two taxa is greater in sympatry than allopatry. The goal was to test an alternative hypothesis to reinforcement - that floral divergence of sympatric genotypes is simply a by-product of adaptation to pollination environments that differ between the allopatric and sympatric portions of the subspecies' range. METHODS: Floral trait data from two common garden studies were used to examine floral divergence between sympatric and allopatric regions and among phylogeographically defined lineages. In natural populations of C. x. parviflora, the magnitude of pollen limitation and reproductive assurance were quantified across its west-to-east range. Potted sympatric and allopatric genotypes were also reciprocally translocated between geographical regions to distinguish between the effects of floral phenotype versus contrasting pollinator environments on reproductive ecology. KEY RESULTS: Sympatric populations are considerably smaller flowered with reduced herkogamy. Pollen limitation and the reproductive assurance value of selfing are greater in sympatric than in allopatric populations. Most significantly, reciprocal translocation experiments showed these differences in reproductive ecology cannot be attributed to contrasting pollinator environments between the sympatric and allopatric regions, but instead reflect the effects of flower size on pollinator attraction. CONCLUSIONS: Floral evolution occurred during the westward range expansion of parviflora, particularly in the zone of sympatry with xantiana. No evidence was found that strongly reduced flower size in sympatric parviflora (and RCD between parviflora and xantiana) is due to adaptation to limited pollinator availability. Rather, floral divergence appears to have been driven by other factors, such as interactions with congenerics in secondary sympatry.

Pollinator-mediated competition between two congeners, Limnanthes douglasii subsp. rosea and L. alba (Limnanthaceae).

PREMISE OF STUDY: Pollinator visits are essential for reproduction in many plants, yet interspecific movements of pollinators can also lead to competitive interactions between coflowering species. Pollination-mediated reductions in fertility could potentially lead to exclusion of competing plant species, and may generate spatial variation in the associations among coflowering species across a landscape. METHODS: I documented the potential for heterospecific pollen transfer to cause competitive interactions between two annual grassland species native to California, Limnanthes douglasii subsp. rosea and L. alba, two reproductively incompatible species that have broadly overlapping geographic ranges in the foothills of the Sierra Nevada. I observed pollinator movement in constructed arrays and controlled crosses in the greenhouse and field to investigate the consequences of heterospecific pollen transfer. KEY RESULTS: Pollinators move readily between species when they are presented together in experimental arrays. In the greenhouse, deposition of heterospecific pollen decreased fertility in both species. The decrease in seeds produced per flower was much more pronounced in L. d. rosea (90.6% reduction) than in L. alba (40.8% reduction). In field experiments, L. d. rosea plants that received pollen from heterospecific neighbors first showed >50% reduction in per-flower fertility. CONCLUSIONS: Under natural pollination conditions, heterospecific pollen transfer has the ability to decrease the fertility of L. d. rosea when it occurs at low frequency in mixed stands. Accordingly, pollinator-mediated competition may contribute to the locally disjunct distributions of these two species. It may also influence important restoration decisions in vernal pool habitats.