Summary1. Several theories have provided a framework for understanding variation in plant defence against herbivores. Among them, the plant apparency theory and the resource availability hypothesis (RAH) have aimed to explain the patterns of defence investment and the selective pressures that have led to the variety of defensive strategies across species. Here we provide a historical review of both theories, present evidence that shaped their development and contrast their predictions. 2. We present the results of a meta-analysis of the utility of the RAH 25 years after it was proposed and compare it to apparency theory. We performed a meta-analysis of 50 studies that have examined plant growth, defences and herbivory in relation to resource availability across latitude and ontogeny. Specifically, we tested four predictions that follow the RAH: (i) species adapted to resource-rich environments have intrinsically faster growth rates than species adapted to resourcepoor environments; (ii) fast-growing species have shorter leaf lifetimes than slow-growing species; (iii) fast-growing species have lower amounts of constitutive defences than slow-growing species; and (iv) fast-growing species support higher herbivory rates than slow-growing species. 3. Our results confirm the predictions that species adapted to resource-poor environments grow inherently more slowly, invest more in constitutive defences and support lower herbivory than species from more productive habitats. Our data also showed that variation in growth rate among species better explains the differences in herbivory than variation in apparency, suggesting that the evolution of different defensive strategies across species is resource, rather than herbivore driven. We also found that the application of this theory appears robust across latitude and ontogeny, as the magnitude of the effect sizes for most of the predictions did not vary significantly between ecosystems or across ontogenic stages. 4. We conclude that the RAH has served as a valid framework for investigating the patterns of plant defences and that its applicability is quite general.
Coevolutionary models suggest that herbivores drive diversification and community composition in plants. For herbivores, many questions remain regarding how plant defenses shape host choice and community structure. We addressed these questions using the tree genus and its lepidopteran herbivores in the Amazon. We constructed phylogenies for both plants and insects and quantified host associations and plant defenses. We found that similarity in herbivore assemblages between species was correlated with similarity in defenses. There was no correlation with phylogeny, a result consistent with our observations that the expression of defenses in is independent of phylogeny. Furthermore, host defensive traits explained 40% of herbivore community similarity. Analyses at finer taxonomic scales showed that different lepidopteran clades select hosts based on different defenses, suggesting taxon-specific histories of herbivore-host plant interactions. Finally, we compared the phylogeny and defenses of to phylogenies for the major lepidopteran clades. We found that closely related herbivores fed on with similar defenses rather than on closely related plants. Together, these results suggest that plant defenses might be more evolutionarily labile than the herbivore traits related to host association. Hence, there is an apparent asymmetry in the evolutionary interactions between and its herbivores. Although plants may evolve under selection by herbivores, we hypothesize that herbivores may not show coevolutionary adaptations, but instead "chase" hosts based on the herbivore's own traits at the time that they encounter a new host, a pattern more consistent with resource tracking than with the arms race model of coevolution.
Ecological theory predicts that the high local diversity observed in tropical forests is maintained by negative density–dependent interactions within and between closely related plant species. By using long-term data on tree growth and survival for coexisting Inga (Fabaceae, Mimosoideae) congeners, we tested two mechanisms thought to underlie negative density dependence (NDD): competition for resources and attack by herbivores. We quantified the similarity of neighbors in terms of key ecological traits that mediate these interactions, as well as the similarity of herbivore communities. We show that phytochemical similarity and shared herbivore communities are associated with decreased growth and survival at the sapling stage, a key bottleneck in the life cycle of tropical trees. None of the traits associated with resource acquisition affect plant performance, indicating that competition between neighbors may not shape local tree diversity. These results suggest that herbivore pressure is the primary mechanism driving NDD at the sapling stage.
We summarize work on a speciose Neotropical tree genus, Inga (Fabaceae), examining how interspecific variation in anti-herbivore defenses may have evolved, how defenses shape host choice by herbivores and how they might regulate community composition and influence species radiations. Defenses of expanding leaves include secondary metabolites, extrafloral nectaries, rapid leaf expansion, trichomes, and synchrony and timing of leaf production. These six classes of defenses are orthogonal, supporting independent evolutionary trajectories. Moreover, only trichomes show a phylogenetic signature, suggesting evolutionary lability in nearly all defenses. The interspecific diversity in secondary metabolite profiles does not arise from the evolution of novel compounds, but from novel combinations of common compounds, presumably due to changes in gene regulation. Herbivore host choice is determined by plant defensive traits, not host phylogeny. Neighboring plants escape each other's pests if their defenses differ enough, thereby enforcing the high local diversity typical of tropical forests. Related herbivores feed on hosts with similar defenses, implying that there are phylogenetic constraints placed on the herbivore traits that are associated with host use. Divergence in defensive traits among Inga appears to be driven by herbivore pressure. However, the lack of congruence between herbivore and host phylogeny suggests that herbivores are tracking defenses, choosing hosts based on traits for which they already have adaptations. There is, therefore, an asymmetry in the host-herbivore evolutionary arms race.
Nicole M. van Dam and Roberto Salguero-Gómez joint last authorship.
Summary1. Classic theory in plant-insect interactions has linked herbivore pressure with diversification in plant species. We hypothesize that herbivores may exert divergent selection on defences, such that closely related plant species will be more different in defensive than in non-defensive traits. 2. We evaluated this hypothesis by investigating two clades of closely related plant species coexisting at a single site in the Peruvian Amazon: Inga capitata Desv. and Inga heterophylla Willd. species complexes. We compared how these lineages differ in the suite of chemical, biotic, phenological and developmental defences as compared to non-defensive traits that are related to habitat use and resource acquisition. We also collected insect herbivores feeding on the plants. 3. Our data show that sister lineages within both species complexes are more divergent in antiherbivore defences than in other non-defensive, functional traits. Moreover, the assemblages of herbivore communities are dissimilar between the populations of coexisting I. capitata lineages. 4. Synthesis. Our results are consistent with the idea that for the I. capitata and I. heterophylla species complexes, interactions with their natural enemies may have played a significant role in their phenotypic divergence and potentially in their diversification and coexistence. It also suggests that defensive traits are evolutionary labile.
Two opposing niche processes have been shown to shape the relationship between ecological traits and species distribution patterns: habitat filtering and competitive exclusion. Habitat filtering is expected to select for similar traits among coexisting species that share similar habitat conditions, whereas competitive exclusion is expected to limit the ecological similarity of coexisting species leading to trait differentiation. Here, we explore how functional traits vary among 19 understory palm species that differ in their distribution across a gradient of soil resource availability in lower montane forest in western Panama. We found evidence that habitat filtering influences species distribution patterns and shifts community-wide and intraspecific trait values. Differences in trait values among sites were more strongly related to soil nutrient availability than to variation in light or rainfall. Soil nutrient availability explained a significant amount of variation in site mean trait values for 4 of 15 functional traits. Site mean values of leaf nitrogen and phosphorus increased 37 and 64%, respectively, leaf carbon:nitrogen decreased 38%, and specific leaf area increased 29% with increasing soil nutrient availability. For Geonoma cuneata, the only species occurring at all sites, leaf phosphorus increased 34% and nitrogen:phosphorus decreased 42% with increasing soil nutrients. In addition to among-site variation, most morphological and leaf nutrient traits differed among coexisting species within sites, suggesting these traits may be important for niche differentiation. Hence, a combination of habitat filtering due to turnover in species composition and intraspecific variation along a soil nutrient gradient and site-specific niche differentiation among co-occurring species influences understory palm community structure in this lower montane forest.
Selective pressures imposed by herbivores are often positively correlated with investments that plants make in defense. Research based on the framework of an evolutionary arms race has improved our understanding of why the amount and types of defenses differ between plant species. However, plant species are exposed to different selective pressures during the life of a leaf, such that expanding leaves suffer more damage from herbivores and pathogens than mature leaves. We hypothesize that this differential selective pressure may result in contrasting quantitative and qualitative defense investment in plants exposed to natural selective pressures in the field. To characterize shifts in chemical defenses, we chose six species of Inga, a speciose Neotropical tree genus. Focal species represent diverse chemical, morphological, and developmental defense traits and were collected from a single site in the Amazonian rainforest. Chemical defenses were measured gravimetrically and by characterizing the metabolome of expanding and mature leaves. Quantitative investment in phenolics plus saponins, the major classes of chemical defenses identified in Inga, was greater for expanding than mature leaves (46% and 24% of dry weight, respectively). This supports the theory that, because expanding leaves are under greater selective pressure from herbivores, they rely more upon chemical defense as an antiherbivore strategy than do mature leaves. Qualitatively, mature and expanding leaves were distinct and mature leaves contained more total and unique metabolites. Intraspecific variation was greater for mature leaves than expanding leaves, suggesting that leaf development is canalized. This study provides a snapshot of chemical defense investment in a speciose genus of tropical trees during the short, few‐week period of leaf development. Exploring the metabolome through quantitative and qualitative profiling enables a more comprehensive examination of foliar chemical defense investment.
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