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Tolerance and resistance are two different plant defense strategies against herbivores. Empirical evidence in natural populations reveals that individual plants allocate resources simultaneously to both strategies, thus plants exhibit a mixed pattern of defense. In this review we examine the conditions that promote the evolutionary stability of mixed defense strategies in the light of available empirical and theoretical evidence. Given that plant tolerance and resistance are heritable and subject to environmentally dependent selection and genetic constraints, the joint evolution of tolerance and resistance is analyzed, with consideration of multiple species interactions and the plant mating system. The existence of mixed defense strategies in plants makes it necessary to re-explore the coevolutionary process between plants and herbivores, which centered historically on resistance as the only defensive mechanism. In addition, we recognize briefly the potential use of plant tolerance for pest management. Finally, we highlight unresolved issues for future development in this field of evolutionary ecology.

Theory predicts patterns of defense across taxa based on notions of tradeoffs and synergism among defensive traits when plants and herbivores coevolve. Because the expression of characters changes ontogenetically, the evolution of plant strategies may be best understood by considering multiple traits along a trajectory of plant development. Here we addressed the ontogenetic expression of chemical and physical defenses in 12 Datura species, and tested for macroevolutionary correlations between defensive traits using phylogenetic analyses. We used liquid chromatography coupled to mass spectrometry to identify the toxic tropane alkaloids of Datura, and also estimated leaf trichome density. We report three major patterns. First, we found different ontogenetic trajectories of alkaloids and leaf trichomes, with alkaloids increasing in concentration at the reproductive stage, whereas trichomes were much more variable across species. Second, the dominant alkaloids and leaf trichomes showed correlated evolution, with positive and negative associations. Third, the correlations between defensive traits changed across ontogeny, with significant relationships only occurring during the juvenile phase. The patterns in expression of defensive traits in the genus Datura are suggestive of adaptation to complex selective environments varying in space and time.

Knowing how species and communities respond to environmental change is fundamental in the context of climate change. The search for patterns of abundance and phenotypic variation along altitudinal gradients can provide evidence on adaptive limits. We evaluated the species abundance and the variation in morphometric and stomatal characters in five tree ferns species ( Cyathea fulva , C . divergens , C . myosuroides , Alsophila firma and Gymnosphaera salvinii ) distributed along an elevation gradient in a well-preserved Mexican cloud forest. Variation at the community and species level was assessed using exploratory and multivariate data analysis methods. We wanted to explore if the species abundance is environmentally determined, to determine the degree of variation along the elevation gradient, to test for differences between zones and associations with elevation, humidity and soil nutrients, and to assess contribution of the intra- and interspecific variation to the community response to elevation and soil nutrients. The studied fern community showed strong species turnover along the elevation gradient, with some influence of soil nutrient concentration, supporting environmental determinism. All measured characters displayed variation along the gradient. Stomatal characters (size and density) had significantly less variation than morphometric characters (trunk diameter, stipe length and blade length), but stomatal density also shows interesting intraspecific patterns. In general, patterns within the fern community suggest a strong influence of species identity, especially of species inhabiting the lower edge of the cloud forest, which showed the clearest morphometric and stomatal patterns, associated to contrasting environments rather than to changes in elevation. The coincidence between morphometric and stomatal patterns in this area suggest hydraulic adjustments in response to contrasting environments. Our results provide evidence that tree ferns species respond to environmental changes through adjustments of morphometric plasticity and stomatal density, which is relevant to predict possible responses to variation in environmental conditions resulting from climate change.

Intraspecific variation is a major component of biodiversity, yet it has received relatively little attention from governmental and nongovernmental organizations, especially with regard to conservation plans and the management of wild species. This omission is ill‐advised because phenotypic and genetic variations within and among populations can have dramatic effects on ecological and evolutionary processes, including responses to environmental change, the maintenance of species diversity, and ecological stability and resilience. At the same time, environmental changes associated with many human activities, such as land use and climate change, have dramatic and often negative impacts on intraspecific variation. We argue for the need for local, regional, and global programs to monitor intraspecific genetic variation. We suggest that such monitoring should include two main strategies: (i) intensive monitoring of multiple types of genetic variation in selected species and (ii) broad‐brush modeling for representative species for predicting changes in variation as a function of changes in population size and range extent. Overall, we call for collaborative efforts to initiate the urgently needed monitoring of intraspecific variation.

Differential expression of genes is key to mediating developmental and stress‐related plant responses. Here, we addressed the regulation of plant metabolic responses to biotic stress and the developmental variation of defense‐related genes in four species of the genus Datura with variable patterns of metabolite accumulation and development. We combine transcriptome profiling with phylogenomic techniques to analyze gene expression and coexpression in plants subjected to damage by a specialist folivore insect. We found (1) common overall gene expression in species of similar chemical profiles, (2) species‐specific responses of proteins involved in specialized metabolism, characterized by constant levels of gene expression coupled with transcriptional rearrangement, and (3) induction of transcriptional rearrangement of major terpene and tropane alkaloid genes upon herbivory. Our results indicate differential modulation of terpene and tropane metabolism linked to jasmonate signaling and specific transcription factors to regulate developmental variation and stress programs, and suggest plastic adaptive responses to cope with herbivory. The transcriptional profiles of specialized metabolism shown here reveal complex genetic control of plant metabolism and contribute to understanding the molecular basis of adaptations and the physiological variation of significant ecological traits. The transcriptional profiles of specialized metabolism shown here reveal complex genetic control of plant metabolism and contribute to understanding the molecular basis of adaptations and the physiological variation of significant ecological traits.

Because most species are collections of genetically variable populations distributed to habitats differing in their abiotic/biotic environmental factors and community composition, the pattern and strength of natural selection imposed by species on each other’s traits are also expected to be highly spatially variable. Here, we used genomic and quantitative genetic approaches to understand how spatially variable selection operates on the genetic basis of plant defenses to herbivores. To this end, an F₂ progeny was generated by crossing Datura stramonium (Solanaceae) parents from two populations differing in their level of chemical defense. This F₂ progeny was reciprocally transplanted into the parental plants’ habitats and by measuring the identity by descent (IBD) relationship of each F₂ plant to each parent, we were able to elucidate how spatially variable selection imposed by herbivores operated on the genetic background (IBD) of resistance to herbivory, promoting local adaptation. The results highlight that plants possessing the highest total alkaloid concentrations (sum of all alkaloid classes) were not the most well-defended or fit. Instead, specific alkaloids and their linked loci/alleles were favored by selection imposed by different herbivores. This has led to population differentiation in plant defenses and thus, to local adaptation driven by plant-herbivore interactions.

Natural enemies of herbivore insects can change the arms race between plants and insects. Their presence and abundance even can affect the co-evolution of interacting species. The annual herb varies geographically in the extent of its direct defenses against herbivores. Its main specialist herbivore, , is adapted to cope with these defenses, but little is known about its natural enemies. Here, we determined the presence and incidence of parasitoids as an initial step to explore other ecological and evolutionary relationships in a tri-trophic context. Field collections of eggs and larvae were performed during the summers of 2018 and 2019 in eleven natural populations of in central Mexico. We recorded their development to evaluate the emergence of parasitoids and their relationship with the abundance of herbivore individuals and environmental variables in each locality. We found six parasitoid fly and wasp species that are new records for Mexico or the host. Throughout their distribution, the interaction varies widely among populations and years. In some localities, egg parasitoids dominate over larval parasitoids and vice versa, and they exert strong pressures on the survival of s populations. The abundance of , the egg parasitoid, is related to the clutch size of and climatic conditions such as temperature, altitude, and precipitation. As an apparent defense strategy against parasitoid flies, larvae of release their oral secretions, which contain alkaloids from . At a geographic scale, these findings change the scenario between the plant-herbivore interaction and open the field to explore the different selective pressures among populations.

The expression of plant resistance traits against arthropod herbivores often comes with costs to other essential plant functions such as growth and fitness. These trade‐offs are shaped by the allocation of limited resources. However, plants might also possess the capability to allocate resources to both resistance and growth, thereby ensuring their survival when under herbivore attacks. Additionally, the extent of damage caused by herbivores could vary across different years or seasons, subsequently impacting plant performance. In this study, we aimed to investigate how the annual variations in herbivore abundance and damage levels affect plant performance. We generated F2 progeny through a cross between two populations of the annual herb Datura stramonium (Solanaceae). These populations are known to have differing levels of chemical defense and herbivory. These F2 plants were cultivated in a common natural environment for two consecutive years (2017 and 2018). Our findings reveal that plants with higher resistance, attained higher seed production but this trend was evident only during 2018. This relationship coincided with a five‐fold increase in the abundance of Lema daturaphila (Chrysomelidae) larvae in 2018. Indeed, the plants experienced a 13‐fold increase in damage during this second year of study. Furthermore, our results indicated that there was no trade‐off between resistance, growth, and fitness in either of the 2 years. In contrast, during 2018, when plants faced stronger herbivore pressure, they allocated all available nutritional resources to enhance both resistance and growth. Our study highlights how the selection for plant resistance is dependent upon the inter‐annual variation in herbivore abundance. The study underscores the influential role of specific herbivores in driving plant resistance and offers fresh insights into the inter‐annual evolutionary dynamics of plant resistance.

Agricultural losses brought about by insect herbivores can be reduced by understanding the strategies that plants use against insect herbivores. The two main strategies that plants use against herbivory are resistance and tolerance. They are, however, predicted to be mutually exclusive, yet numerous populations have them both (hence a mixed defense strategy). This has been explained, among other alternatives, by the non-linear behavior of the costs and benefits of resistance and tolerance and their interaction with plants’ mating system. Here, we studied how non-linearity and mating system affect the evolutionary stability of mixed defense strategies by means of agent-based model simulations. The simulations work on a novel model that was built upon previous ones. It incorporates resistance and tolerance costs and benefits, inbreeding depression, and a continuously scalable non-linearity. The factors that promoted the evolutionary stability of mixed defense strategies include a multiplicative allocation of costs and benefits of resistance and tolerance, a concave non-linearity, non-heritable selfing, and high tolerance costs. We also found new mechanisms, enabled by the mating system, that are worth considering for empirical studies. One was a double trade-off between resistance and tolerance, predicted as a consequence of costs duplication and the inducibility of tolerance, and the other was named the resistance-cost-of-selfing, a term coined by us, and was derived from the duplication of costs that homozygous individuals conveyed when a single resistance allele provided full protection.

Plant mating system determines, to a great extent, the demographic and genetic properties of populations, hence their potential for adaptive evolution. Variation in plant mating system has been documented between phylogenetically related species as well between populations of a species. A common evolutionary transition, from outcrossing to selfing, is likely to occur under environmental spatial variation in the service of pollinators. Here, we studied two phenotypically (in floral traits) and genetically (in neutral molecular markers) differentiated populations of the annual, insect-pollinated, plant Datura inoxia in Mexico, that differ in the service of pollinators (Mapimí and Cañada Moreno). First, we determined the populations’ parameters of phenotypic in herkogamy, outcrossing and selfing rates with microsatellite loci, and assessed between generation (adults and seedlings) inbreeding, and inbreeding depression. Second, we compared the relationships between parameters in each population. Results point strong differences between populations: plants in Mapimí have, on average, approach herkogamy, higher outcrossing rate ( t m = 0.68), lower primary selfing rate ( r = 0.35), and lower inbreeding at equilibrium ( F e = 0.24) and higher inbreeding depression (δ = 0.25), than the populations of Cañada. Outcrossing seems to be favored in Mapimí while selfing in Cañada. The relationship between r and F e were negatively associated with herkogamy in Mapimí; here, progenies derived from plants with no herkogamy or reverse herkogamy had higher selfing rate and inbreeding coefficient than plants with approach herkogamy. The difference F e – F is positively related to primary selfing rate ( r ) only in Cañada Moreno which suggests inbreeding depression in selfing individuals and then genetic purging. In conclusion, mating system evolution may occur differentially among maternal lineages within populations of Datura inoxia , in which approach herkogamy favors higher outcrossing rates and low levels of inbreeding and inbreeding depression, while no herkogamy or reverse herkogamy lead to the evolution of the “selfing syndrome” following the purge of deleterious alleles despite high inbreeding among individuals.