RESUMO
Plant secondary metabolites play important ecological and evolutionary roles, most notably in the deterrence of natural enemies. The classical theory explaining the evolution of plant chemical diversity is that new defences arise through a pairwise co-evolutionary arms race between plants and their specialized natural enemies. However, plant species are bombarded by dozens of different herbivore taxa from disparate phylogenetic lineages that span a wide range of feeding strategies and have distinctive physiological constraints that interact differently with particular plant metabolites. How do plant defence chemicals evolve under such multiple and potentially contrasting selective pressures imposed by diverse herbivore communities? To tackle this question, we exhaustively characterized the chemical diversity and insect herbivore fauna from 31 sympatric species of Amazonian Protieae (Burseraceae) trees. Using a combination of phylogenetic, metabolomic and statistical learning tools, we show that secondary metabolites that were associated with repelling herbivores (1) were more frequent across the Protieae phylogeny and (2) were found in average higher abundance than other compounds. Our findings suggest that generalist herbivores can play an important role in shaping plant chemical diversity and support the hypothesis that chemical diversity can also arise from the cumulative outcome of multiple diffuse interactions.
Assuntos
Burseraceae/química , Evolução Molecular , Cadeia Alimentar , Herbivoria , Insetos/fisiologia , Metaboloma , Animais , Burseraceae/classificação , Metabolômica , Modelos Estatísticos , Peru , Filogenia , Árvores/química , Árvores/classificaçãoRESUMO
Herbivores are often implicated in the generation of the extraordinarily diverse tropical flora. One hypothesis linking enemies to plant diversification posits that the evolution of novel defenses allows plants to escape their enemies and expand their ranges. When range expansion involves entering a new habitat type, this could accelerate defense evolution if habitats contain different assemblages of herbivores and/or divergent resource availabilities that affect plant defense allocation. We evaluated this hypothesis by investigating two sister habitat specialist ecotypes of Protium subserratum (Burseraceae), a common Amazonian tree that occurs in white-sand and terra firme forests. We collected insect herbivores feeding on the plants, assessed whether growth differences between habitats were genetically based using a reciprocal transplant experiment, and sampled multiple populations of both lineages for defense chemistry. Protium subserratum plants were attacked mainly by chrysomelid beetles and cicadellid hemipterans. Assemblages of insect herbivores were dissimilar between populations of ecotypes from different habitats, as well as from the same habitat 100 km distant. Populations from terra firme habitats grew significantly faster than white-sand populations; they were taller, produced more leaf area, and had more chlorophyll. White-sand populations expressed more dry mass of secondary compounds and accumulated more flavone glycosides and oxidized terpenes, whereas terra firme populations produced a coumaroylquinic acid that was absent from white-sand populations. We interpret these results as strong evidence that herbivores and resource availability select for divergent types and amounts of defense investment in white-sand and terra firme lineages of Protium subserratum, which may contribute to habitat-mediated speciation in these trees.
Assuntos
Evolução Biológica , Burseraceae/fisiologia , Ecossistema , Insetos/fisiologia , Animais , Brasil , Burseraceae/química , Burseraceae/genética , Herbivoria , Densidade Demográfica , Solo , ÁrvoresRESUMO
Protium subserratum (Burseraceae) is a neotropical tree species that is comprised of several habitat-specific ecotypes having distinct defense chemical profiles. A previously unknown triterpene, 25,30-dicarboxy-26,27,28,29-tetraacetoxy-10,11,14,15-tetrahydrosqualene, was isolated from P. subserratum young leaf tissue of one ecotype growing in Peru. The structure of 1 was determined by spectroscopic study, including 1 and 2D nuclear magnetic resonance experiments.
Assuntos
Burseraceae/química , Esqualeno/análogos & derivados , Ressonância Magnética Nuclear Biomolecular , Oxirredução , Peru , Extratos Vegetais/química , Folhas de Planta/química , Esqualeno/químicaRESUMO
In addition to the free protein amino acid l-tyrosine, the expanding young leaves of Inga laurina accumulate high concentrations of three new depsides, galloyl, m-digalloyl, and m-trigalloyl l-tyrosine (1, 2, and 3). The structures of these compounds were determined on the basis of their spectroscopic properties and through degradation and derivatization experiments. They occur in young leaves at the following dry-weight mass percentages: tyrosine, 10.4%; 1, 3.1%; 2, 5.0%; 3, 1.3%. These concentrations are most consistent with chemical defense during the vulnerable expansion stage of leaf development. Neither free tyrosine nor its galloyl depsides are present in mature leaves.
Assuntos
Depsídeos/isolamento & purificação , Fabaceae/química , Ácido Gálico/análogos & derivados , Ácido Gálico/isolamento & purificação , Depsídeos/química , Ácido Gálico/química , Estrutura Molecular , Panamá , Folhas de Planta/química , Tirosina/análiseRESUMO
Young leaves of most species experience remarkably higher herbivore attack rates than mature leaves. Considerable theoretical effort has focused on predicting optimal defense and tradeoffs in defense allocation during leaf expansion. Among others, allocation to secondary chemistry may be dependent on growth constraints. We studied flavanoid production during leaf development in two species of Inga (Fabaceae: Mimosoideae) with different expansion strategies: Inga goldmanii, a species with slowly expanding young leaves, and Inga umbellifera, a species with fast-expanding young leaves. In these two species, the most abundant and toxic class of defensive compounds is flavanoids (which include tannins). We measured their concentration by leaf dry weight, their total content per leaf, their HPLC chemical profile and their toxicity to a generalist herbivore at different expansion levels. Although in both species the flavanoid concentration decreased with increasing leaf expansion, that decrease was twice as pronounced for I. umbellifera as it was for I. goldmanii. I. umbellifera leaves produced flavanoids only during the first half of their development while I. goldmanii leaves continued production throughout. The changes in flavanoid HPLC profiles and toxicity were also more dramatic for I. umbellifera, which had different flavanoids in young than in mature leaves. Relative to I. umbellifera, I. goldmanii showed smaller changes in both flavanoid composition and toxicity in the transition from young to mature leaves. These results indicate that, even though young leaves suffer higher rates of attack and are predicted to have better chemical defenses than mature leaves, growth constraints may modulate defense allocation and thus, evolution of defense strategies.
Assuntos
Adaptação Fisiológica , Fabaceae/crescimento & desenvolvimento , Fabaceae/metabolismo , Flavonoides/análise , Folhas de Planta/crescimento & desenvolvimento , Fatores Etários , Animais , Cromatografia Líquida de Alta Pressão , Flavonoides/toxicidade , Mariposas/efeitos dos fármacos , Panamá , Folhas de Planta/química , Análise de Componente Principal , Especificidade da Espécie , Testes de Toxicidade , Clima TropicalRESUMO
The leaves of tropical forest trees are most likely to suffer herbivore damage during the period of expansion. Herbivore selection on young leaves has given rise to a variety of leaf developmental strategies and age-specific chemical defense modes. We are studying correlations between leaf developmental types and chemical defenses in the Neotropical genus Inga. We have characterized defense metabolites in Inga goldmanii and Inga umbellifera, two species that co-occur in the lowland moist forest of Panama. These congeners have markedly different young-leaf developmental phenotypes but suffer approximately equal rates of herbivory. Bioassays of whole and fractionated leaf extracts using larvae of Heliothis virescens show that I. goldmanii chemical defenses are nearly three times more inhibitory than those of I. umbellifera. In both species, most of the inhibitory activity resides in complex mixtures of monomeric and polymeric flavan-3-ols. This group comprises >30% of young leaf dry weight in both I. goldmanii and I. umbellifera. The species' phenolic chemistry differs markedly, however, both in the structure of the monomeric units and in the distribution of polymer sizes. The differences in chemical structure have pronounced effects on their bioactivities, with I. goldmanii flavans being twice as inhibitory to H. virescens larvae as I. umbellifera flavans, and more than three times more efficient at protein binding. Given the extraordinarily high polyphenol concentrations that are found in the young leaves of these species, protein precipitation could be an important mechanism of growth inhibition. Nevertheless, our data show that another mode of phenolic action, possibly oxidative stress, occurs simultaneously.