ResearchPlant chemical defense evolution across scales Fig 1. Environmental gradients determine adaptation through traits relevant to resistance against herbivores in Pinus pinaster. Genetic structure and admixture of pine populations, reflecting gene flow, along a resource gradient (A). Populations from high-resource sites showed greater growth (B), invested more in constitutive defenses (C) and were more resistant to herbivory (D), after accounting for neutral genetic variation of populations from SNP data.
Although there is strong evidence that plant defense adaptively responds to the environment, it is unclear what is the relative contribution of abiotic and biotic factors in determining plant defense evolution. Classic plant defense hypotheses posit that plant species adapted to resource-rich environments typically invest in greater growth and lower defenses, and those adapted to resource-poor environments should invest in lower growth and greater defenses due to differences in replacement costs of tissue lost from herbivores in those habitats. Although these patterns have generally been observed between species over the decades, inferences from intraspecific patterns have been less clear. We propose a conceptual framework to evaluate how biotic drivers, their interaction with abiotic factors, and the role of gene flow between populations shape plant local adaptation (López-Goldar and Agrawal, 2021). Empirically, we combine extensive chemical analysis, genomic data and statistical simulations to elucidate how plant-herbivore interactions are shaped through genetically-based adaptive variation in plant defenses and herbivory along environmental gradients. At large geographical scales, we found in maritime pine (Pinus pinaster), a socioeconomically important European conifer species, that populations from resource-rich environments invested more in growth and constitutive defenses, leading to greater resistance to herbivory through greater investment in specific defensive compounds (López-Goldar et al. 2018, López-Goldar et al. 2019, López-Goldar et al. 2020) (Fig. 1). At finer geographical scales, we found in common milkweed (Asclepias syriaca) that toxin- and tissue-specific evolution of plant defense can occur across nearby populations, likely due to heterogeneous selective pressures by herbivores and where the influence of abiotic conditions were lower compared to larger scales (López-Goldar and Agrawal, 2023).
On the other hand, multiple hypotheses have also been formulated to explain why individual plants produce so many chemical compounds. Nonetheless, the few evidence available have led to heterogeneous outcomes likely because the mode of action of most compounds is unknown, the underlying adaptations of insects to cope with most plant toxins remains unresolved, and teasing apart concentration vs composition of toxins from plant tissues is daunting. In our recent work, we leveraged in vitro and in vivo approaches developed over 10 years with a real herbivore, their cellular machinery, and transgenic fruit flies with the herbivore’ adaptations, and purified plant toxins in isolation or in mixtures using equimolar concentrations. We show that plant chemical diversity enhances defense against herbivory by impacting multiple physiological mechanisms (López-Goldar et al. 2024) (Fig. 2).
Our findings challenge the expected patterns of classic hypotheses and suggest that the adaptive significance of plant defense may differ across scales of biological organization because of distinct evolutionary processes operating in each of them (i.e., from molecular, to individuals, to populations).
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