Heritable plant phenotypes track light and herbivory levels at fine spatial scales

Abstract

Organismal phenotypes often co-vary with environmental variables across broad geographic ranges. Less is known about the extent to which phenotypes match local conditions when multiple biotic and abiotic stressors vary at fine spatial scales. Bittercress (Brassicaceae: Cardamine cordifolia), a perennial forb, grows across a microgeographic mosaic of two contrasting herbivory regimes: high herbivory in meadows (sun habitats) and low herbivory in deeply shaded forest understories (shade habitats). We tested for local phenotypic differentiation in plant size, leaf morphology, and anti-herbivore defense (realized resistance and defensive chemicals, i.e., glucosinolates) across this habitat mosaic through reciprocal transplant-common garden experiments with clonally propagated rhizomes. We found habitat-specific divergence in morphological and defensive phenotypes that manifested as contrasting responses to growth in shade common gardens: weak petiole elongation and attenuated defenses in populations from shade habitats, and strong petiole elongation and elevated defenses in populations from sun habitats. These divergent phenotypes are generally consistent with reciprocal local adaptation: plants from shade habitats that naturally experience low herbivory show reduced investment in defense and an attenuated shade avoidance response, owing to its ineffectiveness within forest understories. By contrast, plants from sun habitats with high herbivory show shade-induced elongation, but no evidence of attenuated defenses canonically associated with elongation in shade-intolerant plant species. Finally, we observed differences in flowering phenology between habitat types that could potentially contribute to inter-habitat divergence by reducing gene flow. This study illuminates how clonally heritable plant phenotypes track a fine-grained mosaic of herbivore pressure and light availability in a native plant.

Variable effects on growth and defense traits for plant ecotypic differentiation and phenotypic plasticity along elevation gradients

“…In other words, we could imagine a scenario in which energy‐saving plasticity of induction has evolved in response to variable herbivory pressure (i.e. optimal defense hypothesis Zangerl and Rutledge ()) (Agrawal et al, ; Humphrey et al, ; Wagner & Mitchell‐Olds, ), and it has been retained during range expansion toward higher elevations. Therefore, plasticity in defense‐related traits is a reflection of both biotic and abiotic environmental conditions that affect the expression of defenses.…”

“…We calculated larval weight gain using the formula ln (final weight − initial weight) For P. major , larval weight gain was averaged across the two caterpillars on each plant. Lower weight gains indicate that plants are more resistant (Humphrey et al, ).…”

From plants to herbivores: novel insights into the ecological and evolutionary consequences of plant variation

“…Performing reciprocal transplant experiments in the field and manipulating the conditions in a greenhouse experiment they provide evidence for adaptive micro-geographic divergence and for heritable differences in the response to shading. The defense phenotypes track the parental habitats, with elevated defenses in plants from open habitats where herbivore pressures are high (Humphrey et al 2018).…”

“…Humphrey et al (2018) investigate how local adaptation to certain abiotic and biotic conditions proceeds at a fine-grained spatial (micro-)scale. Performing reciprocal transplant experiments in the field and manipulating the conditions in a greenhouse experiment they provide evidence for adaptive micro-geographic divergence and for heritable differences in the response to shading.…”

“…The studies of this special topic cover a broad range of plant life forms, from marine algae in an aquatic system (Ledet et al 2018) to terrestrial herbs (Calf et al 2018;Chiriboga et al 2018;Cuny et al 2018;Howard et al 2018;Humphrey et al 2018;Kergunteuil et al 2018;Quintero and Bowers 2018), to shrubs (Nell et al 2018;Ochoa-López et al 2018), to long-lived trees (Albrectsen et al 2018;Bagchi et al 2018;Cipollini and Peterson 2018;Coley et al 2018;Falk et al 2018;Lämke and Unsicker 2018). In twelve case studies and four review papers, selected aspects of the huge variation in phenomena and underlying mechanisms are highlighted and new research questions opened, which may inspire further research in this exciting field.…”