Phylogenetic correlations among chemical and physical plant defenses change with ontogeny

Abstract

SummaryTheory predicts patterns of defense across taxa based on notions of tradeoffs and synergism among defensive traits when plants and herbivores coevolve. Because the expression of characters changes ontogenetically, the evolution of plant strategies may be best understood by considering multiple traits along a trajectory of plant development.Here we addressed the ontogenetic expression of chemical and physical defenses in 12 Datura species, and tested for macroevolutionary correlations between defensive traits using phylogenetic analyses. We used liquid chromatography coupled to mass spectrometry to identify the toxic tropane alkaloids of Datura, and also estimated leaf trichome density.We report three major patterns. First, we found different ontogenetic trajectories of alkaloids and leaf trichomes, with alkaloids increasing in concentration at the reproductive stage, whereas trichomes were much more variable across species. Second, the dominant alkaloids and leaf trichomes showed correlated evolution, with positive and negative associations. Third, the correlations between defensive traits changed across ontogeny, with significant relationships only occurring during the juvenile phase.The patterns in expression of defensive traits in the genus Datura are suggestive of adaptation to complex selective environments varying in space and time.

Macroevolutionary patterns of glucosinolate defense and tests of defense‐escalation and resource availability hypotheses

“…Lack of conservatism in chemical defense could result from multiple nonexclusive sources of variation, including abiotic factors or inducibility (Kim & Jander, ; Himanen et al ., ), or conflicting selection for different compounds imposed by specialist/generalist herbivores or conspecific/heterospecific competitors (Kliebenstein et al ., ; Lankau & Strauss, ; Müller, ) across habitats. That said, studies using common‐garden approaches also find low to moderate phylogenetic signal in secondary compounds (Agrawal et al ., ; Johnson et al ., ; Karinho‐Betancourt et al ., ), and for a subset of our data ( n = 15) we found a significant, moderate correlation between total glucosinolates measured in the field and in the glasshouse. Oenothera 's flavonoids (Johnson et al ., ), Quercus ’ tannins (Pearse & Hipp, ), Inga ’ s phenolics (Kursar et al ., ), Datura 's alkaloids (Karinho‐Betancourt et al ., ), and Bursera 's terpenes (Becerra et al ., ) also have weak phylogenetic signal.…”

Changes in cytokinins are sufficient to alter developmental patterns of defense metabolites in Nicotiana attenuata

“…Using a second approach with a DEX‐inducible construct (i‐ov IPT ), we created short‐term perturbations of the within‐plant ontogenic gradients of CKs and observed the consequences for defense allocations to different tissues that followed the disturbances. CKs were shown to regulate the accumulation of specific defense metabolites in many different plant species (Smigocki et al ., ; Dervinis et al ., ; Schäfer et al ., 2015a) and we see similar distribution of CKs (Hewett and Wareing, ; Ori et al ., ) and defense metabolites (James, ; Kariñho‐Betancourt et al ., ). Therefore we assume that the correlation between CK levels and defense metabolite accumulations is a general phenomenon.…”

Future directions in the ontogeny of plant defence: understanding the evolutionary causes and consequences

“…For example for the Datura clade, leaf pubescence has been associated with arid habitats, and glabrous leaves with more temperate or sub‐tropical regions (Karinho‐Betancourt et al . ), but ontogenetic changes in this trait as a function of the environment have not been investigated in this context.…”