The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga

Abstract

Plants and their herbivores constitute more than half of the organisms in tropical forests. Therefore, a better understanding of the evolution of plant defenses against their herbivores may be central for our understanding of tropical biodiversity. Here, we address the evolution of antiherbivore defenses and their possible contribution to coexistence in the Neotropical tree genus Inga (Fabaceae). Inga has >300 species, has radiated recently, and is frequently one of the most diverse and abundant genera at a given site. For 37 species from Panama and Peru we characterized developmental, ant, and chemical defenses against herbivores. We found extensive variation in defenses, but little evidence of phylogenetic signal. Furthermore, in a multivariate analysis, developmental, ant, and chemical defenses varied independently (were orthogonal) and appear to have evolved independently of each other. Our results are consistent with strong selection for divergent defensive traits, presumably mediated by herbivores. In an analysis of community assembly, we found that Inga species co-occurring as neighbors are more different in antiherbivore defenses than random, suggesting that possessing a rare defense phenotype increases fitness. These results imply that interactions with herbivores may be an important axis of niche differentiation that permits the coexistence of many species of Inga within a single site. Interactions between plants and their herbivores likely play a key role in the generation and maintenance of the conspicuously high plant diversity in the tropics.

Fig. 1.

Young leaves of I. poeppigiana being damaged by a hemipteran (Left; photo by Robyn Burnham) and young leaves of I. thibaudiana with extrafloral nectaries being visited by the ant Ectatomma (Right; photo by Tania Brenes-Arguedes).

Fig. 2.

The rate of expansion of young leaves expressed as the percentage increase in area per day (% per day) versus the chlorophyll content (mg·m⁻²) for Inga species from Panama (n = 11) and Peru (n = 23). For all species combined, there is a significant negative relationship [exp = 971 × (chl^−0.68); r² = 0.50, P < 0.0001]. The dotted diagonal line separates species into two equal-sized groups designated as defense and escape.

Fig. 3.

Phylogenetic tree (Left; 50% majority rule consensus tree from Bayesian analysis of 6,000 bps of plastid DNA) and chemistry dendrogram (Right) for Inga species. Thickened branches on the phylogeny represent >0.95 posterior probability for the adjacent node. The chemistry dendrogram was generated by using hierarchical clustering of presence/absence data for 13 defense chemicals (phenolics and saponins, weighted equally). Thickened branches are adjacent to nodes with P < 0.1 according to multiscale bootstrapping analysis (approximately >90% bootstrap support; see SI Text). Species in bold are classified as defense (see Fig. 2), and other species are classified as escape. Gray species are unclassified because of lack of data.

Fig. 4.

Phylogenetic and defense trait dispersion for Inga communities in Peru and Panama. Phylogenetic results are for one, randomly selected Bayesian tree. Values given are the inverse of the net relatedness index (NRI) and nearest taxon index (NTI) following Webb (41). Values > 0 indicate overdispersion, and values < 0 indicate underdispersion. The departure of communities from the null expectation (zero) of communities being randomly assembled was evaluated by using two-sided t tests for phylogenetic dispersion and one-sided t tests for defense trait dispersion (*, P < 0.05; **, P < 0.01; ***, P < 0.001).