Extraordinary and rapid evolution of chemical defenses in the Neotropical legume genus Inga Mill.
Francisco J. Velásquez-Puentes, PhD student
German Centre for Integrative Biodiversity Research, iDiv, & Leipzig University, Germany
Universidad del Norte, Barranquilla, Colombia
Unlike animals, legumes and other plants cannot run away from their natural enemies when attacked. As a result, they have evolved an impressive array of physical and chemical defense strategies to deter even the hungriest vegan enemies. Among those defenses, plant secondary metabolites, a plethora of diverse chemical compounds, stand out for deterring herbivores and pathogens. The diversity of secondary metabolites across legumes as a whole has been extensively documented over many decades, culminating in the Phytochemical Dictionary of the Leguminosae (Bisby et al. 1994), but the detailed evolutionary trajectories of legume defense chemicals remain poorly understood, especially at species level. Understanding the evolutionary processes and mechanisms involved in the evolution of novel plant defense compounds is important because natural enemies are detrimental for plant species survival, presenting strong selective pressures for evolution of chemical defenses, thereby potentially driving evolutionary diversification and community assembly, and facilitating species co-existence (Marquis et al. 2016).
In a recently published paper in the New Phytologist, Forrister et al. (2022) provide some answers to these fundamental questions using the legume genus Inga Mill., which has emerged as a model system for understanding rapid recent evolutionary radiation in Neotropical rain forests (e.g., Richardson et al. 2001; Nicholls et al. 2015). Forrister et al. assembled an impressive chemical dataset using metabolomics to characterize thousands of individual compounds from leaves of more than 800 individuals representing 97 species of Inga sampled across Neotropical rain forests in Brazil, Ecuador, French Guiana, Panama and Peru. Using a phylogeny based on targeted enrichment of >800 nuclear genes they deployed comparative phylogenetic methods to analyze the phytochemical and evolutionary uniqueness of chemical profiles across these 97 Inga species. What they found was striking. They showed that all species invest in structurally diverse chemical compounds, with an average of 194 distinct compounds per species, and 9,105 unique compounds across these 97 species of Inga. In addition to this spectacular chemical diversity, they found that chemical composition is more divergent between sister species occurring in sympatry than for those in parapatry, and more phylogenetically divergent than expected by chance, indicating that secondary metabolite composition is under strong selection pressure. Furthermore, given that the 250-300 species of Inga evolved in < 10 million years these diverse chemical compounds seem to have evolved extremely rapidly and multiple times, i.e., they are evolutionary extremely labile. This has resulted in a reduced set of shared pests and pathogens, which favors species co-existence due to reduced negative density dependence effects (Janzen 1970; Connell 1971; Chesson 2000; Kursar et al. 2009).
Inga species from left: flowers of Inga vera; young leaf of I. oerstediana showing extrafloral nectaries between leaflet pairs; inflorescences of I. jinicuil. Photos: Colin Hughes.
But how do those chemical defenses evolve so quickly? The authors suggest that instead of evolving gradually, chemical profiles have evolved under a model of divergent adaptation where transcriptional gene regulation coupled with “lego” chemistry (i.e., addition of chemical side groups in a combinatorial manner from a relatively small set of building blocks) provides the most plausible mechanism to explain the rapid evolution of novel combinations of metabolites and chemical structures. In other words, it seems that genes coding for the enzymes involved in the synthesis of those defenses do not necessarily evolve quickly, but the way those genes are expressed and how metabolites are subsequently assembled varies greatly among species. This model provides a possible explanation for the evolutionary fluidity required to escape from the diverse herbivore assemblages which are exerting disparate selective pressures on their hosts (Endara et al. 2017).
Neotropical rain forests include many species-rich tree clades, including legume groups like, Inga, Jupunba, Swartzia, Tachigali, and Zygia, several of which appear to have diversified rapidly and recently over the last few million years and which tend to be characterized by high levels of sympatry, i.e., species co-existence. What combinations of abiotic and biotic factors drove these episodes of hyperfast rain forest species diversification remains an open question. What Forrister et al. show in this elegant study, is that secondary plant chemistry is a key niche axis facilitating species co-existence and undoubtedly played an important role in the assembly of the impressive diversity of Inga species in rain forests.
Bisby, F.A., Buckingham, J. & Harborne, J. (Eds.) (1994) Phytochemical Dictionary of the Leguminosae. Chapman & Hall, London, U.K.
Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: 343–366.
Connell, J.H. (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and rain forest trees. In: den Boer, P.J. & Gradwell, G.R. (Eds.) Dynamics of Populations. Centre for Agricultural Publishing and Documentation. Wageningen. 298–312.
Endara, M.J., Coley, P.D., Ghabash, G., Nicholls, J.A., Dexter, K.G., Donoso, D.A., Stone, G.N., Pennington, R.T. & Kursar, T.A. (2017) Coevolutionary arms race versus host defence chase in a tropical herbivore–plant system. Proceedings of the National Academy of Sciences 114: E7499-E7505.
Forrister, D.L., Endara, M., Soule, A.J., Younkin, G.C., Mills, A.G., Lokvam, J., Dexter, K.G., Pennington, R.T., Kidner, C.A., Nicholls, J.A., Loiseau, O., Kursar, T.A. & Coley, P.D. (2022) Diversity and divergence: Evolution of secondary metabolism in the tropical tree genus Inga. New Phytologist 237: 631-642. https://doi.org/10.1111/nph.18554
Janzen, D.H. (1970) Herbivores and the number of tree species in tropical forests. The American Naturalist 104: 501–528.
Kursar, T.A., Dexter, K. G., Lokvam, J., Pennington, R.T., Richardson, J.E., Weber, M.G., Murakami, E.T., Drake, C., McGregor, R. & Coley, P.D. (2009) The evolution of anti-herbivore defences and their contribution to species coexistence in the tropical tree genus Inga. Proceedings of the National Academy of Sciences 106: 18073–18078.
Marquis, R.J., Salazar, D., Baer, C., Reinhardt, J., Priest, G. & Barnett, K. (2016) Ode to Ehrlich and Raven or how herbivorous insects might drive plant speciation. Ecology 97: 2939–2951.
Nicholls, J.A., Pennington, R.T., Koenen, E.J.M., Hughes, C.E., Hearn, J., Bunnefeld, L., Dexter, K.G., Stone, G.N. & Kidner, C.A. (2015) Using targeted enrichment of nuclear genes to increase phylogenetic resolution in the neotropical rain forest genus Inga (Leguminosae: Mimosoideae). Frontiers in Plant Science 6. https://doi.org/10.3389/fpls.2015.00710
Richardson, J.E., Pennington, R.T., Pennington, T.D. & Hollingsworth, P.M. (2001) Rapid diversifica- tion of a species-rich genus of Neotropical rain forest trees. Science 293: 2242–2245.