Leaf functional traits and insular colonization: Subtropical islands as a melting pot of trait diversity in a widespread plant lineage

Abstract

Aim: One of the main goals of functional biogeography is to examine distribution patterns of trait diversity, and islands provide excellent study cases for this emerging field. We tested the hypothesis that multiple dispersals from a common mainland pool would promote functional similarity among island systems when environmental conditions are similar, but also novel phenotypic traits related to colonization history and exploitation of new habitats. Location: Mediterranean Basin and Macaronesian islands. Taxon: Wolfbane (Periploca laevigata) Methods: We used the well-known biogeographical history of a woody plant complex (P. laevigata s.l.) to examine trait variation and how it relates to climatic conditions of mainland and subtropical island settings. In a common garden experiment, we measured a suite of leaf physiological and anatomical traits tightly related to plant performance in 320 seedlings representing 21 populations of five sublineages-the oldest (2.6 my) island colonization (western Canary Islands) as a reference, three sublineages stemming from independent events of island colonization in the last 0.5 my from NW Africa (Cape Verde, Fuerteventura, Lanzarote) and their widespread Mediterranean mainland counterpart. Results: We observed strong phenotypic divergence between island and mainland sublineages linked to contrasting climatic conditions. Mediterranean mainland populations displayed a very specialized leaf phenotype characteristic of arid plants (i.e. small leaves, amphistomaty, isobilateral mesophyll, high photosynthetic rates). In turn, low seasonality on islands was linked to the recurrent expression of a phenotype characterized by larger leaves and lower photosynthetic rates. Our analyses showed that the high investment in secondary compounds (i.e. tannins) on islands decouples photosynthesis from growth rates. Despite this pattern of parallel differentiation, each island sublineage displayed a distinctive phenotype, with some traits related to colonization time, which resulted in a mosaic of functional variation across island systems. Main conclusions: Our data suggest that the studied subtropical islands promote expression of traits specific to certain sublineages and other common traits that are no longer adaptive in the original mainland pool due to Pleistocene climatic shifts. These | 2363 GARCÍA-VERDUGO Et Al.

Climatic niche pre-adaptation in mainland Europe facilitated the colonization of Madeira by ivies (Hedera L., Araliaceae)

“…To our knowledge, this is the first evidence that explicitly supports mainland pre-adaptation in a Macaronesian plant lineage, which is not totally surprising given that most of the populations of H. iberica occur in mainland Iberian locations that have been frequently considered as climatically and floristically related to Macaronesia (Rutherford 1989;Costa et al 1997;Calleja et al 2009). However, this mainland preadaptation contrasts with previous findings that show phenotypic divergence between sister plant lineages in Macaronesian islands and the mainland suggesting adaptive pressures for in situ evolution (García-Verdugo et al 2019;García-Verdugo et al 2020). Future research will examine the prevalence of this evolutionary pattern in single-species island endemics, and particularly in Macaronesian ivies.…”

Phylogeography at the crossroad: Pleistocene range expansion throughout the Mediterranean and back‐colonization from the Canary Islands in the legume Bituminaria bituminosa

“…Phylogenetic evidence broadly supports the idea of syndrome‐driven diversification in non‐sclerophyllous plant lineages at local scales since the onset of the Mediterranean climate (Verdú & Pausas, 2013). The results from our literature review add another layer of complexity to this observation: Pleistocene conditions may have also favoured wide geographical expansion of species with functional traits shaped by the Mediterranean climate itself (e.g., García‐Verdugo et al, 2020). However, this pattern is probably restricted to species with high colonization abilities, which may overcome the deleterious effects of rapid range expansion on adaptive evolution (discussed in González‐Martínez et al, 2017).…”

“…Traits refer to the following character states: SH = shrub versus PH = tree/woody climber; FD = deciduous, semi‐deciduous or facultative deciduous versus EV = evergreen sclerophylls; LL = large‐leaved (typically >5 cm long or >5 cm 2 in size) versus SL = small leaved. (a) Bello (2015), (b) Viruel et al (2020), (c) Coello et al (2020), (d) Fernández‐Mazuecos and Vargas (2010), (e) Désamoré et al (2011), (f) Rodríguez‐Sánchez et al (2009), (g) Kondraskov et al (2015), (h) Migliore et al (2012), (i) Besnard et al (2013), (j) García‐Verdugo et al (unpublished data), (k) Mateu‐Andrés et al (2015); (l) García‐Verdugo et al (2015, 2020), (m) Vendramin et al (2008), (n) Saladin et al (2017), (o) Vitelli et al (2017), (p) Mateu‐Andrés et al (2013), (q) Chen et al (2014) and (r) Grassi et al (2006).…”

Sticking around: plant persistence strategies on edaphic islands

“…The study of plant functional traits in insular systems has boosted in recent years, providing important insights into the eco-evolutionary dynamics of these systems (e.g. Biddick et al, 2019;Biddick & Burns, 2021;García-Verdugo et al, 2020;Negoita et al, 2016;Schrader et al, 2021;Spasojevic et al, 2014;Taylor et al, 2019).…”

“…The study of plant functional traits in insular systems has boosted in recent years, providing important insights into the eco-evolutionary dynamics of these systems (e.g. Biddick et al, 2019; Biddick & Burns, 2021; García-Verdugo et al, 2020; Negoita et al, 2016; Schrader et al, 2021; Spasojevic et al, 2014; Taylor et al, 2019). Yet, most of this research targeted dispersal and resource acquisition traits, neglecting other important, non-acquisitive functions (but see Aikio et al, 2020), which are needed for better understanding how plant traits promote persistence and help avoid local extinction (Auffret et al, 2017).…”