The soiil mosaic hypothesis: a synthesis of multi-trophic diversification via soil heterogeneity

Abstract

Myriad unexplored mechanisms potentially drive ecological speciation and could help explain global variation in diversity. Here, we develop a novel hypothesis focused on variation in biotic, chemical, and physical properties of soil as a factor contributing to diversification in communities of plants and animals. The Soil Mosaic Hypothesis (SMH) suggests that differences in soil attributes can affect intraspecific variation in phytochemistry, leading to cascading ecological and evolutionary effects on higher trophic levels. To illustrate the potential importance of the SMH, we examine three underlying ideas: (1) plant species and species assemblages shift over time, exposing them to novel soil environments, which can lead to genetic differentiation; (2) differences in soil properties can alter phytochemistry via plasticity and local adaptation; (3) phytochemistry can drive herbivore diversification via divergent natural selection (i.e. ecological speciation). The SMH provides insight into the process of diversification in a variety of landscapes and at a variety of scales and may inform analyses of diversification at local, regional, and global scales.

Patterns of Plumericin Concentration in Leaves of Himatanthus tarapotensis (Apocynaceae) and Its Interactions with Herbivory in the Peruvian Amazon

“…Plant chemistry is in part a function of soil chemistry (i.e., soil nutrients) on the phytochemical landscape [20]. Soil attributes (i.e., chemical and physical factors) can alter secondary metabolites via plasticity and local adaptation of plants across the soil mosaic on the landscape [21]. For example, in the phytochemical landscape, differences among habitats in soil nutrient availability can shape the genetic architecture of plant populations and the molecular machinery by which plants take up nutrients from soils [20].…”

“…The phytochemical landscape hypothesis integrates the mentioned approaches and posits that variation in nutrient availability in soil and variation in trophic interactions (e.g., plant-insect interaction) determine intraspecific variation in plant chemistry across spatial and temporal environmental gradients [20]. The soil mosaic hypothesis [21] mentions that intraspecific variation in plant chemistry is the effect of differences in soil properties (i.e., biotic, chemical, and physical factors), yielding a highly variable phytochemical landscape [20] and leading to cascading ecological and evolutionary effects on higher trophic levels (e.g., herbivores). Plant species and communities are exposed to diverse soil environments across multiple spatial and temporal scales, which can alter the production of metabolites via plasticity and local adaptation, and even lead to divergences in plant populations.…”

“…Plant species and communities are exposed to diverse soil environments across multiple spatial and temporal scales, which can alter the production of metabolites via plasticity and local adaptation, and even lead to divergences in plant populations. Moreover, this variation in phytochemistry can drive herbivore diversification via ecological speciation at fine geographic scales [21]. These relationships could be particularly evident in regions with extreme habitat differences (e.g., white-sand soil forests versus clay soil forests in lowland Amazon).…”

“…Thus, resource availability of the soil (e.g., poor nutrient white-sand soil forests versus rich nutrient clay soil forests) determines levels, patterns, and types of chemical production in plants, as well as the nature of the plant-insect herbivores interactions [1,2,20,21]. Moreover, insect herbivores promote the production of specialized toxic substances for plant defense [10,11,[22][23][24].…”

“…H. tarapotensis grows in two types of forests with floristic and edaphic differences, and which are under a permanent attack of insect herbivores feeding on its leaves: white-sand soil forests (WS) poor in nutrients surrounded by more fertile clay, and soil forests (CS) mixed with brown sand. The mosaic distribution of these habitats creates a natural system where the chemistry of plants would be affected by the environmental gradients caused by the soil differences (e.g., differences in soil fertility and insect herbivore community) [2,11,20,21].…”