Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae).

Phytochemical diversity is thought to result from coevolutionary cycles as specialization in herbivores imposes diversifying selection on plant chemical defenses. Plants in the speciose genus Erysimum (Brassicaceae) produce both ancestral glucosinolates and evolutionarily novel cardenolides as defenses. Here we test macroevolutionary hypotheses on co-expression, co-regulation, and diversification of these potentially redundant defenses across this genus. We sequenced and assembled the genome of E. cheiranthoides and foliar transcriptomes of 47 additional Erysimum species to construct a phylogeny from 9868 orthologous genes, revealing several geographic clades but also high levels of gene discordance. Concentrations, inducibility, and diversity of the two defenses varied independently among species, with no evidence for trade-offs. Closely related, geographically co-occurring species shared similar cardenolide traits, but not glucosinolate traits, likely as a result of specific selective pressures acting on each defense. Ancestral and novel chemical defenses in Erysimum thus appear to provide complementary rather than redundant functions.

Plants are often attacked by insects and other herbivores. As a result, they have evolved to defend themselves by producing many different chemicals that are toxic to these pests. As producing each chemical costs energy, individual plants often only produce one type of chemical that is targeted towards their main herbivore. Related species of plants often use the same type of chemical defense so, if a particular herbivore gains the ability to cope with this chemical, it may rapidly become an important pest for the whole plant family. To escape this threat, some plants have gained the ability to produce more than one type of chemical defense. Wallflowers, for example, are a group of plants in the mustard family that produce two types of toxic chemicals: mustard oils, which are common in most plants in this family; and cardenolides, which are an innovation of the wallflowers, and which are otherwise found only in distantly related plants such as foxglove and milkweed. The combination of these two chemical defenses within the same plant may have allowed the wallflowers to escape attacks from their main herbivores and may explain why the number of wallflower species rapidly increased within the last two million years. Züst et al. have now studied the diversity of mustard oils and cardenolides present in many different species of wallflower. This analysis revealed that almost all of the tested wallflower species produced high amounts of both chemical defenses, while only one species lacked the ability to produce cardenolides. The levels of mustard oils had no relation to the levels of cardenolides in the tested species, which suggests that the regulation of these two defenses is not linked. Furthermore, Züst et al. found that closely related wallflower species produced more similar cardenolides, but less similar mustard oils, to each other. This suggests that mustard oils and cardenolides have evolved independently in wallflowers and have distinct roles in the defense against different herbivores. The evolution of insect resistance to pesticides and other toxins is an important concern for agriculture. Applying multiple toxins to crops at the same time is an important strategy to slow the evolution of resistance in the pests. The findings of Züst et al. describe a system in which plants have naturally evolved an equivalent strategy to escape their main herbivores. Understanding how plants produce multiple chemical defenses, and the costs involved, may help efforts to breed crop species that are more resistant to herbivores and require fewer applications of pesticides.

The role of pollinators in floral diversification in a clade of generalist flowers.

Pollinator-mediated evolutionary divergence has seldom been explored in generalist clades because it is assumed that pollinators in those clades exert weak and conflicting selection. We investigate whether pollinators shape floral diversification in a pollination generalist plant genus, Erysimum. Species from this genus have flowers that appeal to broad assemblages of pollinators. Nevertheless, we recently reported that it is possible to sort plant species into pollination niches varying in the quantitative composition of pollinators. We test here whether floral characters of Erysimum have evolved as a consequence of shifts among pollination niches. For this, we quantified the evolutionary lability of the floral traits and their phylogenetic association with pollination niches. As with pollination niches, Erysimum floral traits show weak phylogenetic signal. Moreover, floral shape and color are phylogenetically associated with pollination niche. In particular, plants belonging to a pollination niche dominated by long-tongued large bees have lilac corollas with parallel petals. Further analyses suggest, however, that changes in color preceded changes in pollination niche. Pollinators seem to have driven the evolution of corolla shape, whereas the association between pollination niche and corolla color has probably arisen by lilac-flowered Erysimum moving toward certain pollination niches for other adaptive reasons.

Using complementary techniques to distinguish cryptic species: a new Erysimum (Brassicaceae) species from North Africa.

PREMISE OF THE STUDY: Cryptic species are superficially morphologically indistinguishable and therefore erroneously classified under one single name. The identification and delimitation of these species is usually a difficult task. The main aim of this study is to provide an inclusive methodology that combines standard and new tools to allow accurate identification of cryptic species. We used Erysimum nervosum s.l. as a model system. METHODS: Four populations belonging to E. nervosum s.l. were sampled at their two distribution ranges in Morocco (the Atlas Mountains and the Rif Mountains). Fifteen individuals per population were collected to assess standard taxonomic traits. Additionally, corolla color and shape were quantified in 30 individuals per population using spectrophotometry and geometric morphometrics, respectively. Finally, we collected tissue samples from each population per species to study the phylogenetic relationships among them. KEY RESULTS: Using the standard taxonomic traits, we could not distinguish the four populations. Nonetheless, there were differences in corolla color and shape between plants from the two mountain ranges. The population differentiation based on quantitative morphological differences were confirmed and supported by the phylogenetic relationships obtained for these populations and the rest of the Moroccan Erysimum species. CONCLUSIONS: The joint use of the results obtained from standard taxonomic traits, quantitative analyses of plant phenotype, and molecular data suggests the occurrence of two species within E. nervosum s.l. in Morocco, one located in the Atlas Mountains (E. nervosum s.s.) and the other in the Rif Mountains (E. riphaeanum sp. nov.). Consequently, we suggest that combining quantitative and molecular approaches with standard taxonomy greatly benefits the identification of cryptic species.