The double life of trichomes: understanding their dual role in herbivory and herbicide resistance.

Understanding the evolutionary forces that maintain phenotypic variation in ecologically relevant traits has long been one of the central goals of evolutionary ecology. While the maintenance of variation in plant defense is most often hypothesized to be due to trait trade-offs or spatio-temporal variation in herbivore abundance, the role that heterogeneous selective agents may play on the maintenance of variation in plant defense is less examined. Trichomes are hair-like appendages on plant surfaces that can defend against multiple damaging agents such as pathogens, herbivores, and UV radiation. It is currently unknown however if conflicting selection from such heterogeneous agents of damage may act to maintain the variation observed in trichome traits. Here, we assess whether trichomes serve as an herbicide resistance trait and how it coincides with the conventionally studied defensive strategy of herbivory resistance. In a series of experiments, we exposed the annual invasive velvetleaf (Abutilon theophrasti) to glyphosate (active ingredient in "Roundup") to investigate whether trichome traits (type and density) are linked to herbicide resistance and to test whether herbicide influences selection on plant trichomes. We found that an increased proportion of branched trichomes positively impacted herbicide resistance and chewing herbivory resistance. We also found evidence that glyphosate imposes positive selection on branched trichomes in velvetleaf. Overall, our results indicate that branched trichomes can contribute to both herbicide and herbivory resistance, serving a concordant rather than conflicting role to reduce plant injury. Our findings further suggest that novel anthropogenic agents of selection can alter the composition of plant defense traits, potentially impacting trait-mediated interactions among external stressors.

Not just flowering time: a resurrection approach shows floral attraction traits are changing over time.

Contemporary anthropogenic changes in climate and landscape form a complex set of selective pressures acting on natural systems, yet, in many systems, we lack information about both whether and how organisms may adapt to these changes. In plants, research has focused on climate-induced changes in phenology and the resultant potential for disruption of plant-pollinator interactions, however, there remains a paucity of knowledge regarding how other pollinator-mediated traits may be involved in the adaptive response. Here, we use resurrection experiments to investigate the phenotypic basis of adaptation in a mixed-mating system plant, the common morning glory (Ipomoea purpurea). Specifically, we measure temporal and spatial changes in traits grouped into three categories relevant to plant-pollinator interactions - floral morphology, floral rewards, and floral phenology. We show a significant temporal increase in corolla size and shift to earlier flowering times, as well as a potential for increased investment in floral rewards, all of which are driven primarily by populations at more northern latitudes. Additionally, we find evidence for directional selection on floral morphology and phenology and evidence of balancing selection acting on anther-stigma distance. Overall, these results show an adaptive response in line with greater investment in pollinator attraction rather than self-pollination and fine-scale spatial differences in adaptive potential.

The consequences of synthetic auxin herbicide on plant-herbivore interactions.

Although herbicide drift is a common side effect of herbicide application in agroecosystems, its effects on the ecology and evolution of natural communities are rarely studied. A recent shift to dicamba, a synthetic auxin herbicide known for 'drifting' to nontarget areas, necessitates the examination of drift effects on the plant-insect interactions that drive eco-evo dynamics in weed communities. We review current knowledge of direct effects of synthetic auxin herbicides on plant-insect interactions, focusing on plant herbivory, and discuss potential indirect effects, which are cascading effects on organisms that interact with herbicide-exposed plants. We end by developing a framework for the study of plant-insect interactions given drift, highlighting potential changes to plant developmental timing, resource quantity, quality, and cues.

Interchromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance.

The adaptation of weeds to herbicide is both a significant problem in agriculture and a model of rapid adaptation. However, significant gaps remain in our knowledge of resistance controlled by many loci and the evolutionary factors that influence the maintenance of resistance. Here, using herbicide-resistant populations of the common morning glory (Ipomoea purpurea), we perform a multilevel analysis of the genome and transcriptome to uncover putative loci involved in nontarget-site herbicide resistance (NTSR) and to examine evolutionary forces underlying the maintenance of resistance in natural populations. We found loci involved in herbicide detoxification and stress sensing to be under selection and confirmed that detoxification is responsible for glyphosate (RoundUp) resistance using a functional assay. We identified interchromosomal linkage disequilibrium (ILD) among loci under selection reflecting either historical processes or additive effects leading to the resistance phenotype. We further identified potential fitness cost loci that were strongly linked to resistance alleles, indicating the role of genetic hitchhiking in maintaining the cost. Overall, our work suggests that NTSR glyphosate resistance in I. purpurea is conferred by multiple genes which are potentially maintained through generations via ILD, and that the fitness cost associated with resistance in this species is likely a by-product of genetic hitchhiking.

Interspecific variation in resistance and tolerance to herbicide drift reveals potential consequences for plant community co-flowering interactions and structure at the agro-eco interface.

BACKGROUND AND AIMS: When plant communities are exposed to herbicide 'drift', wherein particles containing the active ingredient travel off-target, interspecific variation in resistance or tolerance may scale up to affect community dynamics. In turn, these alterations could threaten the diversity and stability of agro-ecosystems. We investigated the effects of herbicide drift on the growth and reproduction of 25 wild plant species to make predictions about the consequences of drift exposure on plant-plant interactions and the broader ecological community. METHODS: We exposed potted plants from species that commonly occur in agricultural areas to a drift-level dose of the widely used herbicide dicamba or a control solution in the glasshouse. We evaluated species-level variation in resistance and tolerance for vegetative and floral traits. We assessed community-level impacts of drift by comparing the species evenness and flowering networks of glasshouse synthetic communities comprised of drift-exposed and control plants. KEY RESULTS: Species varied significantly in resistance and tolerance to dicamba drift: some were negatively impacted while others showed overcompensatory responses. Species also differed in the way they deployed flowers over time following drift exposure. While drift had negligible effects on community evenness based on vegetative biomass, it caused salient differences in the structure of co-flowering networks within communities. Drift reduced the degree and intensity of flowering overlap among species, altered the composition of groups of species that were more likely to co-flower with each other than with others and shifted species roles (e.g. from dominant to inferior floral producers, and vice versa). CONCLUSIONS: These results demonstrate that even low levels of herbicide exposure can significantly alter plant growth and reproduction, particularly flowering phenology. If field-grown plants respond similarly, then these changes would probably impact plant-plant competitive dynamics and potentially plant-pollinator interactions occurring within plant communities at the agro-ecological interface.

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed.

Plastic phenotypic responses to environmental change are common, yet we lack a clear understanding of the fitness consequences of these plastic responses. Here, we use the evolution of herbicide resistance in the common morning glory (Ipomoea purpurea) as a model for understanding the relative importance of adaptive and maladaptive gene expression responses to herbicide. Specifically, we compare leaf gene expression changes caused by herbicide to the expression changes that evolve in response to artificial selection for herbicide resistance. We identify a number of genes that show plastic and evolved responses to herbicide and find that for the majority of genes with both plastic and evolved responses, plastic responses appear to be adaptive. We also find that selection for herbicide response increases gene expression plasticity. Overall, these results show the importance of adaptive plasticity for herbicide resistance in a common weed and that expression changes in response to strong environmental change can be adaptive.

Variable inbreeding depression may explain associations between the mating system and herbicide resistance in the common morning glory.

Inbreeding depression is a central parameter underlying mating system variation in nature and one that can be altered by environmental stress. Although a variety of systems show that inbreeding depression tends to increase under stressful conditions, we have very little understanding across most organisms how the level of inbreeding depression may change as a result of adaptation to stressors. In this work we examined the potential that inbreeding depression varied among lineages of Ipomoea purpurea artificially evolved to exhibit divergent levels of herbicide resistance. We examined inbreeding depression in a variety of fitness-related traits in both the growth chamber and in the field, and paired this work with an examination of gene expression changes. We found that, while inbreeding depression was present across many of the traits, lineages artificially selected for increased herbicide resistance often showed no evidence of inbreeding depression in the presence of herbicide, and in fact, showed evidence of outbreeding depression in some traits compared to nonselected control lines and lineages selected for increased herbicide susceptibility. Further, at the transcriptome level, the resistant selection lines had differing patterns of gene expression according to breeding type (inbred vs. outcrossed) compared to the control and susceptible selection lines. Our data together indicate that inbreeding depression may be lessened in populations that are adapting to regimes of strong selection.

Who are we now? A demographic assessment of three evolution societies.

Scientific societies have the potential to catalyze support for communities that have been historically excluded from science. Many of these societies have formed committees to propose and administer initiatives to promote the career and well-being of their members, with a special emphasis on racial and ethnic minorities. Yet, these societies are rarely armed with data to inform their proposals. Three of the evolution societies (American Society of Naturalists, "ASN"; Society of Systematic Biologists, "SSB"; Society for the Study of Evolution, "SSE") have also formed Diversity, Equity, and Inclusion committees in the last few years. As a first step in determining the needs of the societies, these committees collected data on the demographic characteristics of the societies' constituents by surveying the attendants of the Evolution 2019 meeting. Here, we report the proportions for different demographic groups in attendance at the meeting and compare these proportions to the demographics of recipients of Ph.D. degrees either in evolutionary biology or in the broader life sciences, as well as population demographics of the USA. Our results indicate that historically excluded groups are still underrepresented across US-based evolutionary biology professional societies. We explore whether demographic composition differs at different professional stages and find that representation for women and LGBTQ+ members decreases as the career stage progresses. We also find some evidence for heterogeneity across societies in terms of racial composition. Finally, we discuss the caveats and limitations of our procedures. Our results will serve to inform future efforts to collect demographic data at the society levels, which should in turn be used to design and implement evidence-based initiatives for inclusion and equity. This report should be a starting point for systematic efforts to characterize the ever-changing representation in evolutionary biology and to work toward the inclusion of all groups.

Herbicides as anthropogenic drivers of eco-evo feedbacks in plant communities at the agro-ecological interface.

Herbicides act as human-mediated novel selective agents and community disruptors, yet their full effects on eco-evolutionary dynamics in natural communities have only begun to be appreciated. Here, we synthesize how herbicide exposures can result in dramatic phenotypic and compositional shifts within communities at the agro-ecological interface and how these in turn affect species interactions and drive plant (and plant-associates') evolution in ways that can feedback to continue to affect the ecology and ecosystem functions of these assemblages. We advocate a holistic approach to understanding these dynamics that includes plastic changes and plant community transformations and also extends beyond this single trophic level targeted by herbicides to the effects on nontarget plant-associated organisms and their potential to evolve, thereby embracing the complexity of these real-world systems. We make explicit recommendations for future research to achieve this goal and specifically address impacts of ecology on evolution, evolution on ecology and their feedbacks so that we can gain a more predictive view of the fates of herbicide-impacted communities.

Below-ground competition favors character convergence but not character displacement in root traits.

Character displacement can play a major role in species ecology and evolution; however, research testing whether character displacement can influence the evolution of root traits in plant systems remains scarce in the literature. Here we investigated the potential that character displacement may influence the evolution of root traits using two closely related morning glory species, Ipomoea purpurea and Ipomoea hederacea. We performed a field experiment where we grew the common morning glory, I. purpurea, in the presence and absence of competition from I. hederacea and examined the potential that the process of character displacement could influence the evolution of root traits. We found maternal line variation in root phenotypes and evidence that below-ground competition acts as an agent of selection on these traits. Our test of character displacement, however, showed evidence of character convergence on our measure of root architecture rather than displacement. These results suggest that plants may be constrained by their local environments to express a phenotype that enhances fitness. Therefore, the conditions of the competitive environment experienced by a plant may influence the potential for character convergence or displacement to influence the evolution of root traits.

Belowground Competition Can Influence the Evolution of Root Traits.

Although root traits play a critical role in mediating plant-plant interactions and resource acquisition from the soil environment, research examining whether and how belowground competition can influence the evolution of root traits remains largely unexplored. Here we examine the possibility that root traits may evolve as a target of selection from interspecific competition using Ipomoea purpurea and I. hederacea, two closely related morning glory species that commonly co-occur in the United States, as a model system. We show that belowground competitive interactions between the two species can alter the pattern of selection on root traits in each species. Specifically, competition with I. purpurea changes the pattern of selection on root angle in I. hederacea, and competitive interactions with I. hederacea change the pattern of selection on root size in I. purpurea. However, we did not uncover evidence that intraspecific competition altered the pattern of selection on any root traits within I. hederacea. Overall, our results suggest that belowground competition between closely related species can influence the phenotypic evolution of root traits in natural populations. Our findings provide a microevolutionary perspective of how competitive belowground interactions may impact plant fitness, potentially leading to patterns of plant community structure.

Parallel and nonparallel genomic responses contribute to herbicide resistance in Ipomoea purpurea, a common agricultural weed.

The repeated evolution of herbicide resistance has been cited as an example of genetic parallelism, wherein separate species or genetic lineages utilize the same genetic solution in response to selection. However, most studies that investigate the genetic basis of herbicide resistance examine the potential for changes in the protein targeted by the herbicide rather than considering genome-wide changes. We used a population genomics screen and targeted exome re-sequencing to uncover the potential genetic basis of glyphosate resistance in the common morning glory, Ipomoea purpurea, and to determine if genetic parallelism underlies the repeated evolution of resistance across replicate resistant populations. We found no evidence for changes in 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), glyphosate's target protein, that were associated with resistance, and instead identified five genomic regions that showed evidence of selection. Within these regions, genes involved in herbicide detoxification-cytochrome P450s, ABC transporters, and glycosyltransferases-are enriched and exhibit signs of selective sweeps. One region under selection shows parallel changes across all assayed resistant populations whereas other regions exhibit signs of divergence. Thus, while it appears that the physiological mechanism of resistance in this species is likely the same among resistant populations, we find patterns of both similar and divergent selection across separate resistant populations at particular loci.

The soil microbial community alters patterns of selection on flowering time and fitness-related traits in Ipomoea purpurea.

PREMISE: Plant flowering time plays an important role in plant fitness and thus evolutionary processes. Soil microbial communities are diverse and have a large impact, both positive and negative, on the host plant. However, owing to few available studies, how the soil microbial community may influence the evolutionary response of plant populations is not well understood. Here we sought to uncover whether belowground microbial communities act as an agent of selection on flowering and growth traits in the common morning glory, Ipomoea purpurea. METHODS: We performed a controlled greenhouse experiment in which genetic lines of I. purpurea were planted into either sterilized soils or in soils that were sterilized and inoculated with the microbial community from original field soil. We could thus directly test the influence of alterations to the microbial community on plant growth, flowering, and fitness and assess patterns of selection in both soil microbial environments. RESULTS: A more complex soil microbial community resulted in larger plants that produced more flowers. Selection strongly favored earlier flowering when plants were grown in the complex microbial environment than compared to sterilized soil. We also uncovered a pattern of negative correlational selection on growth rate and flowering time, indicating that selection favored different combinations of growth and flowering traits in the simplified versus complex soil community. CONCLUSIONS: Together, these results suggest the soil microbial community is a selective agent on flowering time and ultimately that soil microbial community influences important plant evolutionary processes.

The remarkable morphological diversity of leaf shape in sweet potato (Ipomoea batatas): the influence of genetics, environment, and G×E.

Leaf shape, a spectacularly diverse plant trait, varies across taxonomic levels, geography and in response to environmental differences. However, comprehensive intraspecific analyses of leaf shape variation across variable environments is surprisingly absent. Here, we performed a multilevel analysis of leaf shape using diverse accessions of sweet potato (Ipomoea batatas), and uncovered the role of genetics, environment, and G×E on this important trait. We examined leaf shape using a variety of morphometric analyses, and complement this with a transcriptomic survey to identify gene expression changes associated with shape variation. Additionally, we examined the role of genetics and environment on leaf shape by performing field studies in two geographically separate common gardens. We showed that extensive leaf shape variation exists within I. batatas, and identified promising candidate genes associated with this variation. Interestingly, when considering traditional measures, we found that genetic factors are largely responsible for most of leaf shape variation, but that the environment is highly influential when using more quantitative measures via leaf outlines. This extensive and multilevel examination of leaf shape shows an important role of genetics underlying a potentially important agronomic trait, and highlights that the environment can be a strong influence when using more quantitative measures of leaf shape.

Evolutionary and ecological insights from herbicide-resistant weeds: what have we learned about plant adaptation, and what is left to uncover?

The evolution of herbicide resistance in crop weeds presents one of the greatest challenges to agriculture and the production of food. Herbicide resistance has been studied for more than 60 yr, in the large part by researchers seeking to design effective weed control programs. As an outcome of this work, various unique questions in plant adaptation have been addressed. Here, I collate recent research on the herbicide-resistant problem in light of key questions and themes in evolution and ecology. I highlight discoveries made on herbicide-resistant weeds in three broad areas - the genetic basis of adaptation, evolutionary constraints, experimental evolution - and similarly discuss questions left to be answered. I then develop how one would use herbicide-resistance evolution as a model for studying eco-evolutionary dynamics within a community context. My overall goals are to highlight important findings in the weed science literature that are relevant to themes in plant adaptation and to stimulate the use of herbicide-resistant plants as models for addressing key questions within ecology and evolution.