Insular woody daisies (Argyranthemum, Asteraceae) are more resistant to drought‐induced hydraulic failure than their herbaceous relatives

Abstract

Abstract1. Insular woodiness refers to the evolutionary transition from herbaceousness towards derived woodiness on (sub)tropical islands and leads to island floras that have a higher proportion of woody species compared to floras of nearby continents. 4. Our results show that stems of insular woody daisies are more resistant to droughtinduced hydraulic failure than the stems of their herbaceous counterparts. The anatomical character that best predicts variation in embolism resistance is intervessel pit membrane thickness (T PM ), which can be functionally linked with air bubble dynamics throughout the 3D vessel network. There is also a strong link between T PM vs. degree of woodiness and thickness of the xylem fibre wall vs. embolism resistance, resulting in an indirect link between lignification and resistance to embolism formation.5. Thicker intervessel pit membranes in Argyranthemum functionally explain why this insular woody genus is more embolism resistant to drought-induced failure compared to the herbaceous relatives from which it has evolved, but additional data are needed to confirm that palaeoclimatic drought conditions have triggered wood formation in this daisy lineage. K E Y W O R D SCanary Islands, drought, hydraulic failure, insular woodiness, lignification, stem anatomy, thickness of intervessel pit membrane, xylem hydraulics

Parallel evolution of arborescent carrots (Daucus) in Macaronesia

“…To explain such habit shifts, Lens et al (2013b) hypothesized that derived woodiness evolved as a result of selection for greater air embolism resistance in the vascular system. This hypothesis has recently been supported by ecophysiological data on shrubby species of Argyranthemum from the dry lowlands of the Canary Islands (Dória et al, 2018). This explanation, however, is not plausible for the chamaephytic Daucinae, as none of the insular endemic species of this tribe is confined to dry coastal regions of the Macaronesian islands.…”

“…(2013b) and Dória et al. () considered drought adaptation to be the trigger because derived woody stems have higher embolism resistance than herbaceous relatives. Each of those hypotheses has its limitations; moreover, they are not mutually exclusive.…”

“…Both phenomena, and especially insular woodiness, have been extensively discussed since the 19th century, and numerous hypotheses have been proposed to explain them (e.g., Darwin, 1859;Wallace, 1878;Carlquist, 1974). Darwin suggested increased competition between herbaceous species favoring taller individuals; Carlquist (1974) postulated that moderate climates with low seasonality and/or the absence of large herbivores may be responsible for the shift; and recently, Lens et al (2013b) and Dória et al (2018) considered drought adaptation to be the trigger because derived woody stems have higher embolism resistance than herbaceous relatives. Each of those hypotheses has its limitations; moreover, they are not mutually exclusive.…”

Multiple origins of insular woodiness on the Canary Islands are consistent with palaeoclimatic aridification

“…Secondly, increased resistance of stems to drought-induced embolism inside water conducting cells, a trait that is associated with drier habitats and survival during drought (Lens, Tixier et al, 2013;Anderegg et al, 2016;Choat et al, 2018), seems correlated to increased woodiness. This is based on water transport measurements in stems comparing herbs and their derived woody relatives in Arabidopsis (Lens, Tixier et al, 2013) and Canary Island Asteraceae (Dória et al, 2018), as well as positive correlations between embolism stress resistance and stem lignification in herbaceous Canary Island Brassicaceae (Dória et al, 2019) and across grasses (Lens et al, 2016).…”

Tracing insular woodiness in giant Daucus (s.l.) fruit fossils from the Early Pleistocene of Madeira Island (Portugal)

“…Originally coined as "insular woodiness" by Sherwin Carlquist (Carlquist, 1974), various hypotheses have been proposed to explain the phenomenon and to account for the radical shift in life-form and traits entailed. These were recently reviewed (see Dulin & Kirchoff, 2010;Lens & al., 2013) and include: (i) competition among species resulting in advantageous gigantism; (ii) promotion of plant fitness through shift to perennial habit; (iii) yearround growth enabled by the buffered oceanic climate; (iv) lack of predation by large herbivores permitting perennial growth; and recently, (v) resistance to drought-induced embolism through the development of secondary wood (Dulin & Kirchoff, 2010;Dória & al., 2018).…”