Can genetically based clines in plant defence explain greater herbivory at higher latitudes?

Greater plant defence is predicted to evolve at lower latitudes in response to increased herbivore pressure. However, recent studies question the generality of this pattern. In this study, we tested for genetically based latitudinal clines in resistance to herbivores and underlying defence traits of Oenothera biennis. We grew plants from 137 populations from across the entire native range of O. biennis. Populations from lower latitudes showed greater resistance to multiple specialist and generalist herbivores. These patterns were associated with an increase in total phenolics at lower latitudes. A significant proportion of the phenolics were driven by the concentrations of two major ellagitannins, which exhibited opposing latitudinal clines. Our analyses suggest that these findings are unlikely to be explained by local adaptation of herbivore populations or genetic variation in phenology. Rather greater herbivory at high latitudes can be explained by latitudinal clines in the evolution of plant defences.

Macroevolution of plant defenses against herbivores in the evening primroses.

Plant species vary greatly in defenses against herbivores, but existing theory has struggled to explain this variation. Here, we test how phylogenetic relatedness, tradeoffs, trait syndromes, and sexual reproduction affect the macroevolution of defense. To examine the macroevolution of defenses, we studied 26 Oenothera (Onagraceae) species, combining chemistry, comparative phylogenetics and experimental assays of resistance against generalist and specialist herbivores. We detected dozens of phenolic metabolites within leaves, including ellagitannins (ETs), flavonoids, and caffeic acid derivatives (CAs). The concentration and composition of phenolics exhibited low to moderate phylogenetic signal. There were clear negative correlations between multiple traits, supporting the prediction of allocation tradeoffs. There were also positively covarying suites of traits, but these suites did not strongly predict resistance to herbivores and thus did not act as defensive syndromes. By contrast, specific metabolites did correlate with the performance of generalist and specialist herbivores. Finally, that repeated losses of sex in Oenothera was associated with the evolution of increased flavonoid diversity and altered phenolic composition. These results show that secondary chemistry has evolved rapidly during the diversification of Oenothera. This evolution has been marked by allocation tradeoffs between traits, some of which are related to herbivore performance. The repeated loss of sex appears also to have constrained the evolution of plant secondary chemistry, which may help to explain variation in defense among plants.

Sesquiterpene lactone stereochemistry influences herbivore resistance and plant fitness in the field.

BACKGROUND AND AIMS: Stereochemical variation is widely known to influence the bioactivity of compounds in the context of pharmacology and pesticide science, but our understanding of its importance in mediating plant-herbivore interactions is limited, particularly in field settings. Similarly, sesquiterpene lactones are a broadly distributed class of putative defensive compounds, but little is known about their activities in the field. METHODS: Natural variation in sesquiterpene lactones of the common cocklebur, Xanthium strumarium (Asteraceae), was used in conjunction with a series of common garden experiments to examine relationships between stereochemical variation, herbivore damage and plant fitness. KEY RESULTS: The stereochemistry of sesquiterpene lactone ring junctions helped to explain variation in plant herbivore resistance. Plants producing cis-fused sesquiterpene lactones experienced significantly higher damage than plants producing trans-fused sesquiterpene lactones. Experiments manipulating herbivore damage above and below ambient levels found that herbivore damage was negatively correlated with plant fitness. This pattern translated into significant fitness differences between chemotypes under ambient levels of herbivore attack, but not when attack was experimentally reduced via pesticide. CONCLUSIONS: To our knowledge, this work represents only the second study to examine sesquiterpene lactones as defensive compounds in the field, the first to document herbivore-mediated natural selection on sesquiterpene lactone variation and the first to investigate the ecological significance of the stereochemistry of the lactone ring junction. The results indicate that subtle differences in stereochemistry may be a major determinant of the protective role of secondary metabolites and thus of plant fitness. As stereochemical variation is widespread in many groups of secondary metabolites, these findings suggest the possibility of dynamic evolutionary histories within the Asteraceae and other plant families showing extensive stereochemical variation.

Does phylogeny matter? Assessing the impact of phylogenetic information in ecological meta-analysis.

Meta-analysis is increasingly used in ecology and evolutionary biology. Yet, in these fields this technique has an important limitation: phylogenetic non-independence exists among taxa, violating the statistical assumptions underlying traditional meta-analytic models. Recently, meta-analytical techniques incorporating phylogenetic information have been developed to address this issue. However, no syntheses have evaluated how often including phylogenetic information changes meta-analytic results. To address this gap, we built phylogenies for and re-analysed 30 published meta-analyses, comparing results for traditional vs. phylogenetic approaches and assessing which characteristics of phylogenies best explained changes in meta-analytic results and relative model fit. Accounting for phylogeny significantly changed estimates of the overall pooled effect size in 47% of datasets for fixed-effects analyses and 7% of datasets for random-effects analyses. Accounting for phylogeny also changed whether those effect sizes were significantly different from zero in 23 and 40% of our datasets (for fixed- and random-effects models, respectively). Across datasets, decreases in pooled effect size magnitudes after incorporating phylogenetic information were associated with larger phylogenies and those with stronger phylogenetic signal. We conclude that incorporating phylogenetic information in ecological meta-analyses is important, and we provide practical recommendations for doing so.

Ellagitannins Inhibit the Exsheathment of Haemonchus contortus and Trichostrongylus colubriformis Larvae: The Efficiency Increases Together with the Molecular Size.

Worldwide, parasitic gastrointestinal nematodes continue to threaten animal health, welfare, and production in outdoor breeding systems of small ruminants. For more than 50 years, the control of these parasitic worms has relied on the use of commercial synthetic anthelmintics. However, anthelmintic resistance in worm populations is nowadays widespread and requires novel solutions. The use of tannin-rich plants has been suggested as an alternative to synthetic anthelmintics to control gastrointestinal nematodes. The majority of previous studies have focused on the activity of proanthocyanidins (syn condensed tannins), and less is known about ellagitannins. In this study, the effects of 30 structurally unique ellagitannins on the exsheathment of third-stage infective larvae were examined on Haemonchus contortus and Trichostrongylus colubriformis by the in vitro larval exsheathment inhibition assay. Ellagitannins were found to be promising natural anthelmintics as they showed direct inhibition on larval exsheathment for both nematode species. In general, ellagitannins were more efficient at inhibiting the exsheathment of H. contortus larvae than those of T. colubriformis. The efficiency of inhibition increased as the degree of oligomerization or the molecular weight of the ellagitannin increased. Otherwise, we found no other structural features of ellagitannins that significantly affected the anthelmintic activity on the third-stage infective larvae. The effective concentrations were physiologically relevant and should be achievable in the gastrointestinal tract also in in vivo conditions.

Correlates of hybridization in plants.

Hybridization is a biological phenomenon increasingly recognized as an important evolutionary process in both plants and animals, as it is linked to speciation, radiation, extinction, range expansion and invasion, and allows for increased trait diversity in agricultural and horticultural systems. Estimates of hybridization frequency vary across taxonomic groups, but causes of this variation are unknown. Here, we ask on a global scale whether hybridization is linked to any of 11 traits related to plant life history, reproduction, genetic predisposition, and environment or opportunity. Given that hybridization is not evenly distributed across the plant tree of life, we use phylogenetic generalized least squares regression models and phylogenetic path analysis to detect statistical associations between hybridization and plant traits at both the family and genus levels. We find that perenniality and woodiness are each weakly associated with an increased frequency of hybridization in univariate analyses, but path analysis suggests that the direct linkage is between perenniality and increased hybridization (with woodiness having only an indirect relationship with hybridization via perenniality). Weak associations between higher rates of hybridization and higher outcrossing rates, abiotic pollination syndromes, vegetative reproductive modes, larger genomes, and less variable genome sizes are detectable in some cases but not others. We argue that correlational evidence at the global scale, such as that presented here, provides a robust framework for forming hypotheses to examine and test drivers of hybridization at a more mechanistic level.

Testing for latitudinal gradients in defense at the macroevolutionary scale.

Plant defenses against herbivores are predicted to evolve to be greater in warmer climates, such as lower latitudes where herbivore pressure is also thought to be higher. Instead, recent findings are often inconsistent with this expectation, suggesting alternative hypotheses are needed. We tested for latitudinal gradients in plant defense evolution at the macroevolutionary scale by characterizing plant chemical defenses across 80 species of the evening primroses, spanning both North and South America. We quantified phenolics in leaves, flowers, and fruits, using advanced analytical chemistry techniques. Dominant individual ellagitannin compounds, total concentrations of ellagitannins, flavonoids, total phenolics, and compound diversity were quantified. Variation in these compounds was predicted with latitude, temperature, precipitation, and continent using phylogenetic generalized least squares (PGLS) multiple regression models. Latitude did not strongly explain variation in chemical defenses. Instead, fruit total ellagitannins, oenothein A, and total phenolics were greater in species inhabiting regions with colder climates. Using analytical chemistry and 80 species in two continents, we show that contrary to classic predictions, concentrations of secondary metabolites are not greater at lower latitudes or in warmer regions. We propose higher herbivore pressure in colder climates and gradients in resource availability as potential drivers of the observed patterns in Oenothera.

Polyphenols in strawberry (Fragaria × ananassa) leaves induced by plant activators.

Strawberry leaves contain high amounts of diverse phenolic compounds potentially possessing defensive activities against microbial pathogens and beneficial properties for human health. In this work, young strawberry plants were treated with two plant activators, S-methylbenzo-1,2,3-thaidiazole-7-carbothiate (BTH) and birch wood distillate. Phenolic compounds from activator-treated and control leaves were subjected to quantitative analyses by HPLC-DAD, HPLC-ESI-MS, and microQTOF ESI-MS. Thirty-two different phenolic compounds were detected and characterized, and 21 different ellagitannins constituted the largest group of compounds in the strawberry leaves (37.88-45.82 mg/g dry weight, 47.0-54.3% of total phenolics). Treatment with BTH resulted in higher levels of individual ellagitannins, whereas treatment with birch wood distillate strongly increased the levels of chlorogenic acid in strawberry leaves compared with the control. The results suggest that different plant activators may be useful tools for the activation of different branches in the phenylpropanoid biosynthesis in strawberry.