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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 F 2 progeny was generated by crossing Datura stramonium (Solanaceae) parents from two populations differing in their level of chemical defense. This F 2 progeny was reciprocally transplanted into the parental plants' habitats and by measuring the identity by descent (IBD) relationship of each F 2 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.

Tropane alkaloids and terpenoids are widely used in the medicine and pharmaceutic industry and evolved as chemical defenses against herbivores and pathogens in the annual herb Datura stramonium (Solanaceae). Here, we present the first draft genomes of two plants from contrasting environments of D. stramonium. Using these de novo assemblies, along with other previously published genomes from 11 Solanaceae species, we carried out comparative genomic analyses to provide insights on the genome evolution of D. stramonium within the Solanaceae family, and to elucidate adaptive genomic signatures to biotic and abiotic stresses in this plant. We also studied, in detail, the evolution of four genes of D. stramonium—Putrescine N-methyltransferase, Tropinone reductase I, Tropinone reductase II and Hyoscyamine-6S-dioxygenase—involved in the tropane alkaloid biosynthesis. Our analyses revealed that the genomes of D. stramonium show signatures of expansion, physicochemical divergence and/or positive selection on proteins related to the production of tropane alkaloids, terpenoids, and glycoalkaloids as well as on R defensive genes and other important proteins related with biotic and abiotic pressures such as defense against natural enemies and drought.

Elucidating the diversification process of congeneric species makes it necessary to identify the factors promoting species variation and diversification. Comparative gene family analysis allows us to elucidate the evolutionary history of species by identifying common genetic/genomic mechanisms underlying species responses to biotic and abiotic environments at the genomic level. In this study, we analyzed the high-quality transcriptomes of four Datura species, D. inoxia, D. pruinosa, D. stramonium, and D. wrightii. We performed a thorough comparative gene family analysis to infer the role of selection in molecular variation, changes in protein physicochemical properties, and gain/loss of genes during their diversification processes. The results revealed common and species-specific signals of positive selection, physicochemical divergence and/or expansion of metabolic genes (e.g., transferases and oxidoreductases) associated with terpene and tropane metabolism and some resistance genes (R genes). The gene family analysis presented here is a valuable tool for understanding the genome evolution of economically and ecologically significant taxa such as the Solanaceae family.

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Background Plants have evolved physical–chemical defense to prevent/diminish damage by their enemies. Chemical defense involves the synthesis’ pathways of specialized toxic, repellent, or anti-nutritive metabolites to herbivores. Molecular evolutionary studies have revealed the origin of new genes, acquisition and functional diversification along time in different plant lineages. Methods Using bioinformatic tools we analyze gene divergence of tropane alkaloids (TAs) and terpene synthases (TPSs) in Datura stramonium and other species of Solanaceae; compared gene and amino acids sequence of TAs and TPSs on genomes, cDNA and proteins sequences of Viridiplantae. We analyzed two recently assembled genomes of D. stramonium (Ticumán and Teotihuacán), transcriptomes of Datura metel and genomes of other Solanaceae. Hence, we analyzed variation of TAs and TPSs to infer genes involved in plant defense and plant responses before stress. We analyzed protein modeling and molecular docking to predict interactions between H6H and ligand; we translated the sequences (Teo19488, Tic8550 and Tic8549) obtained from the two genomes of D. stramonium by using Swiss-Model and Ramachandran plot and MolProbity structure validation of Teo19488 protein model. Results For TAs, we detected an expansion event in the tropinone reductase II (TRII) and the ratio synonymous/non-synonymous substitutions indicate positive selection. In contrast, a contraction event and negative selection was detected in tropinone reductase I (TRI). In Hy-oscyamine 6 b-hydroxylase (H6H), enzyme involved in the production of tropane alkaloids atropine and scopolamine, the synonymous/non-synonymous substitution ratio in its dominion indicates positive selection. For terpenes (TPS), we found 18 DsTPS in D. stramomiun and seven in D. metel; evolutionary analyses detected positive selection in TPS10.1 and TPS10.2 of D. stramonium and D. metel. Comparison of copies of TPSs in D. stramonium detected variation among them in the binding site. Duplication events and differentiation of TAs and TPSs of D. stramonium, as compared to other Solanaceae, suggest their possible involvement on adaptive evolution of defense to herbivores. Protein modeling and docking show that the three protein structures obtained of DsH6H from Teo19488, Tic-8550 and Tic8549 maintain the same interactions and the union site of 2OG-FeII_Oxy with the Hy-o ligand as in 6TTM of D. metel. Conclusion Our results indicate differences in the number of gene copies involved in the synthesis of tropane alkaloids, between the genomes of D. stramonium from two Mexican populations. More copies of genes related to the synthesis of tropane alkaloids (TRI, TRII, H6H, PMT) are found in D. stramonium as compared to Viridiplantae. Likewise, for terpene synthases (TPS), TPS-10 is duplicated in D. stramonium and D. metel. Further studies should be directed to experimentally assess gain (overexpression) or loss (silencing) of function of duplicated genes.

One of the basics and fundamentals problems in ecology is understand the factors that shape the spatial patterns in the distribution of the species and the coexistence of close relatives species. Among the most important factors governing the distributions and the coexistence of species are the spatiotemporal changes occurring in the microhabitat heterogeneity. Here, we assessed the heterogeneity of microhabitats and how they have an effect in the spatial segregation of two species of small mammals (i. e., Peromyscus difficilis and P. melanotis), which coexist in a temperate, mixed forest. We evaluated the microhabitat heterogeneity through multivariate statistics, using onto 23 habitat variables for vertical-horizontal habitat structure along pluvial seasons. To detect specific microdistribution changes and habitat preferences by two species of small mammals, we used second order spatial statistics and general linear models. According to their respective morphology and locomotive adaptations, the middle sized, midscansorial P. difficilis was resident all year long and preferred microhabitats with a high log ground cover, while the opportunistic, small sized, cursorial P. melanotis changed its occupancy area, depending on density of herbaceous and woody plants cover. Under the more benign microhabitat conditions of rainy season (denser plant coverage, milder temperature), both species showed closer microdistribution patterns; while these became repulsive at the less benign conditions of dry season (scarcer plant cover, colder temperature). Thus, we could confirm that seasonal changes of microhabitat heterogeneity promoted Peromyscus coexistence, through dispersion patterns reflecting partition of microhabitat resources.

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